Social play experience in juvenile rats is indispensable for appropriate socio-sexual behavior in adulthood in males but not females
Open accessAbstract
Social play is a dynamic and rewarding behavior abundantly expressed by most mammals during the juvenile period. While its exact function is debated, various rodent studies on the effects of juvenile social isolation suggest that participating in play is essential to appropriate behavior and reproductive success in adulthood. However, the vast majority of these studies were conducted in one sex only, a critical concern given the fact that there are known sex differences in play’s expression: across nearly all species that play, males play more frequently and intensely than females, and there are qualitative sex differences in play patterns. Further limiting our understanding of the importance of play is the use of total isolation to prevent interactions with other juveniles. Here, we employed a novel cage design to specifically prevent play in rats while allowing for other forms of social interaction. We find that play deprivation during the juvenile period results in enduring sex-specific effects on later-life behavior, primarily in males. Males prevented from playing as juveniles exhibited decreased sexual behavior, hypersociability, and increased aggressiveness in adulthood, with no effects on these measures in females. Importantly, play deprivation had no effect on anxiety-like behavior, object memory, sex preference, or social recognition in either sex, showing the specificity of the identified impairments, though there were overall sex differences in many of these measures. Additionally, acute play deprivation impaired performance on a test of prosocial behavior in both sexes, indicating a difference in the motivation and/or ability to acquire this empathy-driven task. Together, these findings provide novel insight into the importance and function of juvenile social play and how this differs in males and females.
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Written from the paper’s full text.
TL;DR
Juvenile play deprivation in rats produced enduring sex-specific socio-sexual impairments, primarily in males, while females were largely unaffected across the behavioral battery. Males deprived of play showed reduced copulatory behavior, hypersociability in the short-duration study, and increased aggression, with no effects on anxiety-like behavior, object memory, sex preference, or social recognition in either sex.
Key findings
- Play deprivation impaired adult male sexual behavior: in the short-duration barrier (SDB) study, average mount rate was significantly reduced (p = 0.014; BARR vs. CTRL p = 0.03, ISO vs. CTRL p = 0.005); in the long-duration barrier (LDB) study, average mounts (p = 0.029) and intromissions (p = 0.016) were reduced, and only ~60% of BARR and ISO males ejaculated in one or both tests versus ~90% expected for controls (BARR p = 0.002, ISO p < 0.001; CTRL non-ejaculators 12.5%).
- In SDB, male BARR animals showed hypersociability, with higher social preference than all other groups (p < 0.001; Cohen’s d 1.9–2.9 for pairwise comparisons), but there was no condition effect in LDB. In LDB resident-intruder testing, total aggressive behaviors differed by condition (p = 0.016), with ISO males higher than CTRL (p = 0.005) and BARR males trending higher (p = 0.056).
- Factor analysis identified a socio-sexual behavior factor affected by condition in both SDB (p = 0.044) and LDB (p = 0.03), with BARR males scoring higher than CTRL males (SDB p = 0.019; LDB p = 0.008).
- Play deprivation had no effect on anxiety-like behavior, object memory, sex preference, or social recognition in either sex; acute play deprivation increased latency to release a cagemate on days 1–6 in both sexes (p = 0.027) but not days 7–12.
Methods
- Sprague-Dawley rats of both sexes (196 total) were weaned on P21 into same-sex sibling pairs. SDB animals were placed from P26–40 into control, BARR (perforated Plexiglass divider preventing play while allowing visual, olfactory, auditory, and tactile contact), or ISO (single-housed full isolation) conditions; LDB animals were placed in the same conditions from P21–45. Animals were then returned to standard group housing around puberty.
- Behavioral battery included social play (P28), open field (P33 or P59), elevated plus maze (P47), novel object recognition (P60), female and male sex behavior (P63/P70), social preference, sex preference, social recognition (P100+), resident-intruder aggression (P120+), and empathy/prosocial helping behavior (P27–38).
- Analyses used two-way ANOVA with sex and juvenile housing condition, post hoc Tukey or Fisher’s LSD tests, nonparametric tests when data were non-normal, one-sample t-tests versus chance, paired t-tests, and factor analysis with varimax rotation conducted separately for SDB and LDB on male data.
Limitations
- The paper states that BARR animals were also deprived of other tactile non-play social interactions such as social grooming, and that differences in physical space between BARR versus CTRL and ISO conditions may affect development. It also notes that female resilience may not hold for all traits or may reflect latent differences not detectable by the paradigms used, and that factor analysis was conducted only on male data because female data were insufficiently correlated.
- Evident from the text: some key effects were trending rather than significant (e.g., BARR vs. CTRL total aggression p = 0.056; LDB mount rate p = 0.151), and the empathy/prosocial helping test had small group sizes (n = 4–5 per group).
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Cites
Statistics
Claims the paper makes
23 of 66 cited sources checked · 17 supported · 0 flagged · accuracy not yet measured
- Findingcitation
The reduction in the percentage of animals successfully ejaculating was similar to that seen in males in which both the androgen receptor and estrogen receptor alpha were genetically deleted.
“the reduction in the percentage of animals which successfully ejaculated we observed was similar to that seen in males in which both the androgen receptor and estrogen receptor alpha were genetically deleted (Trouillet et al., 2022).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Trouillet et al., 2022 source
- Interpretationcitation
The impairments in male copulatory behavior following play deprivation were close to the magnitude seen in other studies in which male copulatory behavior is altered by more substantial pharmacological or genetic manipulations.
“Remarkably, these impairments were close to the magnitude seen in other studies in which male copulatory behavior is altered by more substantial pharmacological or genetic manipulations”
Quote in the paperNot a substantial claim1 of 2 sources checked- cites Amateau and McCarthy, 2004 source
- cites Trouillet et al., 2022 source
The Results section, under “Double neural AR and ERα knockout severely impaired male sexual behavior in mice” (page unavailable), reports substantial changes in male mating behavior after a genetic manipulation. The paper does not examine play deprivation or compare its effects with the knockout effects, so it cannot establish the claimed similarity in magnitude. (LLM, conf=0.82)
Experimental — accuracy not yet measured
- Interpretationcitation
The convergence of evidence from this study and others using different manipulations points to play experience being the critical driver of the impairments observed.
“Nevertheless, the convergence of evidence from our study and others using different manipulations (e.g., reducing play by rearing juveniles with an adult or a peer from a less playful strain) points to play experience being the critical driver of the impairments observed (Schneider et al., 2016; Burleson et al., 2016; Pellis et al., 2017; Stark and Pellis, 2020, 2021).”
Quote in the paperSubstantial claim2 of 3 sources checked - Premisecitation
A study in females found that isolation from P19-70 also decreases sociability.
“This finding was mirrored by a study in females which found that isolation from P19–70 also decreases sociability (Hermes et al., 2011).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Hermes et al., 2011 source
- Findingown data
Acute play deprivation has no effect on anxiety-like behavior as evidenced by center time in an open field test.
“Acute play deprivation has no effect on anxiety-like behavior as evidenced by center time in an open field test”
Quote in the paperNot a substantial claim
- Findingown data
The ability and motivation to engage in play is maintained in BARR and ISO animals of both sexes compared to historical control data.
“additionally, the ability and motivation to engage in play is maintained (C, showing the intact play in BARR and ISO animals of both sexes compared to historical control data, with timeline of experiment shown above graph).”
Quote in the paperSubstantial claim - Findingown data
Males prevented from playing as juveniles exhibited increased aggressiveness in adulthood.
“Males prevented from playing as juveniles exhibited decreased sexual behavior, hypersociability, and increased aggressiveness in adulthood, with no effects on these measures in females.”
Quote in the paperSubstantial claim - Findingown data
Males across the three conditions exhibited more anxiety-like behavior, spending significantly less time in the center of the open field arena than females (p < 0.001).
“we found that males across the three conditions exhibited more anxiety-like behavior, as they spent significantly less time in the center of the open field arena than females (p < 0.001; Figure 2E).”
Quote in the paperNot a substantial claim - Findingown data
Males prevented from playing as juveniles exhibited decreased sexual behavior in adulthood.
“Males prevented from playing as juveniles exhibited decreased sexual behavior, hypersociability, and increased aggressiveness in adulthood, with no effects on these measures in females.”
Quote in the paperSubstantial claim - Findingown data
Performance on the novel object recognition task suggested intact object memory within the 1 h retention interval, as evidenced by a discrimination ratio significantly different from chance (DR = 0) for all six groups.
“The performance of animals in both the SDB and LDB studies on this task suggested intact object memory within our retention interval (1 h), as evidenced by a discrimination ratio (DR) significantly different from chance (DR = 0; Figures 3A,B) for all six groups.”
Quote in the paperNot a substantial claim - Findingown data
Acute play deprivation impaired performance on a test of prosocial behavior in both sexes.
“Additionally, acute play deprivation impaired performance on a test of prosocial behavior in both sexes, indicating a difference in the motivation and/or ability to acquire this empathy-driven task.”
Quote in the paperNot a substantial claim - Findingown data
Males prevented from playing as juveniles exhibited hypersociability in adulthood.
“Males prevented from playing as juveniles exhibited decreased sexual behavior, hypersociability, and increased aggressiveness in adulthood, with no effects on these measures in females.”
Quote in the paperSubstantial claim - Findingown data
In contrast to females, there was a significant impairment in sexual behavior in adult males prevented from playing as juveniles.
“In contrast to females, there was a significant impairment in sexual behavior in adult males prevented from playing as juveniles.”
Quote in the paperSubstantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
- Findingown data
BARR animals of both sexes were significantly more active in the elevated plus maze than both CTRL (p < 0.001) and ISO (p = 0.003) animals.
“Post hoc analysis indicated that BARR animals of both sexes were significantly more active in the maze than both CTRL (p < 0.001) and ISO (p = 0.003) animals.”
Quote in the paperNot a substantial claim - Findingown data
The mean difference in play levels between female BARR and ISO animals (12.7 vs. 29.0 play events) is much larger than that of male BARR and ISO animals (28.6 vs. 31.9 play events).
“the mean difference in play levels between female BARR and ISO animals (12.7 vs. 29.0 play events) is much larger than that of male BARR and ISO animals (28.6 vs. 31.9 play events).”
Quote in the paperSubstantial claim - Findingown data
In both the SDB and LDB studies, there was no effect of housing condition on time in the open arms of the elevated plus maze.
“In both the SDB and LDB studies, we found no effect of housing condition on time in the open arms (Figures 2A,C).”
Quote in the paperNot a substantial claim - Findingown data
Play deprivation during the juvenile period results in enduring sex-specific effects on later-life behavior, primarily in males.
“We find that play deprivation during the juvenile period results in enduring sex-specific effects on later-life behavior, primarily in males.”
Quote in the paperSubstantial claim - Findingown data
There was an increase in hyperactivity in animals deprived of play.
“Additionally, we observed an increase in hyperactivity in animals deprived of play (Figure 2F).”
Quote in the paperNot a substantial claim - Findingown data
In the LDB animals, CTRL males did not show a significant difference from the expected distribution of ejaculators vs. non-ejaculators.
“In the LDB animals, CTRL males also did not show a significant difference (Figure 5H).”
Quote in the paperSubstantial claim - Findingown data
In both the SDB and LDB studies, all six groups demonstrated significant social preference compared to chance (50%), exhibiting a much higher percentage of time interacting closely with the social stimulus box compared to the empty stimulus box.
“In both the SDB and LDB studies, all six groups demonstrated significant social preference compared to chance (50%), exhibiting a much higher percentage of time interacting closely with the social stimulus box compared to the empty stimulus box.”
Quote in the paperNot a substantial claim - Findingown data
Males prevented from playing as juveniles exhibited altered sexual behavior, sociability, and aggressive behavior.
“as males prevented from playing as juveniles exhibited altered sexual behavior, sociability, and aggressive behavior.”
