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Cited by 51Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyNeurotransmitter Receptor Influence on Behavior

Sexually dimorphic role for vasopressin in the development of social play

Open access
Paul, Matthew J., Terranova, Joseph I., Probst, Clemens K., Murray, Elaine K., Ismail, Nafissa I., de Vries, Geert J.·2014·Frontiers in Behavioral Neuroscience
DOI 10.3389/fnbeh.2014.00058PMC PMC3937588
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Abstract

Despite the well-established role of arginine vasopressin (AVP) in adult social behavior, its role in social development is relatively unexplored. In this paper, we focus on the most prominent social behavior of juvenile rats, social play. Previous pharmacological experiments in our laboratory suggested that AVP regulates play in a sex- and brain region-specific manner in juvenile rats. Here we investigate the role of specific AVP systems in the emergence of social play. We first characterize the development of play in male and female Wistar rats and then ask whether the development of AVP mRNA expression correlates with the emergence of play. Unexpectedly, play emerged more rapidly in weanling-aged females than in males, resulting in a sex difference opposite of that typically reported for older, juvenile rats. AVP mRNA and play were correlated in males only, with a negative correlation in the bed nucleus of the stria terminalis (BNST) and a positive correlation in the paraventricular nucleus of the hypothalamus (PVN). These findings support the hypothesis that AVP acts differentially on multiple systems in a sex-specific manner to regulate social play and suggest a role for PVN and BNST AVP systems in the development of play. Differential neuropeptide regulation of male and female social development may underlie well-documented sex differences in incidence, progression, and symptom severity of behavioral disorders during development.

AI snapshot

Written from the paper’s full text.

TL;DR

In weanling Wistar rats, social play emerged more rapidly in females than in males, opposite the usual juvenile sex difference, and AVP mRNA in the BNST and PVN correlated with play in males but not females. The findings suggest sexually dimorphic, region-specific AVP regulation of social play development.

Key findings

  • Play emerged faster in female weanlings than males: females showed more Pins overall (main effect of sex, P < 0.03), Pins increased with age only in females (interaction, P < 0.04), and at 24 days females had more Pins than males (P < 0.0009). This sex difference did not persist in 35–36-day juveniles, where there were no differences in Total Play, Pins, Pounces, or Boxing (P > 0.32).
  • In Experiment 2, female weanlings had higher Total Play and Pounces than males (main effect of sex, P < 0.002 for both), with females showing increases between 18 and 19 days in Total Play, Pounces, and Boxing (P < 0.001 for all three) and higher levels than males at 19 days (P < 0.002 for all three); males did not significantly rise above day 18 values (P > 0.05).
  • BNST AVP mRNA was much higher in males than females (P < 0.0001), declined in males from 18 to 21 days (P < 0.004) but not females (P > 0.99), and was negatively correlated with Total Play in males (R² = 0.71, P < 0.003; at 18 days only, n = 5, R² = 0.78, P < 0.05; at 21 days, P = 0.16). No correlation was found in females (P > 0.28).
  • PVN AVP mRNA did not differ by sex or age (sex P > 0.4; age P > 0.11; interaction P > 0.98) and was positively correlated with Total Play in males (R² = 0.43, P < 0.04), though not when restricted to 18-day (P = 0.07) or 21-day (P > 0.62) males; no correlation was found in females (P > 0.58).

Methods

  • Wistar rats from Charles River were used. Experiment 1a tested same-sex, age-matched pairs once at 16, 19, 21, or 24 days (n = 4 play pairs per group; one 18-day female video was unscorable, reducing that group to n = 3). Experiment 1b tested identically treated rats at 35–36 days (n = 4 per group). Experiment 2 tested weanlings at 18, 19, 20, or 21 days with a 35-day-old same-sex juvenile stimulus rat (n = 8, 7, 4, and 5 males/4 females respectively); a subset was sacrificed for AVP in situ hybridization (n = 5 for 18-day females, 18-day males, and 21-day males; n = 4 for 21-day females).
  • Play tests lasted 30 min under red light; pounces, pins, boxing, and Total Play were scored blind from video. AVP mRNA in BNST and PVN was measured by in situ hybridization, with film and emulsion quantification using ImageJ. Data were analyzed with two-way ANOVA or Student’s t-test, Fisher’s PLSD post hoc tests, and simple regression.

