Play in Rats: Association across Contexts and Types, and Analysis of Structure
Open accessAbstract
Play has been proposed as a promising indicator of positive animal welfare.We aimed to study play in rats across contexts (conspecific/heterospecific) and types (social: pinning, being pinned; solitary: scampering), and we investigated its structure using behavioral sequence analysis.Group-housed (three per cage) adolescent male Lister Hooded rats (n = 21) were subjected to a Play-In-Pairs test: after a 3 hour isolation period, a pair of cagemates was returned to the home cage and both social and solitary play were scored for 20 min.This procedure was repeated for each pair combination across three consecutive days, and individual play scores were calculated.Heterospecific play was measured using a Tickling test: rats were individually tickled by the experimenter through bouts of gentle, rapid finger movements on their underside, and the number of positive 50 kHz frequency modulated vocalizations and experimenter-directed approach behaviors were recorded.Both of the above tests were compared with social play in the home cage.While conspecific play in both the Play-In-Pairs test and home cage were correlated, both seemed to be unrelated to heterospecific play in the Tickling test.During the Play-In-Pairs test, although both solitary and social play types occurred, they were unrelated, and solitary locomotor play of one rat did not predict the subsequent play behavior of its cage mate.Analysis of play structure revealed that social play occurred more often in bouts of repeated behaviors while solitary play sequences did not follow a specific pattern.If play is to be used as an indicator of positive welfare in rats, context, type and structure differences should be taken into account. Keywords -Play,
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Written from the paper’s full text.
TL;DR
Play in adolescent male rats was consistent across two conspecific contexts but unrelated to heterospecific tickling-induced vocalizations. Social and solitary play were also unrelated, and social play sequences were characterized by repeated same behaviors rather than alternations, whereas solitary play showed no clear sequence pattern.
Key findings
- Social play occurred more often than solitary play in the Play-In-Pairs test (t(20) = 7.55, p < 0.001), and social play frequency and duration were highly correlated (r = 0.93, p < 0.001).
- Home-cage social play was related to Play-In-Pairs social play (r(18) = 0.57, p = 0.008), but tickling-induced positive vocalizations were unrelated to both home-cage social play (rs = 0.28, n.s.) and Play-In-Pairs social play (rs = -0.07, n.s.).
- Solitary play was unrelated to social play duration (r(18) = 0.16, n.s.), and one rat’s solitary play did not significantly predict its cage mate’s subsequent play behavior (F(2,40) = 0.27, n.s.).
- Social play showed more repetitions than alternations (t(20) = 9.89, p < 0.001), while solitary play did not (t(20) = -0.18, n.s.); positive vocalizations during tickling bouts correlated with those outside bouts (rs = 0.83, p < 0.001) and with approach behavior (H(3) = 8.68, p = 0.03).
Methods
- Subjects were 21 male Lister Hooded rats, housed three per cage, tested between five and eight weeks of age during the dark phase.
- Play was measured in a conspecific Play-In-Pairs test after 3 hr isolation, scored for 20 min over three consecutive days (d 41–43); a heterospecific Tickling test on d 54 recorded positive 50 kHz frequency-modulated vocalizations and approach behavior; home-cage social play was recorded on d 44 during the first hour of darkness.
- Analyses used SPSS v22 with transformations or non-parametric tests as needed, partial correlations controlling for cage, Spearman correlations, Kruskal-Wallis tests, paired t-tests, and repeated-measures ANOVA for behavioral sequences.
Limitations
- Stated: social play structure analysis was limited to pinning behavior; individual positive vocalizations during conspecific play could not be recorded; the Play-In-Pairs and Tickling tests were 13 days apart, so developmental changes may have masked a relationship.
- Stated: the home cage’s relatively small space and high isolation-induced motivation meant play initiations almost exclusively led to pinning, with few other defensive strategies, making comparison with studies separating dorsal contacts and pinning difficult; short tickling habituation may have lowered vocalization rates.
- Evident: the sample was small (n = 21), all male, one strain, and laboratory-housed, and the main cross-context findings are correlational, so causal or generalizable claims are constrained.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
2 of 71 cited sources checked · 2 supported · 0 flagged
- Premisecitation
Solitary locomotor play is part of the locomotor-rotational behavioral repertoire that can occur before and after conspecific social contact.