Quote in the paperSubstantial claim - Findingown data
Male BARR animals had a significantly higher social preference compared to all other groups, including male CTRL (p < 0.001) and male ISO (p < 0.001) animals.
“Post hoc analysis indicated that male BARR animals had a significantly higher social preference compared to all other groups, including male CTRL (p < 0.001) and male ISO (p < 0.001) animals.”
Quote in the paperSubstantial claim - Findingown data
There was a significant main effect of condition on the Socio-sexual Behavior factor in both the SDB (p = 0.044) and LDB (p = 0.03) animals.
“Most notably, we also detected a significant main effect of condition on the Socio-sexual Behavior factor in both the SDB (p = 0.044) and LDB (p = 0.03) animals.”
Quote in the paperSubstantial claim - Findingown data
In the SDB animals, the distribution of ejaculators vs. non-ejaculators did not significantly differ from the expected distribution across any of the three groups.
“In the SDB animals, the distribution of ejaculators vs. non-ejaculators did not significantly differ from the expected distribution across any of the three groups (Figure 5D).”
Quote in the paperNot a substantial claim - Findingown data
In the LDB study, the third factor (16.9% of total variance) contained positive loadings for sex preference and social preference and negative loading for sex behavior mount rate.
“Similar to the SDB study, the third factor (16.9% of total variance; hence titled “Socio-sexual behavior”) contained loadings for various socio-sexual behaviors: positive loadings for sex preference and social preference and negative loading for sex behavior mount rate.”
Quote in the paperNot a substantial claim - Findingown data
In the SDB study, post hoc analysis detected a significant difference between CTRL animals and both play-deprived groups on the Salience factor (BARR: p = 0.029; ISO: p = 0.015), with CTRL males exhibiting higher positive scores than both play-deprived groups.
“Post hoc analysis detected a significant difference between CTRL animals and those deprived of play on this factor (BARR: p = 0.029; ISO: p = 0.015), with CTRL males exhibiting higher positive scores on this Salience factor than both play-deprived groups.”
Quote in the paperNot a substantial claim - Findingown data
The paper reports persistent alterations in the expression of various adult behaviors following juvenile play deprivation in rats.
“Here, we report persistent alterations in the expression of various adult behaviors following juvenile play deprivation in rats.”
Quote in the paperSubstantial claim - Findingown data
In the SDB animals, both BARR (p = 0.03) and ISO (p = 0.005) males had a significantly lower mount rate than their CTRL counterparts.
“Post hoc analysis of data from the SDB animals revealed both BARR (p = 0.03) and ISO (p = 0.005) males had a significantly lower mount rate than their CTRL counterparts.”
Quote in the paperSubstantial claim - Findingown data
In the SDB study, the first factor (31.3% of total variance) contained positive loadings for distance traveled and percent of time in the open arms of the elevated plus maze, with negative loading for social recognition.
“The first factor (31.3% of total variance) contained positive loadings for distance traveled and percent of the time in the open arms of the elevated plus maze, with negative loading for social recognition.”
Quote in the paperNot a substantial claim - Findingown data
In both the SDB and LDB studies, female data was deemed insufficiently correlated and therefore inadequate for factor analysis based on Kaiser-Meyer-Olkin MSA below 0.5 for both studies and Bartlett's sphericity p > 0.05.
“In both the SDB and LDB studies, female data was deemed insufficiently correlated and therefore inadequate for factor analysis based on these indices (Kaiser-Meyer-Olkin MSA below 0.5 for both studies; Bartlett’s sphericity p > 0.05).”
Quote in the paperSubstantial claim - Findingown data
No significant differences were observed for the Anxiety-related factors in either the SDB or the LDB study.
“No significant differences were observed for the Anxiety-related factors in either the SDB or the LDB study.”
Quote in the paperNot a substantial claim - Findingown data
No effects were observed in females on any other test in the diverse battery conducted.
“we observed no effects in females on any other test in the diverse battery we conducted.”
Quote in the paperSubstantial claim - Findingown data
There was a significant main effect of condition on the average number of total aggressive behaviors exhibited across the two resident intruder tests (p = 0.016).
“Summing these behaviors together, we calculated the average number of total aggressive behaviors exhibited by subjects across the two tests (Figure 9E) and observed a significant main effect of condition on this measure (p = 0.016).”
Quote in the paperNot a substantial claim - Findingown data
Males prevented from playing for as little as 3.5 weeks (in the LDB study) exhibited deficits in ejaculation.
“Furthermore, males prevented from playing for as little as 3.5 weeks (in the LDB study) also exhibited deficits in ejaculation.”
Quote in the paperSubstantial claim - Findingown data
There was no effect of juvenile housing condition on later-life social recognition.
“However, there was no effect of juvenile housing condition, indicating play deprivation has no effect on later-life social recognition.”
Quote in the paperNot a substantial claim - Findingown data
In the SDB animals, there was a significant effect of condition on the Salience factor (p = 0.034).
“However, in the SDB animals, there was a significant effect of condition on the Salience factor (p = 0.034).”
Quote in the paperNot a substantial claim - Findingown data
Play deprivation induces hypersociability in adulthood.
“We also found that play deprivation induces hypersociability in adulthood.”
Quote in the paperSubstantial claim - Findingown data
Play deprivation has a lasting effect on male sexual behavior.
“the most striking of our findings is the lasting effect of play deprivation on male sexual behavior.”
Quote in the paperSubstantial claim - Findingown data
In the SDB study, the third factor (15.9% of total variance) contained positive loadings for sex behavior mount rate and social preference.
“Finally, the third factor (15.9% of total variance) contained positive loadings for sex behavior mount rate and social preference”
Quote in the paperNot a substantial claim - Findingown data
Animals deprived of play exhibited significantly longer latencies to free their cagemates on the first six days of the task compared to controls (p = 0.027).
“Animals deprived of play exhibited significantly longer latencies to free their cagemates on the first six days of the task compared to controls (p = 0.027; Figure 10C).”
Quote in the paperNot a substantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
- Findingown data
In both the SDB and LDB studies, the female data were insufficiently correlated and therefore inappropriate for factor analysis, based on Kaiser-Meyer-Olkin Measure of Sampling Adequacy below 0.5 and Bartlett's sphericity test p-value above 0.05.
“Consequently, we conducted these analyses on only the male data, as the female data in both the SDB and LDB studies was deemed insufficiently correlated and therefore inappropriate for factor analysis based on the Kaiser-Meyer-Olkin Measure of Sampling Adequacy (MSA; below 0.5 for both studies) and Bartlett’s sphericity test (p-value above 0.05 for both studies).”
Quote in the paperSubstantial claim - Findingown data
In the SDB study, there was a significant sex by condition interaction on the percent of time spent near the social stimulus box (p < 0.001).
“In the SDB study, we additionally observed a significant sex × condition interaction on the percent of time spent near the social stimulus box (p < 0.001; Figure 6A; ratio data and representative traces shown in Figure 6B).”
Quote in the paperNot a substantial claim - Findingown data
Males prevented from playing for as little as 2 weeks (in the SDB study) showed a significant reduction in mount rate across two tests of sexual behavior.
“Males prevented from playing for as little as 2 weeks (in the SDB study) showed a significant reduction in mount rate across two tests of sexual behavior.”
Quote in the paperSubstantial claim - Findingcitation
The decrease in the number of mounts observed was of similar magnitude to that seen in males treated with a cyclooxygenase-2 inhibitor for 2 weeks during the perinatal sensitive period.
“the decrease in the number of mounts we observed was of similar magnitude to that seen in males treated with a cyclooxygenase-2 inhibitor for 2 weeks during the perinatal sensitive period (Amateau and McCarthy, 2004)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Amateau and McCarthy, 2004 source
- Findingown data
The impairment in the prosocial motivation task was resolved by the latter half of testing, with the performance of play-deprived animals improving to that seen in controls on days 7-12 of the paradigm.
“This impairment was resolved by the latter half of testing, with the performance of play-deprived animals improving to that seen in controls on days 7–12 of the paradigm.”
Quote in the paperNot a substantial claim - Findingown data
In the SDB study, BARR males exhibited social preference that was significantly higher than that seen in all other groups.
“In the SDB study, BARR males exhibited social preference that was significantly higher than that seen in all other groups.”
Quote in the paperSubstantial claim - Findingown data
No effects of play deprivation were seen on any other assessed behavior, with the exception of a small but significant effect on locomotion shortly after animals were returned to standard group housing.
“Importantly, we saw no effects of play deprivation on any other assessed behavior, with the exception of a small but significant effect on locomotion shortly after animals were returned to standard group housing.”
Quote in the paperSubstantial claim - Findingown data
Females appeared largely resilient to play deprivation across the myriad of behavioral assays conducted.
“while females appeared largely resilient to play deprivation across the myriad of behavioral assays we conducted”
Quote in the paperSubstantial claim - Findingown data
There was no effect on social preference in the LDB animals.
“However, there was no effect on social preference in the LDB animals.”
Quote in the paperNot a substantial claim - Findingown data
BARR animals of both sexes performed worse on the prosocial motivation task, taking significantly longer to free their distressed cagemate from a confinement box on the first 6 days of testing.
“BARR animals of both sexes performed worse on this task, taking significantly longer to free their distressed cagemate from a confinement box on the first 6 days of testing.”
Quote in the paperNot a substantial claim - Interpretationown data
Acute play deprivation indicates a difference in the motivation and/or ability to acquire the empathy-driven prosocial behavior task.
“Additionally, acute play deprivation impaired performance on a test of prosocial behavior in both sexes, indicating a difference in the motivation and/or ability to acquire this empathy-driven task.”
Quote in the paperSubstantial claim - Premisecitation
Juvenile social isolation in rats leads to impairments in social behavior.
“juvenile social isolation in rats leads to impairments in social behavior (Hol et al., 1999; Van den Berg et al., 1999; Von Frijtag et al., 2002)”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationown data
Together, the factor analyses suggest that socio-sexual behavior is a distinct category of later-life behavior specifically sensitive to play deprivation in juvenile males.
“Together, these analyses suggest that socio-sexual behavior is a distinct category of later-life behavior specifically sensitive to play deprivation in juvenile males.”
Quote in the paperSubstantial claim - Interpretationown data
In females, play is more dispensable.
“In females, however, play is more dispensable.”
Quote in the paperSubstantial claim - Interpretationown data
The decreased interaction time appeared to represent true social recognition rather than an artifact of repeated testing, as there was no difference in interaction time between Train and Test trials for any of the six SDB or LDB groups in a control experiment with a novel stimulus animal in both trials.
“This decreased interaction time appeared to represent true social recognition, as opposed to an artifactual decrease as a result of being assessed in a second consecutive test, as there was no difference in interaction time between the Train and Test trials for any of the six SDB or LDB groups in a control experiment in which subjects received a novel stimulus animal in both trials (Supplementary”
Quote in the paperSubstantial claim - Interpretationown data
The vast majority of the observed effects of play deprivation were seen in males but not females.
“a choice supported by the fact that the vast majority of our observed effects of play deprivation were seen in males but not females.”
Quote in the paperSubstantial claim - Interpretationown data
Juvenile play deprivation significantly increased aggressiveness in adulthood.
“demonstrating that juvenile play deprivation significantly increased aggressiveness in adulthood.”
Quote in the paperSubstantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
- Interpretationown data
Social play experience is critical for the development of appropriate socio-sexual behavior in males.
“We demonstrate that social play experience is critical for the development of appropriate socio-sexual behavior in males”
Quote in the paperSubstantial claim - Premisecitation
The period from P26 to P40 encompasses the peak of the window in which social play is maximally expressed.
“the peak of the window in which social play is maximally expressed (Panksepp, 1981)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Panksepp, 1981 source
- Premisecitation
The expected distribution for control animals is 90% ejaculators and 10% non-ejaculators/duds.
“the expected distribution (90% ejaculators, 10% non-ejaculators/“duds”)”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationown data
The LDB first two factors appeared to reflect a latent anxiety-like phenotype, separating based on the specific anxiety-like behavior test in question.