Limitations

  • The paper states that no play–AVP correlations were detected in females and suggests AVP may act through other nuclei not studied (e.g., nucleus circularis, supraoptic nucleus, medial amygdaloid nucleus), through a different regulatory stage such as peptide production or secretion, or through a subset of PVN cells whose mRNA differences could be obscured by whole-PVN analysis.
  • The paper notes that the reversed sex difference in play emergence may depend on testing conditions and may not manifest under all paradigms; it also raises the possibility that shipping stress in the second week of life contributed to earlier female play, though no studies have directly tested shipping effects on play emergence.
  • Evident from the text: the AVP analyses are correlational and cannot establish causation; sample sizes for AVP quantification were small (n = 4–5 per group, with the 18-day male correlation based on n = 5); AVP expression was examined at only 18 and 21 days; PVN signal was overexposed on film for most cases and required emulsion quantification, while BNST could not be reliably quantified from emulsion-dipped slides.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3389/fnbeh.2014.00058

Cites

53 of 53 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

21 of 64 cited sources checked · 15 supported · 0 flagged · accuracy not yet measured

  • Interpretationown data

    The sex difference in play emergence in weanling rats is opposite to that typically reported for older juvenile rats.

    “Unexpectedly, play emerged more rapidly in weanling-aged females than in males, resulting in a sex difference opposite of that typically reported for older, juvenile rats.”
    • Also stated in: § Experiment 1a: emergence of play behavior · plain
      “Female weanling-aged rats exhibited a more rapid emergence of pinning behavior than males (Figure 1A) resulting in a sex difference opposite that typically reported for juveniles (e.g., Krebs-Kraft et al., 2010).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Krebs-Kraft et al., 2010 source
  • Premisecitation

    Play behavior is increased in juvenile male rats infused with a V1aR antagonist into the septum.

    “play behavior is increased in juvenile male rats infused with a V1aR antagonist into the septum (Veenema et al., 2013)”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Veenema et al., 2013 source
  • Premisecitation

    Intracerebroventricular infusions of a V1aR antagonist reduced play in males.

    “intracerebroventricular infusions of this V1aR antagonist, which reach a much wider range of potential neural AVP targets, reduced play in males.”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Veenema et al., 2013 source
  • Premisecitation

    Infusions of a V1aR antagonist alter levels of play in females in a region-specific manner.

    “infusions of a V1aR antagonist alter levels of play in females, again in a region-specific manner (Veenema et al., 2013)”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Veenema et al., 2013 source
  • Premisecitation

    Effects of V1aR antagonist infusions in females are opposite to those seen in males.

    “Effects of these infusions, however, are opposite to those seen in males.”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Veenema et al., 2013 source
  • Classified as probably not a substantial claim. 23
  • May combine two claims. 23

  • Classified as probably not a substantial claim.

    Premisecitation

    The lateral septum receives projections from the BNST.

    “The lateral septum receives projections from the BNST (De Vries and Buijs, 1983), a primary node in the neural network thought to play a role in social behavior (Newman, 1999).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites De Vries and Buijs, 1983 source

  • May combine two claims.

    Premisecitation

    Intracerebroventricular injections of a V1aR antagonist decrease play fighting of male rats but increase that of females, whereas septal injections cause the opposite effects.

    “For example, intracerebroventricular injections of a V1aR antagonist decrease play fighting of male rats, but increase that of females, whereas septal injections cause the opposite effects (Veenema et al., 2013).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Veenema et al., 2013 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Many neurodevelopmental disorders exhibit sex differences in incidence, progression, and symptom severity.

    “Many neurodevelopmental disorders exhibit sex differences in incidence, progression, and symptom severity (Fombonne, 2009; Abel et al., 2010).”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites Fombonne, 2009 source
    • cites Abel et al., 2010 source

      The available passages contain bibliographic information and the title, “Sex differences in schizophrenia,” but no substantive discussion of incidence, progression, or symptom severity. Searches for those outcomes and for neurodevelopmental disorders found no passage that verifies the broader claim. (LLM, conf=0.72)

      Experimental — accuracy not yet measured

  • Classified as probably not a substantial claim.