“Solitary locomotor play (described as 'running' by Pellis & Pellis, 1983) is part of the locomotorrotational behavioral repertoire that can occur before and after conspecific social contact (Pellis & Pellis, 1983;Wilson & Kleiman, 1974).”
Quote in the paperNot a substantial claim1 of 2 sources checked - Findingown data
Conspecific play in the Play-In-Pairs test and home cage were correlated.
“While conspecific play in both the Play-In-Pairs test and home cage were correlated, both seemed to be unrelated to heterospecific play in the Tickling test.”
Quote in the paperSubstantial claim - Findingown data
Solitary and social play types were unrelated during the Play-In-Pairs test.
“During the Play-In-Pairs test, although both solitary and social play types occurred, they were unrelated, and solitary locomotor play of one rat did not predict the subsequent play behavior of its cage mate.”
Quote in the paperSubstantial claim - Findingown data
Conspecific play in both the Play-In-Pairs test and home cage was unrelated to heterospecific play in the Tickling test.
“While conspecific play in both the Play-In-Pairs test and home cage were correlated, both seemed to be unrelated to heterospecific play in the Tickling test.”
Quote in the paperSubstantial claim - Findingown data
Solitary locomotor play of one rat did not predict the subsequent play behavior of its cage mate.
“During the Play-In-Pairs test, although both solitary and social play types occurred, they were unrelated, and solitary locomotor play of one rat did not predict the subsequent play behavior of its cage mate.”
Quote in the paperSubstantial claim
- Findingown data
Solitary play sequences did not follow a specific pattern.
“Analysis of play structure revealed that social play occurred more often in bouts of repeated behaviors while solitary play sequences did not follow a specific pattern.”
Quote in the paperSubstantial claim - Findingown data
Social play occurred more often in bouts of repeated behaviors.
“Analysis of play structure revealed that social play occurred more often in bouts of repeated behaviors while solitary play sequences did not follow a specific pattern.”
Quote in the paperSubstantial claim - Findingown data
The number of fecal boli tended to be negatively correlated with positive vocalizations during tickling.
“yet tended to be negatively correlated with positive vocalizations during tickling (r s = -0.40,p = 0.07).”
Quote in the paperNot a substantial claim - Findingown data
The Play-Role index was positively correlated with Pinning duration.
“The Play-Role index was positively correlated with Pinning duration (ṟ (18) = 0.45, p = 0.04), but was unrelated to Being Pinned duration (ṟ (18) = -0.17,n.s.).”
Quote in the paperNot a substantial claim - Findingown data
Behavioral repetitions were not more frequent than alternations for solitary play behavior.
“but not for solitary play behavior (t(20) = -0.18,n.s.; Figure 2b).”
Quote in the paperNot a substantial claim - Findingown data
Behavioral repetitions were more frequent than alternations for social play behaviors.
“behavioral repetitions were more frequent than alternations for social play behaviors (t(20) = 9.89, p < 0.001; Figure 2a)”
Quote in the paperSubstantial claim - Findingown data
Positive vocalizations during tickling were unrelated to social play in the home cage.
“positive vocalizations during tickling were unrelated to both social play in the home cage (r s = 0.28, n.s.)”
Quote in the paperSubstantial claim - Findingown data
Social play occurred more often than solitary play in the Play-In-Pairs test.
“Social play (average between Pinning and Being Pinned frequencies) occurred more often than solitary play (Scampering frequency; t(20) = 7.55, p < 0.001).”
Quote in the paperNot a substantial claim - Findingown data
Positive vocalizations emitted during tickling bouts highly correlated with those emitted in the remaining time of the tickling session.
“Positive vocalizations emitted during tickling bouts highly correlated with those emitted in the remaining time of the tickling session (r s = 0.83, p < 0.001).”
Quote in the paperSubstantial claim - Findingown data
Frequency of solitary play was unrelated to social play duration.
“Frequency of solitary play (Scampering behavior) was unrelated to social play duration (ṟ (18) = 0.16, n.s.).”
Quote in the paperNot a substantial claim - Findingown data
The number of fecal boli and the latency to eat the cereal were correlated.
“The number of fecal boli (1.48 ± 0.33, range 0-4) and the latency to eat the cereal (104.1 ± 7.0 s, range 45-150 s) were correlated (r s = 0.54, p = 0.01).”