“The first two factors appeared to reflect a latent anxiety-like phenotype, separating based on the specific anxiety-like behavior test in question.”
Quote in the paperNot a substantial claim - Interpretationown data
The female resilience supports the hypothesis that the purpose of play differs across the sexes, at least in the rat.
“Regardless, this female resilience is notable, supporting our hypothesis that the purpose of play differs across the sexes, at least in the rat.”
Quote in the paperSubstantial claim - Interpretationown data
This suggests that play itself is the critical feature driving the motivation to play in males.
“suggesting that play itself is the critical feature driving the motivation to play in males.”
Quote in the paperSubstantial claim - Premisecitation
Isolation across the full window from P22-35 also decreased sociability.
“Isolation across the full window, from P22–35, also decreased sociability.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hol et al. (1999) source
- Classified as probably not a substantial claim. 63
- May combine two claims. 60
- The quote only partly states this claim. 1
Classified as probably not a substantial claim.
PremisecitationInteraction with a conspecific across a similar physical barrier has been shown to be socially rewarding.
“Interaction with a conspecific across a similar physical barrier has been shown to be socially rewarding (Peartree et al., 2012)”
Quote in the paperSubstantial claim1 of 1 sources checked- cites Peartree et al., 2012 source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationJuvenile social isolation in rats leads to impairments in cognition.
“cognition (Einon et al., 1978; Baarendse et al., 2013; Yusufishaq and Rosenkranz, 2013)”
Quote in the paperNot a substantial claim2 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationStudies investigating neural underpinnings of this behavioral sex difference have identified various nodes within the larger circuitry of social behavior, including the medial amygdala and lateral septum, which exert sex-specific influences on play following sexual differentiation early in life as part of typical brain development.
“Studies investigating the neural underpinnings of this behavioral sex difference have identified various nodes within the larger circuitry of social behavior, including the medial amygdala (VanRyzin et al., 2019) and lateral septum (Bredewold et al., 2014), which exert sex-specific influences on play following sexual differentiation early in life as part of typical brain development.”
Quote in the paperNot a substantial claim2 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationDeficits in play are core symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia.
“Indeed, deficits in play are core symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia (Alessandri, 1992; Jones et al., 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005)”
Quote in the paperNot a substantial claim1 of 3 sources checked- cites Alessandri, 1992 source
- cites Jones et al., 1994 source
- cites Møller and Husby, 2000 source
The Behavioral Dimensions section identifies school or work impairment, shifts in interests, and social withdrawal as potential features of the schizophrenia prodrome, but does not identify deficits in play. Searches for play, childhood play, early-onset schizophrenia, autism, and ADHD found no passage addressing the attributed claim. The available passages have no page numbers. (LLM, conf=0.73)
Experimental — accuracy not yet measured
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationMany neurodevelopmental disorders also exhibit robust sex differences in diagnosis and symptomology.
“many of which also exhibit robust sex differences in diagnosis and symptomology (Aleman et al., 2003; Ramtekkar et al., 2010; Arnett et al., 2015; Halladay et al., 2015; Giordano et al., 2021; Prosperi et al., 2021).”
Quote in the paperNot a substantial claim1 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationJuvenile social isolation in rats impacts susceptibility to addiction-related behaviors.
“impacts susceptibility to addiction-related behaviors (Whitaker et al., 2013; Baarendse et al., 2014)”
Quote in the paperNot a substantial claim2 of 2 sources checkedMay combine two claims.
PremisecitationIsolation prevents all social interaction-both play and non-play-so it is unclear whether identified impairments are due to lack of play vs. lack of general social interaction, as well as additional stress that total isolation induces.
“First, isolation prevents all social interaction—both play and non-play—so it is unclear in most of these studies whether and to what extent any identified impairments are due to the lack of play vs. the lack of general social interaction, as well as the additional stress that total isolation induces (Begni et al., 2020).”
Quote in the paperSubstantial claim1 of 1 sources checked- cites Begni et al., 2020 source
The Discussion reports that deprivation of social contacts impairs neuroplasticity in rats, supporting the claim that isolation removes social contact and can produce impairments. The paper does not distinguish lack of play from lack of other social interaction as causes of those impairments. It also does not establish that total isolation adds stress in these animals; the Discussion reports no altered wellbeing from isolation housing itself and describes resocialization as a temporary stressor. The indexed passages have section labels but no page numbers. (LLM, conf=0.83)
Experimental — accuracy not yet measured
May combine two claims.
Findingown dataThe ability and motivation to participate in play was intact in BARR and ISO animals and was increased relative to historical data for control-housed animals.
“we found that the ability and motivation to participate in play was not only intact in BARR and ISO animals but was increased relative to our historical data for control-housed animals (Figure 1C; Argue and McCarthy, 2015).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Argue and McCarthy, 2015 source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationInteraction with a conspecific across a similar physical barrier reduces anxiety-like behavior as compared to full isolation.
“and to reduce anxiety-like behavior as compared to full isolation, an additional benefit (Klapper-Goldstein et al., 2020).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Klapper-Goldstein et al., 2020 source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationRecent work in Drosophila identified a transcriptional regulator believed to govern this same effect, suppressing aggression in a social experience-dependent manner.
“Indeed, recent work in Drosophila identified a transcriptional regulator believed to govern this same effect, suppressing aggression in a social experience-dependent manner (Ishii et al., 2022)”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Ishii et al., 2022 source
Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).
PremisecitationIndependently assessing males and females and noting a sex difference if an effect is observed in one sex but not the other is a common misconception of the appropriate way to assess sex differences.
“This was as opposed to independently assessing males and females and noting a sex difference if we observed an effect in one sex but not the other, a common misconception of the appropriate way to assess sex differences (Garcia-Sifuentes and Maney, 2021).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Garcia-Sifuentes and Maney, 2021 source
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationThese regions have distinct roles in socio-sexual behavior in adulthood, often driven by distinct, separable cell type-specific and projection-specific mechanisms.
“These regions have distinct roles in socio-sexual behavior in adulthood as well, often driven by distinct, separable cell type-specific and projection-specific mechanisms (Unger et al., 2015; Wong et al., 2016; Ishii et al., 2017; Kohl et al., 2018).”
Quote in the paperNot a substantial claim2 of 3 sources checked- cites Unger et al., 2015 source
The Discussion section (“Global versus modular control of complex social behaviors”; page unavailable) reports that aromatase-positive neurons in the medial amygdala regulate aggression but not sexual behavior, supporting a separable, cell-type-specific role. It does not establish the projection-specific mechanisms also attributed to this source. (LLM, conf=0.86)
Experimental — accuracy not yet measured - cites Wong et al., 2016 source
- cites Ishii et al., 2017 source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationIsolation starting later in adolescence, from P28-70, produced hypersociability in both sexes in mice.
“In contrast, isolation starting later in adolescence, from P28–70, was shown to produce hypersociability in both sexes, although this study was conducted in mice (Rivera-Irizarry et al., 2020).”
Quote in the paperNot a substantial claim1 of 1 sources checked- cites Rivera-Irizarry et al., 2020 source
May combine two claims.
PremisecitationPlay is itself a social behavior and involves the activity of many regions in the social circuitry, such as the medial amygdala, lateral septum, and hypothalamus.
“given play is itself a social behavior and involves the activity of many regions in the social circuitry, such as the medial amygdala, lateral septum, and hypothalamus (summarized in Siviy, 2016 and VanRyzin et al., 2020a).”
Quote in the paperSubstantial claim1 of 2 sources checked- cites Siviy, 2016 source
The Introduction describes social rough-and-tumble play in rats, while noting that human play can also be solitary. The Subcortical involvement section links play to activity in the medial amygdala and hypothalamus, and reports that a lateral septal infusion changes play in rats; it does not establish play-related neural activity in the lateral septum. The claim therefore overgeneralizes both the social nature of play and the evidence for activity in every listed region (page numbers unavailable). (LLM, conf=0.85)
Experimental — accuracy not yet measured - cites VanRyzin et al., 2020a
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
Findingown dataThere was no effect of sex or housing condition on the discrimination ratio, indicating no difference in object memory.
“However, there was no effect of sex or housing condition on the discrimination ratio, indicating no difference in object memory.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThere was a significant reduction in the average mount rate in the SDB animals (p = 0.014), which was also trending in the LDB animals (p = 0.151).
“This resulted in a significant reduction in the average mount rate (the total number of mounts, intromissions, and ejaculations divided by the active time) in the SDB animals (p = 0.014; Figure 5C) which was also trending in the LDB animals (p = 0.151; Figure 5G).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataThe sex by condition interaction on play did not reach statistical significance (p = 0.13).
“Although the sex × condition interaction did not reach statistical significance (p = 0.13)”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataEven in naturally cycling conditions, there was no effect of play deprivation on either sexual receptivity or proceptivity.
“Even in naturally cycling conditions, we again observed no effect of play deprivation on either sexual receptivity or proceptivity (Figures 4C,D).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThere was a significant main effect of sex on distance traveled in the maze in both studies (SDB: p = 0.034; LDB: p = 0.005), with males exploring the maze significantly less than females.
“we observed a significant main effect of sex in the distance traveled in the maze in both studies (SDB: p = 0.034; LDB: p = 0.005; Figures 2B,D), with males exploring the maze significantly less than females.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataFemales across conditions were more locomotive on the open field test than males.
“As before, females across conditions were also more locomotive on this test than males.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThere were either significant or trending effects on the average number of mounts (SDB: p = 0.075; LDB: p = 0.029) and the average number of intromissions (SDB: p = 0.13; LDB: p = 0.016) in both the SDB and LDB animals, with BARR and ISO males exhibiting an often stepwise decrease in the numbers of both sexual behaviors compared to CTRL males.
“We observed either significant or trending effects on the average number of mounts (SDB: p = 0.075; LDB: p = 0.029; Figures 5A,E) and the average number of intromissions (SDB: p = 0.13; LDB: p = 0.016; Figures 5B,F) in both the SDB and LDB animals, with BARR and ISO males exhibiting an often stepwise decrease in the numbers of both sexual behaviors compared to CTRL males.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThere was no effect of sex or housing condition on center time in the open field in juvenile rats.
“We found no effect of sex or housing condition on center time in the open field (Figure 1B).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingown dataThere was a small but significant sex difference in the LDB animals and a trending effect in the SDB animals (p = 0.007 and 0.097, respectively), whereby males spent significantly less time in the open arms of the maze.
“we observed a small but significant sex difference in the LDB animals with a trending effect in the SDB animals (p = 0.007 and 0.097, respectively) whereby males spent significantly less time in the open arms of the maze.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataFemales prevented from playing as juveniles exhibited no effects on sexual behavior, sociability, or aggressiveness in adulthood.
“Males prevented from playing as juveniles exhibited decreased sexual behavior, hypersociability, and increased aggressiveness in adulthood, with no effects on these measures in females.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataIn the LDB animals, there was a main effect of condition (p < 0.001) on distance traveled in the elevated plus maze.
“In the LDB animals, we also observed a main effect of condition (p < 0.001) on distance traveled.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThere was a significant main effect of sex and treatment on play data, with males of both housing conditions and ISO animals of both sexes playing significantly more than females and BARR animals, respectively.
“we detected a significant main effect of both sex (p = 0.036) and treatment (p = 0.026), with males of both housing conditions and ISO animals of both sexes playing significantly more than females and BARR animals, respectively.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThere was no effect of juvenile housing condition on female sexual behavior, with no differences in receptivity (lordosis quotient) or proceptivity (number of proceptive behaviors) across groups.
“We observed no effect of juvenile housing condition on female sexual behavior, as there were no differences in receptivity (lordosis quotient, Figure 4A) or proceptivity (number of proceptive behaviors, Figure 4B) across groups.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataFollowing a significant main effect of both sex (p < 0.001) and condition (p = 0.013) on gridline crossings, CTRL animals of both sexes were significantly less locomotive than BARR animals (p = 0.01), with a trending effect when compared to ISO animals (p = 0.117).