    Premisecitation

    AVP has been implicated in juvenile social play.

    “While AVP has been implicated in juvenile social play (Cheng and Delville, 2009; Veenema et al., 2013)”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Cheng and Delville, 2009 source
    • cites Veenema et al., 2013 source

  • May combine two claims.

    Premisecitation

    V1aR antagonists influence levels of play fighting in juvenile hamsters and rats, but the direction depends on sex and brain area injected.

    “Studies in our and other laboratories have demonstrated that AVP 1a receptor (V1aR) antagonists influence levels of play fighting in juvenile hamsters and rats (Cheng and Delville, 2009; Veenema et al., 2013), but the direction of these effects depends upon the sex of the subject and brain area injected.”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites Cheng and Delville, 2009 source
    • cites Veenema et al., 2013 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    AVP may act via other nuclei not considered in the present study that likely contribute to AVP's actions on play.

    “AVP may act via other nuclei not considered in the present study that likely contribute to AVP’s actions on play, e.g., nucleus circularis, supraoptic nucleus, medial amygdaloid nucleus (Cheng et al., 2008; Kurian et al., 2008; Forbes-Lorman et al., 2012).”
    Quote in the paperNot a substantial claim2 of 3 sources checked
    • cites Cheng et al., 2008 source
    • cites Kurian et al., 2008 source

      The Results section reports that disrupting Mecp2 in the developing amygdala reduced juvenile social play in male rats, supporting a role for the amygdala in play. The paper does not identify the medial amygdaloid nucleus specifically or address AVP acting through it, the nucleus circularis, or the supraoptic nucleus (searched: AVP, vasopressin, and the named nuclei). No page numbers are available in our copy. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites Forbes-Lorman et al., 2012 source

      The paper’s Experiment 1 section says AVP expression in the bed nucleus of the stria terminalis and centromedial amygdala is involved in social play. Its Discussion also notes a correlation between AVP expression and juvenile play, while saying it is unclear whether reduced AVP explains reduced play. Our copy does not link the nucleus circularis or supraoptic nucleus to play, so it supports the general possibility but not the cited examples as a group. (LLM, conf=0.83)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationcitation

    Understanding the underlying mechanisms that direct social development, particularly those that differ between males and females, may explain sex differences in vulnerability to neurodevelopmental disorders.

    “Understanding the underlying mechanisms that direct social development, particularly those mechanisms that differ between males and females, may explain sex differences in vulnerability to neurodevelopmental disorders (De Vries, 2004).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites De Vries, 2004 source

      The Dual-Function Hypothesis for Neural Sex Differences (p. 2) says the mechanisms underlying social behavior may differ between males and females. The discussion of developing brains (pp. 3–4) addresses sex differences in neural development, but our copy does not link those mechanisms to sex differences in vulnerability to neurodevelopmental disorders. (LLM, conf=0.84)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Various early-life manipulations can increase or decrease play of juvenile males, or affect both sexes equivalently.

    “various early-life manipulations can increase or decrease play of juvenile males (Veenema and Neumann, 2009; Edelmann et al., 2013), or affect both sexes equivalently (Karkow and Lucion, 2013).”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites Veenema and Neumann, 2009 source
    • cites Edelmann et al., 2013 source
    • cites Karkow and Lucion, 2013 source

  • Classified as probably not a substantial claim.

    Premisecitation

    Neurodevelopmental disorders that impact social behavior often show striking sex differences in incidence, progression, and symptom severity.

    “Neurodevelopmental disorders that impact social behavior often show striking sex differences in incidence, progression, and symptom severity (Rutter et al., 2003; Fombonne, 2009; Abel et al., 2010).”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites Rutter et al., 2003 source
    • cites Fombonne, 2009 source
    • cites Abel et al., 2010 source

      The available copy provides the title and bibliographic metadata, but no substantive passage about incidence, progression, or symptom severity. Searches for those terms and for age of onset and course returned only the title, so the attributed claim cannot be checked against our copy. (LLM, conf=0.70)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation

    Prenatal exposure to an immune challenge, lipopolysaccharide (LPS), decreases both play and BNST AVP mRNA of juvenile male rats.