Quote in the paperSubstantial claim - Findingown data
Social play in the home cage was related to social play in the Play-In-Pairs test.
“Social play in the home cage was related to social play in the Play-In-Pairs test (ṟ (18) = 0.57, p = 0.008; Figure 4)”
Quote in the paperSubstantial claim - Findingreasoning
Social play events in the Play-In-Pairs test occurred more often than solitary play.
“Social play events (average between Pinning and Being Pinned frequencies) in the Play-In-Pairs test occurred more often than solitary play.”
Quote in the paperNot a substantial claim - Findingown data
93.7% (± 2.2%) of home cage social play was observed in the first 30 min of darkness.
“of which 93.7 % (± 2.2 %) was observed in the first 30 min of darkness.”
Quote in the paperNot a substantial claim - Findingown data
Solitary play was unrelated to social play duration.
“Solitary play was unrelated to social play duration”
Quote in the paperSubstantial claim - Findingown data
The Play-Role index positively correlated with Pinning duration.
“the Play-Role index positively correlated with Pinning duration”
Quote in the paperSubstantial claim - Findingown data
The Approach Behavior score was related to positive vocalizations.
“The Approach Behavior score (range 0-3) was related to positive vocalizations (H(3) = 8.68, p = 0.03; Figure 3).”
Quote in the paperNot a substantial claim - Findingown data
The Play-Role index was unrelated to Being Pinned duration.
“The Play-Role index was positively correlated with Pinning duration (ṟ (18) = 0.45, p = 0.04), but was unrelated to Being Pinned duration (ṟ (18) = -0.17,n.s.).”
- Also stated in: § Social and Solitary Play Types · plain
“but was unrelated to Being Pinned duration”
Quote in the paperSubstantial claim - Also stated in: § Social and Solitary Play Types · plain
- Findingown data
The number of fecal boli was unrelated to solitary play in the Play-In-Pairs test.
“and to social and solitary play in the Play-In-Pairs test (r s = 0.15, n.s., and r s = 0.24, n.s., respectively)”
Quote in the paperNot a substantial claim - Findingown data
The mean frequency of social play in the home cage during the first hour of the dark phase was 31.5 ± 1.7.
“The mean frequency of social play in the home cage during the first hour of the dark phase was 31.5 ± 1.7”
Quote in the paperNot a substantial claim - Findingown data
Positive vocalizations during tickling were unrelated to social play in the Play-In-Pairs test.
“and in the Play-In-Pairs test (r s = -0.07,n.s.).”
Quote in the paperSubstantial claim - Findingown data
The number of fecal boli was unrelated to social play in the home cage.
“The number of fecal boli was unrelated to social play in the home cage (r s = 0.12, n.s.)”
Quote in the paperNot a substantial claim - Findingown data
The number of fecal boli was unrelated to social play in the Play-In-Pairs test.
“and to social and solitary play in the Play-In-Pairs test (r s = 0.15, n.s., and r s = 0.24, n.s., respectively)”
Quote in the paperNot a substantial claim - Findingown data
The proportions of each play behavior that one animal performed following solitary play of its cage mate were not significantly different.
“The proportions of each play behavior (of total play events) that one animal performed following solitary play of its cage mate were not found to be significantly different (F(2,40) = 0.27, n.s.).”
Quote in the paperNot a substantial claim - Findingreasoning
Initiations of social play almost exclusively led to pinning behavior, with very few instances of other playful defensive strategies such as partial rotation and evasion.
“Likely due to the relatively small space available in the home cage and to the high motivation to play induced by isolation, initiations of social play (i.e., attacks to the nape) almost exclusively led to pinning behavior, with very few instances of other playful defensive strategies such as partial rotation and evasion (preliminary experimenter's observations; see also Pellis & Pellis, 1991;Pell”
Quote in the paperSubstantial claim0 of 2 sources checked - Findingown data
The factor 'cage' did not influence the relationship between any of the variables.
“The factor 'cage' was not found to influence the relationship between any of our variables.”
Quote in the paperNot a substantial claim - Findingown data
Frequencies and durations of social play were highly correlated.
“Frequencies and durations of social play were highly correlated (ṟ (18) = 0.93, p < 0.001), thus only durations (a more comprehensive measure), were used for further data analysis concerning social play.”