“Post hoc analysis following a significant main effect of both sex (p < 0.001) and condition (p = 0.013) on the number of gridline crossings indicated that CTRL animals of both sexes were significantly less locomotive than BARR animals (p = 0.01), with a trending effect when compared to ISO animals as well (p = 0.117).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataIn the LDB animals, the distribution of ejaculators vs. non-ejaculators in BARR (p = 0.002) and ISO (p < 0.001) males significantly differed from the expected distribution, with only about 60% of animals ejaculating in one or both tests and about 40% being duds.
“However, the distribution of ejaculators vs. non-ejaculators in BARR (p = 0.002) and ISO (p < 0.001) males significantly differed from the expected distribution. In both groups, only ~60% of animals ejaculated in one or both tests, while ~40% were “duds”.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThere was a strong sex difference in the ratio of investigation duration, with males exhibiting ratios closer to 1, indicating less intact social recognition (SDB: p < 0.001; LDB: p < 0.001); this followed a sex difference in overall interaction times, whereby males spent much more time interacting with the stimulus animal across both trials than females did.
“Interestingly, we detected a strong sex difference in the ratio of investigation duration, with males exhibiting ratios closer to 1, indicating less intact social recognition (SDB: p < 0.001; LDB: p < 0.001; Figures 8B,D); this followed a sex difference we observed in the overall interaction times, whereby males spent much more time interacting with the stimulus animal across both trials than Fem”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThere were trending effects of condition on the average number of keep downs (p = 0.189), lateral threats (p = 0.13), and upright postures (p = 0.088), but no difference in the number of clinch attacks.
“We detected trending effects of condition on the average number of keep downs (p = 0.189; Figure 9A), lateral threats (p = 0.13; Figure 9B), and upright postures (p = 0.088; Figure 9C), but no difference in the number of clinch attacks (Figure 9D).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataUsing male data alone, datasets from both the SDB and LDB study indicated appropriateness for factor analysis, with an overall Kaiser-Meyer-Olkin MSA above 0.5 (SDB: MSA = 0.53; LDB: MSA = 0.53) and a significant p-value for Bartlett's test (SDB: p = 0.001; LDB: p < 0.001).
“Using male data alone, datasets from both the SDB and LDB study indicated appropriateness for factor analysis, with an overall Kaiser-Meyer-Olkin MSA above 0.5 (SDB: MSA = 0.53; LDB: MSA = 0.53) and a significant p-value for Bartlett’s test (SDB: p = 0.001; LDB: p < 0.001).”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataPost hoc analyses indicated BARR males had a significantly higher positive score for the Socio-sexual Behavior factor than CTRL males in both studies (SDB: p = 0.019; LDB: p = 0.008), with trending effects compared to ISO males (SDB: p = 0.059; LDB: p = 0.147).
“Post hoc analyses indicated BARR males had a significantly higher positive score for this factor than CTRL males in both studies (SDB: p = 0.019; LDB: p = 0.008), and there were trending effects when compared to ISO males in both studies as well (SDB: p = 0.059; LDB: p = 0.147).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataIn the SDB study, the second factor (19.3% of total variance) contained positive loadings for discrimination ratio on the novel object recognition task and sex behavior mount rate.
“The second factor (19.3% of total variance) contained positive loadings for discrimination ratio on the novel object recognition task and sex behavior mount rate”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataIn the LDB study, factor two (17.5% of total variance) contained strong positive loadings for distance traveled and open arm time on the elevated plus maze.
“while factor two (17.5% of total variance) contained strong positive loadings for distance traveled and open arm time on the elevated plus maze.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataRats of both sexes were hyperactive shortly after play deprivation and displayed impairments in a test of empathy motivation when acutely prevented from playing.
“While rats of both sexes were hyperactive shortly after play deprivation and displayed impairments in a test of empathy motivation when acutely prevented from playing”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe performance of play-deprived animals improved to control levels by the second half of testing, with no effect of condition on this measure on days 7-12 of the assay.
“The performance of play-deprived animals improved to control levels by the second half of testing, as there was no effect of condition on this measure on days 7–12 of the assay (Figure 10D).”
Quote in the paperNot a substantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Findingown dataFactor analysis generated a three-factor solution for both the SDB and LDB datasets, and this three-factor solution was again identified after removing low-communality variables.
“which generated a three-factor solution for both the SDB and LDB datasets.”
- Also stated in: § Statistical analysis · plain
“again identifying a three-factor solution for both datasets.”
Quote in the paperNot a substantial claim- Also stated in: § Statistical analysis · plain
May combine two claims.
Findingown dataIn both the SDB and LDB studies, all six groups demonstrated social recognition, as their interaction time on the Test trial was significantly decreased compared to the Train trial, with the exception of the Male BARR group in the SDB study, which was trending (p = 0.085).
“In both the SDB and LDB studies, all six groups demonstrated social recognition (Figures 8A,C), as their interaction time on the Test trial was significantly decreased compared to that of the Train trial, with the exception of the Male BARR group in the SDB study, which was trending (p = 0.085).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataIn the LDB study, factor one (23.6% of total variance) contained strong positive loadings for center time and line crossings in the open field test, with negative loading for novel object discrimination ratio.
“Factor one (23.6% of total variance) contained strong positive loadings for center time and line crossings in the open field test, with negative loading for novel object discrimination ratio”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataCTRL males exhibited significantly fewer total aggressive behaviors than ISO males (p = 0.005), with a trending effect when compared to BARR males (p = 0.056).
“Post hoc analysis indicated CTRL males exhibited significantly fewer total aggressive behaviors than ISO males (p = 0.005), with a trending effect when compared to BARR males (p = 0.056)”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataIn the LDB study, there was a small but significant (p = 0.003) sex difference in the percentage of time near the social box, with males showing increased social preference relative to females, but there was no effect of juvenile housing condition.
“However, while a small but significant (p = 0.003) sex difference in the percentage of time near the social box was detected in the LDB study (Figure 6C; ratio data shown in Figure 6D), with males showing increased social preference relative to females, there was no effect of juvenile housing condition.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThere was a sex difference in the prosocial helping task in both stages of testing, with males on average exhibiting significantly longer latencies to release their cagemates in the early stage (Days 1-6; p = 0.046) and a trending effect in the late stage (Days 7-12; p = 0.063).
“There was also a sex difference in this task in both stages of testing, with males on average exhibiting significantly longer latencies to release their cagemates in the early stage of testing (Days 1–6; p = 0.046) with a trending effect in the late stage of testing (Days 7–12; p = 0.063).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataIn the LDB study, three factors were sufficient to explain the data, accounting for 58% of the total variance.
“From this analysis, we again identified three factors to be sufficient to explain the data, accounting for 58% of the total variance (Figure 11C).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingown dataIn the SDB study, three factors were sufficient to explain the data, accounting for 66.5% of the total variance.
“We identified three factors to be sufficient to explain the data, accounting for 66.5% of the total variance (Figure 11A).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataAround 40% of BARR and ISO males did not ejaculate in either test of copulatory behavior, a significant deviation from CTRL males (12.5%) and from the expected distribution of non-ejaculators (~10%).
“Around 40% of BARR and ISO males did not ejaculate in either test of copulatory behavior, a significant deviation from what was seen in CTRL males (12.5%) and from the expected distribution of non-ejaculators (~10%) based on decades of research on male rat sexual behavior (Dewsbury, 1972; Pattij et al., 2005; Portillo et al., 2006).”
Quote in the paperSubstantial claim0 of 3 sources checkedMay combine two claims.
Findingown dataIn both the SDB and LDB studies, all six groups demonstrated significant opposite-sex preference compared to chance (50%), with the exception of the two BARR groups in the LDB study, in which the one-sample t-test vs. chance was trending (Male BARR: p = 0.075; Female BARR: p = 0.148).
“In both the SDB and LDB studies, all six groups demonstrated significant opposite-sex preference as compared to chance (50%), with the exception of the two BARR groups in the LDB study, in which the one-sample t-test vs. chance was trending (Male BARR: p = 0.075; Female BARR: p = 0.148).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataNo significant differences were detected as a result of condition on the percent of time spent near the opposite-sex stimulus box, indicating sex preference in adulthood is unaffected by juvenile play deprivation.
“However, no significant differences were detected as a result of condition on the percent of time spent near the opposite-sex stimulus box (Figures 7A,C), indicating sex preference in adulthood is unaffected by juvenile play deprivation.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThere were no sex differences on the percent time near the opposite-sex stimulus box in either the SDB or LDB animals, but a main effect of sex was detected when considering the ratio of time spent near the opposite sex compared to the same-sex stimulus box in the LDB animals but not the SDB animals, with males exhibiting stronger opposite-sex preference than females.
“While there were no sex differences on this measure in either the SDB or LDB animals, a main effect of sex was detected when considering the data as a ratio of the time spent near the opposite sex compared to the same-sex stimulus box in the LDB animals (Figure 7D) but not the SDB animals (Figure 7B), with males exhibiting stronger opposite-sex preference than females.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataThe additional non-play social experience provided by the BARR vs. the ISO housing condition is sufficient to decrease play motivation in females but not males.
“In our initial studies, we found that the additional non-play social experience provided by the BARR vs. the ISO housing condition is sufficient to decrease play motivation in females but not males (Figure 1C)”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataPlay deprivation had no effect on anxiety-like behavior, object memory, sex preference, and social recognition in both sexes, and on sex behavior and social preference in females.
“Our findings in which we observed play deprivation had no effect—on anxiety-like behavior, object memory, sex preference, and social recognition in both sexes and on sex behavior and social preference in females”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataJuvenile play deprivation increases aggressive behavior in adult males, not decreases as a straightforward interpretation of the play-as-practice theory would predict.
“We here provide further evidence against the play-as-practice theory, as we demonstrate that juvenile play deprivation increases aggressive behavior in adult males, not decreases as a straightforward interpretation of the theory would predict.”
Quote in the paperSubstantial claimMay combine two claims.
Findingown dataThe hypersocial phenotype was seen across multiple SDB cohorts, with a substantial effect size (Cohen's d ranging between 1.9 and 2.9 for all pairwise comparisons between Male BARR and the other groups for percent of time near the social box).
“This hypersocial phenotype was seen across multiple SDB cohorts, and the effect size was substantial (Cohen’s d ranging between 1.9 and 2.9 for all pairwise comparisons between Male BARR and the other groups for percent of time near the social box; Figure 6A).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataMales generally performed worse than females in the empathy assay, exhibiting a significantly higher latency to release their cagemate on average in the first half of testing.
“We also observed a sex difference in this assay: males generally performed worse than females, as they exhibited a significantly higher latency to release their cagemate on average in the first half of testing.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S4 (based).
Premisenone givenThe vast majority of studies on effects of juvenile social isolation were conducted in one sex only.
“the vast majority of these studies were conducted in one sex only”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim. May combine two claims.
PremisecitationThere are known sex differences in play's expression: across nearly all species that play, males play more frequently and intensely than females, and there are qualitative sex differences in play patterns.
“there are known sex differences in play’s expression: across nearly all species that play, males play more frequently and intensely than females, and there are qualitative sex differences in play patterns.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites VanRyzin et al., 2020a
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Pellis and Pellis, 1990, 1997
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSocial play is a dynamic and rewarding behavior abundantly expressed by most mammals during the juvenile period.
“Social play is a dynamic and rewarding behavior abundantly expressed by most mammals during the juvenile period.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Pellis and Pellis, 2009
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Classified as probably not a substantial claim. May combine two claims.
PremisecitationParticipating in play is essential to appropriate behavior and reproductive success in adulthood.
“While its exact function is debated, various rodent studies on the effects of juvenile social isolation suggest that participating in play is essential to appropriate behavior and reproductive success in adulthood.”