    “prenatal exposure to an immune challenge, lipopolysaccharide (LPS), decreases both play and BNST AVP mRNA of juveniles male rats (Taylor et al., 2012).”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites Taylor et al., 2012 source

  • May combine two claims.

    Findingown data

    The number of pins increased across age in female weanling rats but not in males.

    “The number of Pins increased across age (main effect of age, P < 0.002, two-way ANOVA), but only in females (interaction, P < 0.04, two-way ANOVA).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Only levels of Pins were affected by the differing ages of the playmates, which were variable and low in number in the weanlings.

    “Only levels of Pins were affected by the differing ages of the playmates, which were variable and low in number in the weanlings.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In Experiment 2, there was an overall increase in Total Play, Pounces, and Boxing events across age.

    “There was an overall increase in Total Play, Pounces, and Boxing events across age (main effect of age, P < 0.008 for all 3 measures, two-way ANOVA).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Total Play and Pounces increased across age in weanling rats.

    “Total Play (data not shown) and Pounces (Figure 1C) increased across age (main effect of age, P < 0.005 for both measures, two-way ANOVA).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    There were no differences in Total Play, Pins, Pounces, or Boxing between male and female juvenile rats.

    “There were no differences in Total Play, Pins, Pounces, or Boxing between male and female juvenile rats (P > 0.32 for all measures, Student’s t-test; Figures 1B, D; Total Play and Boxing data not shown).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    In Experiment 2, no main effects or interaction were seen for Pins.

    “No main effects or interaction were seen for Pins (main effect of age, P > 0.4; main effect of sex, P > 0.09; interaction, P > 0.60, two-way ANOVA; Figure 2).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the PVN, AVP expression was similar between males and females and did not vary significantly with age.

    “In contrast to the BNST, the PVN showed similar AVP expression between males and females, which did not vary significantly with age (main effect of sex, P > 0.4; main effect of age, P > 0.11; interaction, P > 0.98, two-way ANOVA; Figure 3F).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingown data

    The radioactive signal from AVP expression in the PVN was much greater than that in the BNST and appeared overexposed in the majority of cases.

    “The radioactive signal from AVP expression in the PVN was much greater than that in the BNST, and appeared overexposed in the majority of cases.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    There was no effect of sex and no sex-by-age interaction on Total Play or Pounces in weanling rats.

    “However, there was no effect of sex and the interaction was not significant (P > 0.05 for both measures, two-way ANOVA).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Boxing behavior was low and did not differ across age or between sexes in weanling rats.

    “Boxing was low and did not differ across age or between sex (age, sex, interaction, P > 0.05; two-way ANOVA; data not shown).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Play emerged more rapidly in females than in males, resulting in a sex difference (females > males).

    “Unexpectedly, play emerged more rapidly in females than in males, resulting in a sex difference (females > males) counter to that traditionally reported in juvenile rats (e.g., Meaney and Stewart, 1981b).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The reversed sex difference did not persist beyond the weanling period; sex differences were not detected in 35-day-old juvenile rats tested under the same conditions.

    “This “reversed” sex difference did not persist beyond the weanling period, as sex differences were not detected in the 35-day-old juvenile rats tested under the same conditions (Figure 1).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingcitation

    Play first emerged around 18-19 days of age.

    “As in previous studies, play first emerged around 18–19 days of age (Bolles and Woods, 1964; Panksepp, 1981; Thiels et al., 1990).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Bolles and Woods, 1964 source
    • cites Panksepp, 1981 source
    • cites Thiels et al., 1990 source

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Testing each animal only one time ensured that effects seen were due to developmental changes rather than experience of repeated testing.

    “Testing each animal only one time ensured that effects seen in the current study were due to developmental changes rather than experience of repeated testing.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    The use of a juvenile stimulus rat ensured pups were paired with a motivated playmate and their play behavior was not suppressed by an unwilling partner.