Quote in the paperSubstantial claim - Premisecitation
Panksepp and Burgdorf (1999) found little or no evidence for associations between social play and other play behaviors such as pinning.
“While Panksepp and Burgdorf (1999) found a positive association between initiations of social play and vocalizations during tickling at 44 days old, this was not found at 58 days old, and little or no evidence was found for associations with other play behaviors (i.e., 'pinning').”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Panksepp and Burgdorf (1999)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Social isolation increases the motivation to initiate play in adolescent rats.
“Though individual play motivation can be influenced by several factors, social isolation increases the motivation to initiate play in adolescent rats, and the increase in play depends on the duration of isolation (Niesink & van Ree, 1989;Vanderschuren, Stein et al., 1995).”
Quote in the paperSubstantial claim0 of 2 sources checked - Premisecitation
Play can act as a reinforcer in the same way as food and sex.
“Play can also act as a reinforcer in the same way as food and sex (Vanderschuren, 2010), since the same neurotransmitters that mediate the motivational and hedonic properties of reward have been shown to also affect social play in rats (Burgdorf & Panksepp, 2006;Vanderschuren, 2010).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Vanderschuren, 2010
- Study design and conductcitation
Repeated play sessions using different pair combinations of cage mates provides a measure of individual playfulness that is at least partly independent from the playfulness of the play partners.
“Repeated play sessions using different pair combinations of cage mates provides a measure of individual playfulness that is at least partly independent from the playfulness of the play partners (Pellis & McKenna, 1992).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis & McKenna, 1992 source
- Premisecitation
Rats exhibit social play, commonly referred to as play-fighting or rough-and-tumble play.
“Firstly, like most social mammals, rats exhibit social play, commonly referred to as play-fighting, or rough-and-tumble play (Pellis & Pellis, 2007), which is ideal for comparative research.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis & Pellis, 2007 source
- Premisecitation
The same neurotransmitters that mediate the motivational and hedonic properties of reward also affect social play in rats.
“Play can also act as a reinforcer in the same way as food and sex (Vanderschuren, 2010), since the same neurotransmitters that mediate the motivational and hedonic properties of reward have been shown to also affect social play in rats (Burgdorf & Panksepp, 2006;Vanderschuren, 2010).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Burgdorf & Panksepp, 2006 source
- cites Vanderschuren, 2010
- Premisecitation
Rats emit frequency modulated 50 kHz calls in both conspecific and heterospecific play contexts (tickling).
“Rats emit these frequency modulated 50 kHz calls in both conspecific and heterospecific play contexts ('tickling' administered by the experimenter; Panksepp & Burgdorf, 1999), and some evidence suggests that they will self-administer the playback of such calls if given the possibility to do so (Burgdorf et al., 2008).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Panksepp & Burgdorf, 1999
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Webber et al. (2012) found that rats selectively bred for higher vocalization rates during tickling showed lower durations of pinning behavior during play.
“Webber et al. (2012) found that while rats selectively bred for higher vocalization rates during tickling showed more initiations of play, compared with rats selected for lower vocalization rates, they showed lower durations of 'pinning' behavior during play.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Webber et al. (2012) source
- Premisecitation
Social isolation increases the probability that play initiations result in the play partner being pinned, as opposed to adopting other defensive strategies.
“Social isolation also increases the probability that play initiations result in the play partner being pinned, as opposed to adopting other defensive strategies (Pellis et al., 1997).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Pellis et al., 1997 source
- Premisecitation
A period of social isolation is often used to induce high rates of play behavior in rats within a short time interval.
“A period of social isolation is often used to induce high rates of play behavior in rats within a short time interval (Niesink & van Ree, 1989;Panksepp & Beatty, 1980;Vanderschuren, Niesink, Spruijt, 1995;Vanderschuren, Stein, Wiegant, & van Ree, 1995).”
Quote in the paperSubstantial claim0 of 3 sources checked - Premisecitation
Play fighting in rats is distinguishable from aggressive behavior.
“Play fighting in rats has been thoroughly studied and characterized (Pellis & McKenna, 1992;Pellis et al., 1997), and is distinguishable from aggressive behavior (Pellis & Pellis, 1987).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis & Pellis, 1987 source
- Interpretationreasoning
Rats can serve as a promising model for the study of play and emotional state.