Quote in the paperSubstantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe position of objects within the arena and the order of object exposure was counterbalanced across groups.
“The position of objects within the arena and the order of object exposure was counterbalanced across groups.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationJuvenile social isolation in rats increases anxiety- and depression-like behavior.
“increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al., 1991; Arakawa, 2003; Leussis and Andersen, 2008; Lukkes et al., 2009; Cuesta et al., 2020)”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisereasoningIn many studies, animals were isolated through adulthood, when testing was conducted; it is unclear whether there may be an effect of acute isolation on observed phenotypes.
“Second, in many of these studies, animals were isolated through adulthood, when testing was conducted; as such, it is also unclear whether and to what extent there may be an effect of acute isolation on the observed phenotypes.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenAll behavioral tests were performed and scored offline by an experimenter blind to condition (at all times) and sex (when appropriate).
“Unless stated otherwise, all behavioral tests were performed and scored offline by an experimenter blind to condition (at all times) and sex (when appropriate).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductreasoningA control experiment was independently conducted for social recognition, with a novel stimulus rat in both Train and Test trials, to control for effects of a second interaction trial unrelated to recognition.
“Separately, a control experiment was independently conducted which followed the same procedure; however, a novel stimulus rat was placed in the cage with the test rat in both the Train trial and the Test trial, to control for any effects of a second interaction trial in general, unrelated to recognition of the stimulus animal or the lack thereof.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataThe increased social interaction allowed by the BARR housing condition is sufficient to reduce play motivation in females but not males.
“This suggests that the increased social interaction allowed by the BARR housing condition is sufficient to reduce play motivation in females but not males, an unexpected finding speaking to the differential role that play may serve in females compared to males.”
Quote in the paperSubstantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
Probably not a substantial claim: may not pass S3 (load-bearing).
Interpretationown dataThe effect of housing condition on play seems to be driven more strongly in females than in males.
“However, this effect of the condition seems to be driven more strongly in females than in males.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Interpretationown dataThe initial studies provide intriguing evidence in support of the idea that play may serve different purposes across the sexes.
“and provides intriguing evidence in support of the idea that play may serve different purposes across the sexes.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenCondition groups and sexes were balanced across multiple litters.
“Both male and female pups were used, with condition groups and sexes balanced across multiple litters.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Premisenone givenThe majority of these studies were conducted in only one sex-typically male subjects-preventing assessment of sex differences in identified impairments.
“Finally, and most notably, the majority of these studies were conducted in only one sex—typically, male subjects—thereby preventing the ability to assess whether there are sex differences in the identified impairments.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe position of the social chamber and the empty chamber within the arena was counterbalanced across groups.
“The position of the social chamber and the empty chamber within the arena was counterbalanced across groups.”
Quote in the paperNot a substantial claimMay combine two claims.
Study design and conductreasoningThe perforated Plexiglass cage divider prevents play while still allowing for other forms of social interaction in the visual, auditory, olfactory, and tactile domain.
“Improving upon the previous methodology, this manipulation prevents play while still allowing for other forms of social interaction in the visual, auditory, olfactory, and tactile domain.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S2 (checkable).
PremisereasoningUse of total isolation to prevent interactions with other juveniles limits understanding of the importance of play.
“Further limiting our understanding of the importance of play is the use of total isolation to prevent interactions with other juveniles.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe position of the chamber containing the male stimulus animal and the chamber containing the female stimulus animal within the arena was counterbalanced across groups.
“The position of the chamber containing the male stimulus animal and the chamber containing the female stimulus animal within the arena was counterbalanced across groups.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataThe modified housing used to prevent play does not in itself increase anxiety-like behavior or impair the ability to play if given the opportunity.
“Overall, these initial studies indicate that the modified housing used to prevent play does not in itself increase anxiety-like behavior or impair the ability to play if given the opportunity”
Quote in the paperSubstantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
Probably not a substantial claim: may not pass S3 (load-bearing).
Interpretationown dataThe SDB third factor was titled "Socio-sexual behavior" because it contained two tests within the socio-sexual domain.
“two tests within the socio-sexual domain (hence titled “Socio-sexual behavior”).”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationP45 is an age when rats of both sexes have typically entered puberty, at which point playfulness dramatically decreases.
“an age when rats of both sexes have typically entered puberty, at which point playfulness dramatically decreases (Meaney and Stewart, 1981; Panksepp, 1981).”
Quote in the paperSubstantial claim0 of 2 sources checkedMay combine two claims.
Interpretationown dataThe increased social preference in male BARR animals appeared to be a true difference in sociability not affected by differences in overall exploration time, as there was no effect of condition on the time spent near either stimulus box.
“This appeared to be a true difference in sociability not affected by differences in overall exploration time, as there was no effect of condition on the time spent near either stimulus box (Supplementary Figure 1A).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThe SDB first factor was interpreted as reflecting a latent anxiety-like phenotype and renamed "Anxiety".
“As these enriched behaviors generally reflected measures of a latent anxiety-like phenotype, we renamed it accordingly (“Anxiety”).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAround 10% of all sexually mature male rats are duds (sexually sluggish), meaning that they do not ejaculate in the course of a 20-30 min assay with a sexually receptive female.
“It is well known in the field of rodent sexual behavior that around 10% of all sexually mature male rats will be “duds” (otherwise known as “sexually sluggish”), meaning that they do not ejaculate in the course of a 20–30 min assay with a sexually receptive female (Dewsbury, 1972; Pattij et al., 2005; Portillo et al., 2006).”
Quote in the paperNot a substantial claim0 of 3 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThe LDB first two factors were renamed "Anxiety I" and "Anxiety II".
“As such, we renamed the factors as “Anxiety I” and “Anxiety II”, respectively.”
Quote in the paperNot a substantial claimMay combine two claims. The quote only partly states this claim.
Interpretationown dataThe effects of juvenile play deprivation are complex and pervasive, seen weeks to months after all animals were returned to group housing, and impact reproductively critical behaviors.
“These effects are complex and pervasive, seen weeks to months after all animals were returned to group housing, and impact reproductively critical behaviors.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThe SDB second factor was interpreted as reflecting recognition of the salience of a given stimulus and renamed "Salience".
“both phenotypes that require recognition of the salience of a given stimulus; thus, we renamed the factor as such (“Salience”).”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataJuvenile play deprivation impairs both the number/rate of sexual behaviors (SDB and LDB) and the proportion of animals which successfully ejaculate (LDB) in adult males.
“Together, these studies indicate that juvenile play deprivation impairs both the number/rate of sexual behaviors (SDB and LDB) and the proportion of animals which successfully ejaculate (LDB) in adult males, a notable finding given the paramount importance sexual behavior plays in reproductive fitness.”
Quote in the paperSubstantial claim- Rests on an assumption: The barrier (BARR) housing condition prevents social play while allowing other social interaction.
May combine two claims.
Interpretationown dataThe reduction in mount rate was seen in both BARR and ISO males, indicating that the lack of play, not the lack of social interaction writ large, was the critical driver of this impairment.
“This was seen in both BARR and ISO males, indicating that the lack of play, not the lack of social interaction writ large, was the critical driver of this impairment.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataThe impairment in male copulatory behavior did not seem to represent a simple delay in learning, but rather a persistent reduction in the rate of copulatory behavior, evident across both successive tests.
“Moreover, this impairment did not seem to represent a simple delay in the learning process, but rather a persistent reduction in the rate of copulatory behavior; while we present the data here as an average, the deficit in BARR and ISO males was evident across both successive tests.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Interpretationown dataThe LDB third factor was titled "Socio-sexual behavior".
“hence titled “Socio-sexual behavior””
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
InterpretationreasoningPerhaps in females, the significance of play is more so the social experience in general, and less so the experience of play itself.
“Perhaps in females, the significance of play is more so the social experience in general, and less so the experience of play itself.”
Quote in the paperNot a substantial claimMay combine two claims.
Interpretationown dataIt appears little social experience during the juvenile window is necessary for appropriate social development in females, given few impairments were observed following even full social isolation.
“Even then, it appears little social experience during the juvenile window is necessary for appropriate social development in females, given we observed few impairments following even full social isolation.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningBARR animals may perform worse on the empathy test due to a deficit in their perception of and/or responsiveness to the social signals generated by their distressed cagemate.
“In this view, BARR animals may perform worse on the empathy test due to a deficit in their perception of and/or responsiveness to the social signals generated by their distressed cagemate.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe "play-as-practice" theory argues that the individual behaviors constituting social play resemble adult agonistic behaviors because play serves as practice for later-life aggressive encounters.
“One of many theories regarding the function of social play is the “play-as-practice” theory, which argues that the individual behaviors constituting social play (e.g., pounces, pins, and boxing behaviors in rats) resemble adult agonistic behaviors for a reason: because play serves as practice for later-life aggressive encounters (Fagen, 1981; Smith, 1997).”
Quote in the paperNot a substantial claim0 of 2 sources checkedClassified as probably not a substantial claim.
PremisecitationReciprocity is a fundamental feature of social play.
“This reciprocity—necessitating monitoring one’s own actions and those of a partner, recognizing social signals indicating the partner’s responses and intentions, and adjusting one’s actions appropriately to maintain the back-and-forth of the play bout—is a fundamental feature of social play (Pellis and Pellis, 2017)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis and Pellis, 2017
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningIt is possible that no effect on sociability was observed in the LDB study because the play deprivation spanned across the two sensitive windows (from P21-45), canceling out any effects.
“In this view, it is possible we observed no effect on sociability in the LDB study as the play deprivation spanned across those windows (from P21–45), canceling out any effects.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningPlay experience may be fundamental to the developmental firing and wiring of individual cells and projections that establishes appropriate adult circuit organization.
“play experience may be fundamental to the developmental firing and wiring of individual cells and projections that establishes appropriate adult circuit organization.”
Quote in the paperNot a substantial claimMay combine two claims.
PremisecitationSocial isolation from P22-28, but not P29-35, decreases sociability in adulthood in male rats.
“Work from Hol et al. (1999) demonstrated that social isolation from P22–28, but not P29–35, decreases sociability in adulthood in male rats.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Hol et al. (1999) source
Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).
Interpretationown dataThis finding may serve as another example of the concept that play aids in developing the ability to appropriately sense and respond to social signals.
“This finding may serve as another example of the concept that play aids in developing the ability to appropriately sense and respond to social signals.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationLong-term post-weaning social isolation has been shown to induce qualitative differences in the attack patterns of male rats.
“and long-term post-weaning social isolation has been shown to induce qualitative differences in the attack patterns of male rats (Toth et al., 2011).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Toth et al., 2011 source
May combine two claims.
Interpretationown dataThe effects of play deprivation preferentially center around socio-sexual behaviors in adulthood, supported by factor analyses identifying socio-sexual behavior factors that significantly differed in control and play-deprived males.
“The effects of play deprivation (and therefore, the importance of play itself) seem to preferentially center around socio-sexual behaviors in adulthood, a concept further supported by our factor analyses, which in an independent and unbiased manner identified factors in both the SDB and LDB studies that represent socio-sexual behavior and significantly differed in control and play-deprived males.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim.
Interpretationown dataOur results would argue that boys may be more vulnerable to a reduction in access to play than girls.
“Our results would argue that boys may be more vulnerable to a reduction in access to play than girls.”
Quote in the paperSubstantial claim- Rests on an assumption: Social play is remarkably similar across the many mammalian species in which it is expressed and has strong face validity in humans.
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
InterpretationreasoningThe impairment in the prosocial motivation task may have improved over time due to the increased social experience afforded as part of the test, or because animals had sufficient experience with the paradigm by the latter half of testing.
“This impairment may have improved over time due to the increased social experience afforded as part of the test (while animals were allowed only 10 s to interact with their cagemate following release from the confinement box, this social experience may have accumulated over time), or because animals had sufficient experience with the paradigm by the latter half of testing such that it allowed BARR”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThe differential effect on social preference in the SDB compared to the LDB study may be due to an as-yet-unidentified sensitive period for social development around the time of weaning.