    “To ensure that pups were paired with a motivated playmate and that their play behavior was not suppressed by an unwilling partner, each weanling-aged rat was tested with a juvenile (35 days of age) of the same-sex that had been single-housed for 24 h before testing”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    Differential neuropeptide regulation of male and female social development may underlie well-documented sex differences in incidence, progression, and symptom severity of behavioral disorders during development.

    “Differential neuropeptide regulation of male and female social development may underlie well-documented sex differences in incidence, progression, and symptom severity of behavioral disorders during development.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Sex differences in neurobiological mechanisms that influence social development contribute to differential vulnerability to neurodevelopmental disorders.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The BNST is a primary node in the neural network thought to play a role in social behavior.

    “The lateral septum receives projections from the BNST (De Vries and Buijs, 1983), a primary node in the neural network thought to play a role in social behavior (Newman, 1999).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Newman, 1999 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In rats, 24 h of isolation further stimulates play.

    “in rats, play peaks around 30–40 days of age, and 24 h of isolation further stimulates play (Panksepp, 1981).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Panksepp, 1981 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    AVP has been implicated in a number of adult social behaviors.

    “The neuropeptide arginine vasopressin (AVP) has been implicated in a number of adult social behaviors (reviewed in Caldwell et al., 2008).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Caldwell et al., 2008 source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    ASD and ADHD are much more common in boys than in girls.

    “This is particularly striking among disorders affecting social development such as autism spectrum disorders (ASD) and attention deficit hyperactivity disorder (ADHD), which are much more common in boys than in girls (reviewed in Rutter et al., 2003).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Rutter et al., 2003 source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    Pins in Experiment 2 appeared to be hindered by the large body size of the juvenile stimulus playmate.

    “This time, however, the effect was stronger for Total Play and Pounces than it was for Pins, which appeared to be hindered by the large body size of the juvenile stimulus playmate.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Play fighting in rats emerges around 18 days of age, peaks at 30-40 days of age, and declines thereafter.

    “Play fighting in rats emerges around 18 days of age, peaks at 30–40 days of age, and declines thereafter (Panksepp, 1981).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Panksepp, 1981 source

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    Pairing weanlings with a motivated juvenile stimulus rat removed the need to isolate experimental weanlings prior to the play test, avoiding confounding measures of AVP expression.

    “Pairing weanlings with a motivated juvenile stimulus rat also removed the need to isolate the experimental weanlings prior to the play test, a procedure that would confound measures of AVP expression.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductown data

    Play behavior was scored by a researcher blind to treatment conditions.

    “were scored by a researcher blind to the treatment conditions using JWatcher software.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    AVP cells within the BNST are sensitive to sex steroids and exhibit the most consistent sexual dimorphism found across vertebrates, with more cells in males than in females.

    “Furthermore, AVP cells within this nucleus are sensitive to sex steroids and exhibit the most consistent sexual dimorphism found across vertebrates, with more cells in males than in females (De Vries and Panzica, 2006).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites De Vries and Panzica, 2006 source

  • May combine two claims.

    Interpretationreasoning

    AVP acts on multiple systems, with both stimulatory and inhibitory actions on play.

    “This suggests that AVP acts on multiple systems, with both stimulatory and inhibitory actions on play.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Evidence is mounting that social and affective disorders involve perturbations in AVP and other neuropeptide systems.

    “Evidence is now mounting that social and affective disorders involve perturbations in AVP and other neuropeptide systems (e.g., Heinrichs et al., 2009; Harony and Wagner, 2010).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Heinrichs et al., 2009 source
    • cites Harony and Wagner, 2010 source

  • May combine two claims.

    Interpretationreasoning

    Different AVP systems have distinct influences on male play early in development, perhaps with BNST and PVN AVP systems opposing each other.

    “our findings when considered with those discussed above suggest that different AVP systems have distinct influences on male play early in development, perhaps with BNST and PVN AVP systems opposing each other.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    AVP has a complex role in social development that differs by age and sex.

    “Collectively, these studies indicate a complex role for AVP in social development that differs by age and sex.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Interpretationreasoning

    Only males would be subject to BNST AVP inhibition, and AVP's decline around weaning may facilitate play development in males.