“Such properties of play have been studied extensively in rats (Douglas, Varlinskaya, & Spear, 2004;Knutson, Burgdorf, & Panksepp, 1998;Panksepp, 1981;Pellis, Field, Smith, & Pellis, 1997;Pellis & McKenna, 1992;Pellis & Pellis, 1987;Vanderschuren, 2010), and rats can serve as a promising model for the study of play and emotional state for a number of reasons.”
Quote in the paperNot a substantial claim - Premisecitation
Play partners can influence each other in a contagious way, i.e., a highly playful rat may induce more frequent play in its partner.
“Play partners can influence each other in a contagious way, i.e., a highly playful rat may induce more frequent play in its partner (Pellis & McKenna, 1992), therefore the analysis of sequences of play behavior between rats can shed light on possible associations between different types of play, namely social and locomotor play.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis & McKenna, 1992 source
- Premisecitation
The increase in play after social isolation depends on the duration of isolation.
“Though individual play motivation can be influenced by several factors, social isolation increases the motivation to initiate play in adolescent rats, and the increase in play depends on the duration of isolation (Niesink & van Ree, 1989;Vanderschuren, Stein et al., 1995).”
Quote in the paperNot a substantial claim0 of 2 sources checked - Premisecitation
Only two studies have investigated whether conspecific social play is related to vocalizations induced by tickling.
“While studies have reported that the same positive vocalizations produced during play (and sex) are also emitted during tickling (Burgdorf et al., 2008), only two studies have investigated whether conspecific social play (Rough-and-Tumble play) is related to vocalizations induced by tickling (Panksepp & Burgdorf, 1999;Webber et al., 2012).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Panksepp & Burgdorf, 1999
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Webber et al., 2012 source
- Premisecitation
Individual consistency of play across conspecific and heterospecific contexts has been scarcely investigated in rats.
“While studies have reported that the same positive vocalizations produced during play (and sex) are also emitted during tickling (Burgdorf et al., 2008), only two studies have investigated whether conspecific social play (Rough-and-Tumble play) is related to vocalizations induced by tickling (Panksepp & Burgdorf, 1999;Webber et al., 2012).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Burgdorf et al., 2008
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Panksepp & Burgdorf, 1999
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Webber et al., 2012 source
- Premisecitation
Webber et al. (2012) found that rats selectively bred for higher vocalization rates during tickling showed more initiations of play compared with rats selected for lower vocalization rates.
“Webber et al. (2012) found that while rats selectively bred for higher vocalization rates during tickling showed more initiations of play, compared with rats selected for lower vocalization rates, they showed lower durations of 'pinning' behavior during play.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Webber et al. (2012) source
- Interpretationown data
Our result confirms the finding of Panksepp and Burgdorf (1999) that conspecific pinning behavior is unrelated to positive vocalizations during tickling.
“While our result seem to confirm the finding of Panksepp and Burgdorf (1999) that conspecific pinning behavior is unrelated to positive vocalizations during tickling”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Panksepp and Burgdorf (1999)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationreasoning
All animals experienced at least a moderate level of anxiety during testing in the Novelty-Induced Suppression-of-Feeding test.
“In the Novelty-Induced Suppression-of-Feeding test, since the minimum latency for a rat to eat the sweetened cereal was 45 seconds, and up to four fecal boli were produced, we conclude that all animals experienced at least a moderate level of anxiety during testing.”
Quote in the paperNot a substantial claim - Interpretationreasoning
Positive vocalizations at tickling might reflect general lower levels of anxiety in the presence of the experimenter('s hand) and not necessarily levels of playfulness.
“This suggests that positive vocalizations at tickling might reflect general lower levels of anxiety in the presence of the experimenter('s hand) and not necessarily levels of playfulness.”
Quote in the paperSubstantial claim - Premiseown data
Different types of play may have had independent evolutionary origins and trajectories.
“supporting the theory that different types of play may have had independent evolutionary origins and trajectories (Burghardt, 2005).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Burghardt, 2005 source
- Interpretationown data
Our finding contrasts with Webber et al. (2012), who found some indications that different play behaviors were associated with animals selected for high and low levels of positive vocalizations during tickling.
“However, our finding contrasts with Webber et al. (2012), who found some indications that different play behaviors were associated with animals selected for high and low levels of positive vocalizations during tickling (i.e., high responders performed more dorsal contacts while low responders performed more pinning behaviors on some testing days).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Webber et al. (2012) source
- Interpretationown data
Alterations in affective state induced by tickling (or the anticipation of it) extended to the entire testing session.