“This differential effect in the SDB compared to the LDB study may be due to an as-yet-unidentified sensitive period for social development around the time of weaning.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Interpretationown dataThis sex difference may speak to the heightened importance of play experience in males compared to females, given even at baseline males are less successful on this socially-driven task.
“This too may speak to the heightened importance of play experience in males compared to females, given even at baseline males are less successful on this socially-driven task.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
Study design and conductnone givenSex was statistically tested as a variable, calling a finding a "sex difference" if and only if a significant main effect of sex or a significant interaction was detected.
“We statistically tested sex as a variable, calling a finding a “sex difference” if and only if we detected a significant main effect of sex or a significant interaction.”
Quote in the paperSubstantial claimClassified as probably not a substantial claim. May combine two claims.
Study design and conductnone givenWhen possible, males and females were included in all experiments, all of which were adequately powered to detect sex differences if they were present.
“When possible (i.e., in assays that are not only applicable to animals of one sex), males and females were included in all experiments, all of which were adequately powered to detect sex differences if they were present.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductnone givenThe BARR manipulation improves upon previous methodology in that it prevents play while allowing for other forms of social interaction.
“While our BARR manipulation improves upon previous methodology in that it prevents play while allowing for other forms of social interaction, there are nonetheless limitations.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Study design and conductnone givenBARR animals are also deprived of other tactile non-play social interactions such as social grooming, and other variables such as the difference in physical space allowed by the BARR vs. CTRL and ISO conditions may affect development.
“BARR animals are also deprived of other tactile non-play social interactions such as social grooming, and there may be other variables such as the difference in physical space allowed by the BARR vs. CTRL and ISO conditions that may affect development.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningThe maturation of these cell subtypes and/or projections may be modulated in an experience-dependent (and potentially sex-dependent) manner based on playfulness.
“The maturation of these cell subtypes and/or projections, then, may be modulated in an experience-dependent (and, potentially, sex-dependent) manner based on playfulness.”
Quote in the paperNot a substantial claimMay combine two claims.
InterpretationreasoningAnimals deprived of play may lack this experience, thereby hindering their ability to appropriately recognize and/or respond to social signals to de-escalate an agonistic encounter, resulting in increased aggression.
“Animals deprived of play may lack this experience, thereby hindering their ability to appropriately recognize and/or respond to social signals to de-escalate an agonistic encounter, resulting in increased aggression as we observed.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.
InterpretationreasoningThe female resilience may not be true for all traits, or there may be latent differences in assessed traits not detectable by the paradigms used to evaluate them.
“this may not be true for all traits, or there may be latent differences in our assessed traits not detectable by the paradigms we used to evaluate them.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Interpretationown dataIt is possible that the additional stress caused by full isolation may alter the direction and magnitude of these effects.
“It is also possible that the additional stress caused by full isolation may alter the direction and magnitude of these effects, given ours were seen only in BARR, but not ISO, males.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationThe play-as-practice theory has received criticism because there are key differences in the microstructure of juvenile play-fighting and adult aggressive behaviors.
“This theory has received criticism for various reasons, primarily that there are several key differences in the microstructure of juvenile play-fighting and adult aggressive behaviors, thus hindering play’s applicability as a means of physical “practice” (Pellis and Pellis, 1987).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Pellis and Pellis, 1987 source
May combine two claims.
InterpretationreasoningPlay may serve to provide experience in social skills, allowing for the maturation of brain circuitry to the same effect.
“so play may serve to provide experience in these social skills, allowing for the maturation of brain circuitry to the same effect.”
Quote in the paperSubstantial claim
The paper relies on this without support.
The barrier (BARR) housing condition prevents social play while allowing other social interaction.
“the modified housing used to prevent play”
“the increased social interaction allowed by the BARR housing condition”
The paper relies on this without support.
Social play is remarkably similar across the many mammalian species in which it is expressed and has strong face validity in humans.
“While our studies were conducted in rats, social play is remarkably similar across the many mammalian species in which it is expressed and has strong face validity in humans.”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Claimed LDB sex difference in preference ratio is absent from the table
MajorThe results claim a sex effect for the LDB opposite-sex preference ratio, whereas Table 1 reports p = 0.437 for that effect.
“a main effect of sex was detected when considering the data as a ratio of the time spent near the opposite sex compared to the same-sex stimulus box in the LDB animals”
“| Ratio Time Near Opposite-Sex | Non-normal | Wilcoxon rank-sum test | Effect of sex | W = 595 | 0.437 | r = 0.092 |”
Open-field result cites the play panel
MinorThe text cites Figure 1C for the initial open-field exposure, but the Figure 1 caption identifies panel B as the open-field test and panel C as the play test.
“the SDB animals were exposed to the open field in our initial studies (Figure 1C)”
“Acute play deprivation has no effect on anxiety-like behavior as evidenced by center time in an open field test (B), with timeline of experiment shown above graph); additionally, the ability and motivation to engage in play is maintained (C”
Male sexual-behavior test duration differs between methods and figure
MinorThe methods specify two 20-minute male sexual-behavior tests, but the Figure 5 caption calls them two 10-minute tests.
“For the sex behavior tests, males were placed in an enclosure as described above with a primed adult female stimulus rat for 20 min.”
“across two 10-min tests with a hormonally primed adult female stimulus rat on P63 and P70”
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“Indeed, deficits in play are core symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia (Alessandri, 1992; Jones et al., 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robus…”
BackgroundSex Differences in the Risk of Schizophrenia: Evidence From Meta-analysis
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“, 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robust sex differences in diagnosis and symptomology (Aleman et al., 2003; Ramtekkar et al., 2010; Arnett et al., 2015; Halladay et al., 2015; Giordano et al., 2021; Prosperi et al., 2021).”
BackgroundExperience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo
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ResultHalladay, A. K., Bishop, S. L., Constantino, J. N., Daniels, A. M., Koenig, K., Palmer, K., Messinger, D. S., Pelphrey, K. A., Sanders, S., Singer, A., et al. (2015) · Molecular Autism · doi:10.1186/s13229-015-0019-y · Cited by 582 · cited 1× · see citing works
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Ramtekkar, U. P., Reiersen, A. M., Todorov, A. A., & Todd, R. D. (2010) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2009.11.011 · Cited by 480 · cited 1× · see citing works
“, 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robust sex differences in diagnosis and symptomology (Aleman et al., 2003; Ramtekkar et al., 2010; Arnett et al., 2015; Halladay et al., 2015; Giordano et al., 2021; Prosperi et al., 2021).”
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“Indeed, deficits in play are core symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia (Alessandri, 1992; Jones et al., 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robus…”
BackgroundFunctional circuit architecture underlying parental behaviour
Kohl, J., Babayan, B. M., Rubinstein, N. D., Autry, A. E., Marin-Rodriguez, B., Kapoor, V., Miyamichi, K., Zweifel, L. S., Luo, L., Uchida, N., et al. (2018) · Nature · doi:10.1038/s41586-018-0027-0 · Cited by 459 · cited 1× · see citing works
“These regions have distinct roles in socio-sexual behavior in adulthood as well, often driven by distinct, separable cell type-specific and projection-specific mechanisms (Unger et al., 2015; Wong et al., 2016; Ishii et al., 2017; Kohl et al., 2018).”
BackgroundSocial deprivation and play in rats
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ResultA descriptive study of social development in the rat (Rattus norvegicus)
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Induction of PGE2 by estradiol mediates developmental masculinization of sex behavior
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ResultSelf-citationSex differences in <scp>ADHD</scp> symptom severity
Arnett, A. B., Pennington, B. F., Willcutt, E. G., DeFries, J. C., & Olson, R. K. (2015) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12337 · Cited by 333 · cited 1× · see citing works
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BackgroundPatterns of copulatory behavior in male mammals
Dewsbury, D. A. (1972) · The Quarterly Review of Biology · doi:10.1086/407097 · Cited by 330 · cited 4× · see citing works
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BackgroundMedial amygdalar aromatase neurons regulate aggression in both sexes
Unger, E. K., Burke, K. J., Yang, C. F., Bender, K. J., Fuller, P. M., & Shah, N. M. (2015) · Cell Reports · doi:10.1016/j.celrep.2014.12.040 · Cited by 275 · cited 1× · see citing works
“These regions have distinct roles in socio-sexual behavior in adulthood as well, often driven by distinct, separable cell type-specific and projection-specific mechanisms (Unger et al., 2015; Wong et al., 2016; Ishii et al., 2017; Kohl et al., 2018).”
BackgroundVanRyzin, J. W., Marquardt, A. E., Argue, K. J., Vecchiarelli, H. A., Ashton, S. E., Arambula, S. E., Hill, M. N., & McCarthy, M. M. (2019) · Neuron · doi:10.1016/j.neuron.2019.02.006 · Cited by 272 · see citing works
Self-citationPellis, S. M., & Pellis, V. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230303 · Cited by 255 · cited 1× · see citing works
“Additionally, there are known sex differences in the qualitative characteristics of social play interactions (Pellis and Pellis, 1990, 1997).”
BackgroundSex differences in the elevated plus-maze test and large open field test in adult Wistar rats.
Knight, P., Chellian, R., Wilson, R., Behnood-Rod, A., Panunzio, S., & Bruijnzeel, A. W. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173168 · Cited by 252 · cited 1× · see citing works
“However, replicating other studies (Johnston and File, 1991; Knight et al., 2021), we observed a small but significant sex difference in the LDB animals with a trending effect in the SDB animals (p = 0.”
ResultJordan, R. (2003) · Autism · doi:10.1177/1362361303007004002 · Cited by 248 · cited 2× · see citing works
“Indeed, deficits in play are core symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia (Alessandri, 1992; Jones et al., 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robus…”
BackgroundReporting and misreporting of sex differences in the biological sciences
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Brief periods of socialization and later behavior in the rat
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“, 2002), cognition (Einon et al., 1978; Baarendse et al., 2013; Yusufishaq and Rosenkranz, 2013), and sexual behavior (Gerall et al.”
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“, 2000), increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al., 1991; Arakawa, 2003; Leussis and Andersen, 2008; Lukkes et al., 2009; Cuesta et al., 2020), and impacts susceptibility to addiction-related behaviors (Whitaker et al.”
BackgroundEffective modulation of male aggression through lateral septum to medial hypothalamus projection
Wong, L. C., Wang, L., D’Amour, J. A., Yumita, T., Chen, G., Yamaguchi, T., Chang, B. C., Bernstein, H., You, X., Feng, J. E., et al. (2016) · Current Biology · doi:10.1016/j.cub.2015.12.065 · Cited by 213 · see citing works
Isolation during the play period in infancy decreases adult social interactions in rats
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“Various studies have found that juvenile social isolation in rats leads to impairments in social behavior (Hol et al., 1999; Van den Berg et al., 1999; Von Frijtag et al., 2002), cognition (Einon et al.”
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A note on the power of Fisher's least significant difference procedure
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“, tests in which sex was not a factor, such as male sex behavior), post hoc analysis was conducted using Fisher’s least significant difference procedure, as there were three groups (Meier, 2006).”
MethodA labeled-line neural circuit for pheromone-mediated sexual behaviors in mice
Ishii, K. K., Osakada, T., Mori, H., Miyasaka, N., Yoshihara, Y., Miyamichi, K., & Touhara, K. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.038 · Cited by 185 · cited 1× · see citing works
“These regions have distinct roles in socio-sexual behavior in adulthood as well, often driven by distinct, separable cell type-specific and projection-specific mechanisms (Unger et al., 2015; Wong et al., 2016; Ishii et al., 2017; Kohl et al., 2018).”