    “Therefore only males would be subject to this inhibition, and AVP’s decline around weaning (present results; Szot and Dorsa, 1993) may facilitate play development in this sex.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Premisecitation

    Early-life experience can impact later levels of juvenile play in a sex-dependent manner.

    “Early-life experience can also impact later levels of juvenile play in a sex-dependent manner (Parent and Meaney, 2008).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Parent and Meaney, 2008 source
41 of 41

  • The paper relies on this without support.

    Sex differences in neurobiological mechanisms that influence social development contribute to differential vulnerability to neurodevelopmental disorders.

    “Sex differences in neurobiological mechanisms that influence social development likely contribute to this differential vulnerability.”

  • The paper relies on this without support.

    AVP plays an important role in social behavior during adolescence.

    “AVP may play an equally important role in social behavior during adolescence.”

  • The paper relies on this without support.

    AVP mRNA expression in the BNST and PVN reflects functional AVP system activity relevant to social play.

    “AVP mRNA expression in the BNST and PVN was analyzed using the exposed film.”

  • The paper relies on this without support.

    The neural circuits through which AVP influences juvenile social play are not known.

    “the circuits through which AVP influences play are not known”
4 of 4

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • A negative correlation was found between AVP mRNA expression in the bed nucleus of the stria terminalis and social play in juvenile males.

    “In line with this, a negative correlation was found between AVP mRNA expression in the bed nucleus of the stria terminalis and social play in juvenile males (Paul et al., 2014).”

    From Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context (2014) · cites this paper as Paul et al., 2014

    Experiment 2 reports a significant negative correlation between BNST AVP mRNA and play in male rats aged 18 and 21 days. The Discussion distinguishes the weanlings tested in this study from juveniles tested in another study, so “juvenile males” is broader than the study population. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • Juvenile social play contributes to the development of adult social and emotional skills in humans and non-human animals.

    “Juvenile social play contributes to the development of adult social and emotional skills in humans and non human animals [1–6]”

    From Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats (2020) · cites this paper as [5]

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.

  • Figure 3 assigns panel E to two different contents

    Minor

    The caption identifies panel E as a representative PVN image, but also identifies it as a panel showing the correlation between PVN AVP mRNA and play. Elsewhere in the caption, panel G is identified as the female PVN correlation.

  • Experiment 1a lists an 18-day-old recording outside its test ages

    Minor

    Experiment 1a says pups were tested at 16, 19, 21, or 24 days of age, but then says an 18-day-old female play pair was recorded and excluded from scoring.

2 of 2

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Related

Authors
Paul, M. J., Terranova, J. I., Probst, C. K., Murray, E. K., Ismail, N. I., & de Vries, G. J.
Affiliations
  • Georgia State University (US)
  • University of Massachusetts Amherst (US)
  • University of Ulster (GB)
  • University of Ottawa (CA)
Corresponding author
Paul, Matthew J.
ORCID
Venue
Frontiers in Behavioral Neuroscience
Publisher
Frontiers Media SA
Published
2014
Volume
8
Pages
58-58
ISSN
1662-5153 (ISSN-L)
DOI
10.3389/fnbeh.2014.00058
PMC
PMC3937588
OpenAlex
W2155589586
Semantic Scholar
ae3bdd3e2726c5946731f1b6576611632a5ab4f6
Cited by
51
References
53
Citations by year
2026: 3 · 2025: 1 · 2024: 5 · 2023: 7 · 2022: 3 · 2021: 2 · 2020: 5 · 2019: 4 · 2018: 8 · 2017: 4 · 2016: 3 · 2015: 3 · 2014: 2
FWCI
5.72
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Ulster University Research Portal (Ulster University) (submittedVersion, cc-by)
  • Europe PMC (PubMed Central) (submittedVersion, cc-by)
  • PubMed Central (submittedVersion, cc-by)
  • Digital Archive @ GSU (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Counseling And Psychological Services Dissertations (Georgia State University) (submittedVersion, cc-by)
Funders
National Institute of Mental Health (RO1 MH47538, MH47538, R01-MH047538)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
vasopressin, social play, sex differences, young rats, social development (developmental psychology), bed nucleus of the stria terminalis, paraventricular nucleus, weaning, neuropeptide regulation, behavioral disorders

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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