Wright, I. K., Upton, N., & Marsden, C. A. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90572-6 · Cited by 177 · see citing works
Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning
Whitaker, L. R., Degoulet, M., & Morikawa, H. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.022 · Cited by 177 · cited 1× · see citing works
“, 2020), and impacts susceptibility to addiction-related behaviors (Whitaker et al., 2013; Baarendse et al., 2014).”
BackgroundPattij, T., De Jong, T. R., Uitterdijk, A., Waldinger, M. D., Veening, J. G., Cools, A. R., Van Der Graaf, P. H., & Olivier, B. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04252.x · Cited by 163 · cited 2× · see citing works
“It is well known in the field of rodent sexual behavior that around 10% of all sexually mature male rats will be “duds” (otherwise known as “sexually sluggish”), meaning that they do not ejaculate in the course of a 20–30 min assay with a sexually receptive female (Dewsbury, 1972; Pattij et al., 2005; Portillo et al.,…”
BackgroundWhat is play fighting and what is it good for?
Pellis, S. M., & Pellis, V. C. (2017) · Learning & Behavior · doi:10.3758/s13420-017-0264-3 · Cited by 160 · cited 2× · see citing works
“This reciprocity—necessitating monitoring one’s own actions and those of a partner, recognizing social signals indicating the partner’s responses and intentions, and adjusting one’s actions appropriately to maintain the backand-forth of the play bout—is a fundamental feature of social play (Pellis and Pellis, 2017), s…”
BackgroundAttention, play, and social behavior in ADHD preschoolers
Alessandri, S. M. (1992) · Journal of Abnormal Child Psychology · doi:10.1007/bf00916693 · Cited by 157 · cited 2× · see citing works
“…symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia (Alessandri, 1992; Jones et al., 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robust sex…”
BackgroundBredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 157 · see citing works
Toth, M., Mikics, E., Tulogdi, A., Aliczki, M., & Haller, J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.003 · Cited by 152 · see citing works
Disruption of the male rat’s sexual behaviour induced by social isolation
Gerall, H. D., Ward, I. L., & Gerall, A. A. (1967) · Animal Behaviour · doi:10.1016/s0003-3472(67)80010-1 · Cited by 136 · cited 1× · see citing works
“, 2013; Yusufishaq and Rosenkranz, 2013), and sexual behavior (Gerall et al., 1967; Cooke et al., 2000), increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al.”
BackgroundGiordano, G. M., Bucci, P., Mucci, A., Pezzella, P., & Galderisi, S. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.789179 · Cited by 133 · cited 1× · see citing works
“, 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robust sex differences in diagnosis and symptomology (Aleman et al., 2003; Ramtekkar et al., 2010; Arnett et al., 2015; Halladay et al., 2015; Giordano et al., 2021; Prosperi et al., 2021).”
BackgroundThe effects of early social isolation on the motivation for social play in juvenile rats
Ikemoto, S., & Panksepp, J. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250404 · Cited by 121 · cited 1× · see citing works
“As seen in previous studies of juvenile isolation (Panksepp and Beatty, 1980; Ikemoto and Panksepp, 1992), we found that the ability and motivation to participate in play was not only intact in BARR and ISO animals but was increased relative to our historical data for control-housed animals (Figure 1C; Argue and McCar…”
ResultVon Frijtag, J. C., Schot, M., van den Bos, R., & Spruijt, B. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10057 · Cited by 116 · see citing works
The socially-isolated rat as a model for anxiety
Parker, V., & Morinan, A. (1986) · Neuropharmacology · doi:10.1016/0028-3908(86)90224-8 · Cited by 113 · cited 1× · see citing works
“, 2000), increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al., 1991; Arakawa, 2003; Leussis and Andersen, 2008; Lukkes et al., 2009; Cuesta et al., 2020), and impacts susceptibility to addiction-related behaviors (Whitaker et al.”
BackgroundA brain motivated to play: insights into the neurobiology of playfulness
Siviy, S. M. (2016) · Behaviour · doi:10.1163/1568539x-00003349 · Cited by 113 · cited 1× · see citing works
“This specificity to socio-sexual behavior makes sense, given play is itself a social behavior and involves the activity of many regions in the social circuitry, such as the medial amygdala, lateral septum, and hypothalamus (summarized in Siviy, 2016 and VanRyzin et al., 2020a).”
BackgroundHermes, G., Li, N., Duman, C., & Duman, R. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.12.019 · Cited by 111 · see citing works
Peartree, N. A., Hood, L. E., Thiel, K. J., Sanabria, F., Pentkowski, N. S., Chandler, K. N., & Neisewander, J. L. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.10.001 · Cited by 90 · cited 1× · see citing works
“Interaction with a conspecific across a similar physical barrier has been shown to be socially rewarding (Peartree et al., 2012) and to reduce anxiety-like behavior as compared to full isolation, an additional benefit (Klapper-Goldstein et al.”
BackgroundSchneider, P., Bindila, L., Schmahl, C., Bohus, M., Meyer-Lindenberg, A., Lutz, B., Spanagel, R., & Schneider, M. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00203 · Cited by 89 · cited 1× · see citing works
“, reducing play by rearing juveniles with an adult or a peer from a less playful strain) points to play experience being the critical driver of the impairments observed (Schneider et al., 2016; Burleson et al., 2016; Pellis et al., 2017; Stark and Pellis, 2020, 2021).”
BackgroundDisrupted social development enhances the motivation for cocaine in rats
Baarendse, P. J. J., Limpens, J. H. W., & Vanderschuren, L. J. M. J. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3362-8 · Cited by 87 · cited 1× · see citing works
“, 2020), and impacts susceptibility to addiction-related behaviors (Whitaker et al., 2013; Baarendse et al., 2014).”
BackgroundThe effects of isolation rearing on open-field behavior in male rats depends on developmental stages
Arakawa, H. (2003) · Developmental Psychobiology · doi:10.1002/dev.10120 · Cited by 83 · cited 2× · see citing works
“…behavior (Gerall et al., 1967; Cooke et al., 2000), increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al., 1991; Arakawa, 2003; Leussis and Andersen, 2008; Lukkes et al., 2009; Cuesta et al., 2020), and impacts susceptibility to addiction-related behaviors…”
BackgroundVanRyzin, J. W., Yu, S. J., Perez‐Pouchoulen, M., & McCarthy, M. M. (2016) · eNeuro · doi:10.1523/eneuro.0297-16.2016 · Cited by 83 · cited 2× · see citing works
“scored offline for the number of mounts, intromissions, and ejaculations as previously described (VanRyzin et al., 2016).”
MethodSelf-citationPost-weaning social isolation impairs observational fear conditioning
Yusufishaq, S., & Rosenkranz, J. A. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.12.050 · Cited by 80 · cited 1× · see citing works
“, 2002), cognition (Einon et al., 1978; Baarendse et al., 2013; Yusufishaq and Rosenkranz, 2013), and sexual behavior (Gerall et al.”
BackgroundSocial isolation in rats: effects on animal welfare and molecular markers for neuroplasticity
Begni, V., Sanson, A., Pfeiffer, N., Brandwein, C., Inta, D., Talbot, S. R., Riva, M. A., Gass, P., & Mallien, A. S. (2020) · PLOS ONE · doi:10.1371/journal.pone.0240439 · Cited by 78 · cited 1× · see citing works
“the lack of general social interaction, as well as the additional stress that total isolation induces (Begni et al., 2020).”
BackgroundRivera-Irizarry, J. K., Skelly, M. J., & Pleil, K. E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00129 · Cited by 72 · cited 1× · see citing works
“In contrast, isolation starting later in adolescence, from P28–70, was shown to produce hypersociability in both sexes, although this study was conducted in mice (Rivera-Irizarry et al., 2020).”
ResultCharacterization of juvenile play in rats: importance of sex of self and sex of partner
Argue, K. J., & McCarthy, M. M. (2015) · Biology of Sex Differences · doi:10.1186/s13293-015-0034-x · Cited by 71 · cited 1× · see citing works
“As seen in previous studies of juvenile isolation (Panksepp and Beatty, 1980; Ikemoto and Panksepp, 1992), we found that the ability and motivation to participate in play was not only intact in BARR and ISO animals but was increased relative to our historical data for control-housed animals (Figure 1C; Argue and McCar…”
ResultSelf-citationBurleson, C. A., Pedersen, R. W., Seddighi, S., DeBusk, L. E., Burghardt, G. M., & Cooper, M. A. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000148 · Cited by 69 · cited 1× · see citing works
“, reducing play by rearing juveniles with an adult or a peer from a less playful strain) points to play experience being the critical driver of the impairments observed (Schneider et al., 2016; Burleson et al., 2016; Pellis et al., 2017; Stark and Pellis, 2020, 2021).”
BackgroundCooke, B. M., Chowanadisai, W., & Breedlove, S. M. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00301-6 · Cited by 67 · cited 1× · see citing works
“, 2013; Yusufishaq and Rosenkranz, 2013), and sexual behavior (Gerall et al., 1967; Cooke et al., 2000), increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al.”
BackgroundProsperi, M., Turi, M., Guerrera, S., Napoli, E., Tancredi, R., Igliozzi, R., Apicella, F., Valeri, G., Lattarulo, C., Gemma, A., et al. (2021) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2020.594082 · Cited by 46 · cited 1× · see citing works
“, 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robust sex differences in diagnosis and symptomology (Aleman et al., 2003; Ramtekkar et al., 2010; Arnett et al., 2015; Halladay et al., 2015; Giordano et al., 2021; Prosperi et al., 2021).”
BackgroundTrouillet, A.-C., Ducroq, S., Naulé, L., Capela, D., Parmentier, C., Radovick, S., Hardin-Pouzet, H., & Mhaouty-Kodja, S. (2022) · Communications Biology · doi:10.1038/s42003-022-03324-w · Cited by 39 · cited 1× · see citing works
“For example, the decrease in the number of mounts we observed was of similar magnitude to that seen in males treated with a cyclooxygenase-2 inhibitor for 2 weeks during the perinatal sensitive period (Amateau and McCarthy, 2004), and the reduction in the percentage of animals which successfully ejaculated we observed…”
ResultPlay Fighting and Real Fighting
Smith, P. K. (2007) · New Aspects of Human Ethology · doi:10.1007/978-0-585-34289-4_3 · Cited by 36 · cited 1× · see citing works
“…is the “play-as-practice” theory, which argues that the individual behaviors constituting social play (e.g., pounces, pins, and boxing behaviors in rats) resemble adult agonistic behaviors for a reason: because play serves as practice for later-life aggressive encounters (Fagen, 1981; Smith, 1997).”
BackgroundStability and prediction of schizophrenia from adolescence to adulthood
Helgeland, M. I., & Torgersen, S. (2005) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-005-0436-0 · Cited by 35 · cited 1× · see citing works
“Indeed, deficits in play are core symptoms of neurodevelopmental disorders like autism spectrum disorder, attention-deficit/hyperactivity disorder, and early onset schizophrenia (Alessandri, 1992; Jones et al., 1994; Møller and Husby, 2000; Jordan, 2003; Helgeland and Torgersen, 2005), many of which also exhibit robus…”
BackgroundDevelopmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
Self-citationStark, R., & Pellis, S. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1720142 · Cited by 32 · see citing works
Pellis, S. M., Williams, L. A., & Pellis, V. C. (2017) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2017.30.00.14 · Cited by 29 · see citing works
PORTILLO, W., DIAZ, N., RETANAMARQUEZ, S., & PAREDES, R. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.04.023 · Cited by 26 · cited 2× · see citing works
“It is well known in the field of rodent sexual behavior that around 10% of all sexually mature male rats will be “duds” (otherwise known as “sexually sluggish”), meaning that they do not ejaculate in the course of a 20–30 min assay with a sexually receptive female (Dewsbury, 1972; Pattij et al., 2005; Portillo et al.,…”
BackgroundCuesta, S., Funes, A., & Pacchioni, A. M. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00466-x · Cited by 26 · cited 1× · see citing works
“, 2000), increases anxiety- and depression-like behavior (Parker and Morinan, 1986; Wright et al., 1991; Arakawa, 2003; Leussis and Andersen, 2008; Lukkes et al., 2009; Cuesta et al., 2020), and impacts susceptibility to addiction-related behaviors (Whitaker et al.”
BackgroundSocial behavior in prepubertal neurexin 1α deficient rats: A model of neurodevelopmental disorders.
Kight, K. E., Argue, K. J., Bumgardner, J. G., Bardhi, K., Waddell, J., & McCarthy, M. M. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000482 · Cited by 17 · see citing works
Self-citationStark, R. A., & Pellis, S. M. (2021) · Behavioural Processes · doi:10.1016/j.beproc.2021.104492 · Cited by 17 · see citing works
Klapper-Goldstein, H., Murninkas, M., Gillis, R., Mulla, W., Levanon, E., Elyagon, S., Schuster, R., Danan, D., Cohen, H., & Etzion, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-57528-3 · Cited by 16 · cited 1× · see citing works
“, 2012) and to reduce anxiety-like behavior as compared to full isolation, an additional benefit (Klapper-Goldstein et al., 2020).”
BackgroundAssessing Rough-and-tumble Play Behavior in Juvenile Rats
VanRyzin, J., Marquardt, A., & McCarthy, M. (2020) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3481 · Cited by 16 · see citing works
Self-citationA neurogenetic mechanism of experience-dependent suppression of aggression
Ishii, K., Cortese, M., Leng, X., Shokhirev, M. N., & Asahina, K. (2022) · Science Advances · doi:10.1126/sciadv.abg3203 · Cited by 16 · cited 1× · see citing works
“Indeed, recent work in Drosophila identified a transcriptional regulator believed to govern this same effect, suppressing aggression in a social experience-dependent manner (Ishii et al., 2022), and long-term post-weaning social isolation has been shown to induce qualitative differences in the attack patterns of male…”
BackgroundSocial Recognition Task in the Rat
Lemaire, M. (2003) · Current Protocols in Pharmacology · doi:10.1002/0471141755.ph0530s20 · Cited by 15 · cited 2× · see citing works
“…recognition assay, subjects were assessed for the amount of time spent interacting with a novel stimulus animal (“Train” trial) compared to the amount of time spent interacting with that same (now familiar) animal on a second trial (“Test” trial) after a 30 min inter-trial interval (Lemaire, 2003).”
BackgroundBekoff, M., & Fagen, R. (1981) · Evolution · doi:10.2307/2408140 · Cited by 2
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1 of the 76 references couldn’t be matched to a known paper.
Research works printed but not linked: 2
- Pellis, 2009, The Playful Brain
- 2021, RStudio: Integrated Development Environment for R
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Sorted by citations
The neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · see citing works
Neural Control of Sexually Dimorphic Social Behavior: Connecting Development to Adulthood
McCarthy, M. M. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-121522-110856 · Cited by 36 · see citing works
Self-citationBehavioral neuroscience’s inevitable SABV growing pains
Shansky, R. M. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.06.007 · Cited by 21 · see citing works
Ham, J. R., Szabo, M., Annor‐Bediako, J., Stark, R. A., Iwaniuk, A. N., & Pellis, S. M. (2024) · Developmental Psychobiology · doi:10.1002/dev.22456 · Cited by 18 · see citing works
Pellis, S. M., Pellis, V. C., & Ham, J. R. (2024) · Frontiers in Ethology · doi:10.3389/fetho.2024.1362052 · Cited by 15 · see citing works
Play partner preferences among groups of unfamiliar juvenile male rats
Ham, J. R., & Pellis, S. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-66988-w · Cited by 13 · see citing works
“Although males and female juvenile rats play using the same behavioral patterns 27 , and gain some of the same benefits from playing in the juvenile period 9 , females also gain some unique benefits 16 .”
BackgroundNyberg, H., Bogen, I. L., Nygaard, E., Achterberg, E. J. M., & Andersen, J. M. (2024) · Psychopharmacology · doi:10.1007/s00213-024-06718-2 · Cited by 11 · see citing works
“…studies have linked reduced play during the juvenile period to a number of negative outcomes in adulthood, such as increased aggression, heightened anxiety, decreased sexual behavior, and altered social interactions (Lukkes et al. 2009; Marquardt et al. 2023; Vanderschuren and Trezza 2014).”
Bijlsma, A., Birza, E. E., Pimentel, T. C., Maranus, J. P. M., van Gaans, M. J. J. M., Klooster, J. G. L. T., Baars, A. M., Achterberg, E. J. M., Lesscher, H. M. B., Wierenga, C. J., et al. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16313 · Cited by 10 · see citing works
“Recent studies suggested that social play is equally important for PFC development in both sexes (Stark et al., 2023), but that differences can occur in sex-specific behaviours (Marquardt et al., 2023).”
BackgroundLeonetti, A. M., Sheehan, A. C., Murray, S. H., Burke, F. F., Fletcher, B. C. J., & McCormick, C. M. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115702 · Cited by 8 · see citing works
“This switch in preference may reflect frustration (which can be characterized by an aversive response; reviewed in; [53]) when a reward is removed.”
Whitten, C. J., Kelly, J. R., Gillespie, A. L., Brooks, H. J. B., Hooker, M. K., Temple, A., Hennon, L. M., Kilgore, B. J., Singamaneni, Y. B., Schulz, K. M., et al. (2025) · Developmental Psychobiology · doi:10.1002/dev.70020 · Cited by 7 · see citing works
Pham, A. L., Marquardt, A. E., Montgomery, K. R., Sobota, K. N., McCarthy, M. M., & VanRyzin, J. W. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02173-5 · Cited by 6 · see citing works
Self-citationMaturation of a cortical-amygdala circuit limits sociability in male rats
Ferrara, N. C., Trask, S., Padival, M., & Rosenkranz, J. A. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad124 · Cited by 7 · see citing works
Mota‐Ramírez, L. D., & Escobar, C. (2023) · Developmental Psychobiology · doi:10.1002/dev.22392 · Cited by 6 · see citing works
Cullins, E., & Chester, J. A. (2024) · Alcohol and Alcoholism · doi:10.1093/alcalc/agae006 · Cited by 6 · see citing works
Ham, J. R., & Pellis, S. M. (2025) · iScience · doi:10.1016/j.isci.2025.112562 · Cited by 5 · see citing works
Conspecific interactions predict social transmission of fear in female rats
Seese, S., Tinsley, C. E., Wulffraat, G. C., Hixon, J. G., & Monfils, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-58258-6 · Cited by 4 · see citing works
“While the frequency of play decreases with age, it continues into adulthood in males 29 and is posited to be an essential means of conflict reduction and relationship maintenance 28,30–34 .”
BackgroundMethodOrsucci, I. C., Becker, K. D., Ham, J. R., Lee, J. D. A., Bowden, S. M., & Veenema, A. H. (2025) · Physiology & Behavior · doi:10.1016/j.physbeh.2025.115080 · Cited by 3 · see citing works
Polzin, B. J., Zhao, C., Stevenson, S. A., Gammie, S. C., & Riters, L. V. (2024) · Genes Brain & Behavior · doi:10.1111/gbb.12908 · Cited by 2 · see citing works
Achterberg, E. J. M., Klooster, J. G. L. T., Pimentel, T. C., Aleksić, A., Hendriks, J., Nijhof, S. L., van der Ent, C. K., & Lesscher, H. M. B. (2024) · Frontiers in Ethology · doi:10.3389/fetho.2024.1458136 · Cited by 2 · see citing works
Marquardt, A. E., Basu, M., VanRyzin, J. W., Ament, S. A., & McCarthy, M. M. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115782 · Cited by 2 · see citing works
Self-citationDevelopmental and dynamic systems: insights for sex/gender research
Grossi, G., Duchesne, A., & Maney, D. L. (2026) · Biology of Sex Differences · doi:10.1186/s13293-026-00920-x · Cited by 2 · see citing works
“In humans, to DST, development is contingent on these interactions throughout life and on the very conditions in which the organism develops (e.g., [1, 66]).”
Feminization of social play behavior depends on microgliaPreprint
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.08.19.608675 · Cited by 2 · see citing works
“Recent studies have revealed that juvenile play imparts later-life reproductive fitness benefits in males (Marquardt et al., 2023; Holmes et al., 2024), which could explain the tightly regulated control of masculinization of neural circuitry underlying play (Pellis 2002; Bredewold et al., 2014;…”
BackgroundSelf-citationPartner Choice and Context‐Dependent Sex Differences in Rat Rough‐and‐Tumble Play
Ham, J. R., Pellis, S. M., & McDonald, R. J. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70426 · Cited by 1 · see citing works
“…Pellis, Ham, and Achterberg 2022), it has been used extensively to study the mechanisms regulating social behavior and the development of associated brain systems (e.g., Bagi et al. 2022; Ham, Szabo, et al. 2024; Marquardt et al. 2023; Reinhold et al. 2019; Stark et al. 2023; Veenema et al. 2013).”
Ham, J. R., Iwaniuk, A. N., & Pellis, S. M. (2026) · Behavioural Brain Research · doi:10.1016/j.bbr.2026.116198 · Cited by 1 · see citing works
Daddy matters: Exploring the effects of stallion presence on foal behaviour
Šandlová, K., Ceacero, F., & Komárková, M. (2025) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2025.106683 · Cited by 1 · see citing works
Calado, C. M. S. D. S., Manhães‐de‐Castro, R., Gouveia, H. J. C. B., Nogueira, R. M. T. B. L., Souza, V. D. S., de Lira, A. V. S. M., Merencio, S. M. D. A., Lima, B. M. P., de Oliveira, M. V. P., & Toscano, A. E. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149924 · Cited by 2 · see citing works
Unravelling the Role of the Dopamine D1 Receptor in Anhedonia, Asociality, and Avolition
Witt, K. (2023) · doi:10.26686/wgtn.24646128 · Cited by 1 · see citing works
Orsucci, I. C., Becker, K. D., Ham, J. R., Lee, J., Bowden, S., & Veenema, A. H. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.14.623692 · Cited by 1 · see citing works
Evaluating the play fighting of rats: A sociological perspective
Ham, J. R., Pellis, S. M., Pellis, V. C., & Achterberg, E. J. M. (2026) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2026.110836
Neural Mechanisms of Social Homeostasis: Dynamic Range Plasticity
Cressy, J., Jia, C., Salk, J. D., & Tye, K. M. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0224-25.2025
“…play reverses stress-induced de fi cits in forced swim, novelty-induced hypophagia, and sucrose preference tests (Burgdorf et al., 2017), while play deprivation reduces prosocial behavior, increases aggression, and impairs cognitive fl exibility (Panksepp and Beatty, 1980; Marquardt et al., 2023).”
Murray, S. H., Randell, A. M., Krajcovic, F. S. E., Fletcher, B. C. J., & McCormick, C. M. (2026) · Developmental Psychobiology · doi:10.1002/dev.70174
- Authors
- Marquardt, A. E., VanRyzin, J. W., Fuquen, R. W., & McCarthy, M. M.
- Affiliations
- University of Maryland, Baltimore (US)
- Corresponding author
- McCarthy, Margaret M.
- Venue
- Frontiers in Behavioral Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2023-01-23
- Volume
- 16
- Pages
- 1076765-1076765
- ISSN
- 1662-5153 (ISSN-L)
- PMC
- PMC9899815
- OpenAlex
- W4317718243
- Semantic Scholar
- 0e692f3be2503ec241a2ae492375b847bbc7e05c
- Cited by
- 31
- References
- 76
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 12 · 2023: 5
- FWCI
- 8.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Keywords
- social play, play deprivation, sex differences, sociosexual behavior, sexual behavior, hypersociability, aggression, prosocial behavior, empathy, anxiety-like behavior, social recognition, object memory, sex preference, rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-12.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-12.
Cited sources are checked by gpt-6-sol.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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