“Our results also suggest that alterations in affective state induced by tickling (or the anticipation of it) extended to the entire testing session.”
Quote in the paperSubstantial claim - Premisecitation
Changes in ratio between the occurrence of play initiations (attacks to the nape) and playful defensive strategies (e.g., Pinning) have been shown to occur across a longer period of time (pre-vs.post-sexual maturity).
“However, changes in ratio between the occurrence of play initiations (i.e., attacks to the nape) and playful defensive strategies (e.g., Pinning) have been shown to occur, though across a longer period of time (pre-vs.post-sexual maturity; Pellis & Pellis, 1991).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis & Pellis, 1991 source
- Interpretationown data
Individual playfulness in rats was consistent across two conspecific play contexts: home cage play in the first hour of the dark phase and play of pairs of cage mates after a short isolation period.
“Individual playfulness in rats was consistent across two conspecific play contexts, namely play in the home cage in the first hour of the dark phase, and play of pairs of cage mates after a short isolation period.”
Quote in the paperSubstantial claim - Interpretationown data
The Play-In-Pairs test can be a useful tool for a relatively quick assessment of playfulness.
“This result supports previous research suggesting that the Play-In-Pairs test can be a useful tool for a relatively quick assessment of playfulness (Niesink & van Ree, 1989;Pellis & McKenna, 1992;Vanderschuren, Stein et al., 1995).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationreasoning
When play roles were more different, higher overall levels of Pinning were performed.
“indicating that when play roles were more different, higher overall levels of Pinning were performed.”
Quote in the paperSubstantial claim - Study design and conductcitation
The 3 hr isolation period was chosen because it was shown to induce a substantial increase of social play in rats without reaching a ceiling effect.
“This isolation period was chosen because it was shown to induce a substantial increase of social play in rats, without reaching a ceiling effect (Niesink & van Ree, 1989;Vanderschuren, Niesink et al., 1995;Vanderschuren, Stein et al., 1995).”
Quote in the paperSubstantial claim0 of 3 sources checked - Interpretationown data
These play types are unrelated in rats.
“suggesting that these play types are unrelated in rats”
Quote in the paperSubstantial claim - Interpretationown data
The animals did not find the tickling procedure to be aversive.
“they did not produce fecal boli or emit negative vocalizations during testing, indicating that they did not find the procedure to be aversive.”
Quote in the paperSubstantial claim - Premisecitation
Burgdorf et al. (2009) found that rats selected for high tickle responding showed less anxiety in an open field test than low tickle responders.
“However, similar to our findings, Burgdorf et al. (2009) found that rats selected for high tickle responding showed less anxiety in an open field test than low tickle responders.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Burgdorf et al. (2009)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Classified as probably not a substantial claim. 23
- May combine two claims. 18
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationAn overall decrease in pinning behavior would be expected between 41 and 54 days of age.
“While an overall decrease in pinning behavior would be expected between 41 and 54 days of age (Takahashi & Lore, 1983;Thor & Holloway, 1984)”
Quote in the paperNot a substantial claim1 of 2 sources checkedMay combine two claims.
Findingown dataBoth solitary and social play types occurred during the Play-In-Pairs test.
“During the Play-In-Pairs test, although both solitary and social play types occurred, they were unrelated, and solitary locomotor play of one rat did not predict the subsequent play behavior of its cage mate.”
Quote in the paperNot a substantial claimMay combine two claims.
Findingnone givenAnimals did not produce fecal boli or emit negative vocalizations during the Tickling Test.
“Animals did not produce fecal boli or emit negative vocalizations during the Tickling Test.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Findingnone givenAll animals ate the sweetened cereal before the end of the Novelty-Induced Suppression-of-Feeding test.
“All animals ate the sweetened cereal before the end of the Novelty-Induced Suppression-of-Feeding test.”
Quote in the paperNot a substantial claimClassified as probably not a substantial claim.
PremisereasoningBehavioral sequence analysis within individuals can provide additional insight on the structure of a play bout and how this structure may vary according to play type.
“Moreover, behavioral sequence analysis within individuals can provide additional insight on the structure of a play bout, and how this structure may vary according to play type (i.e., solitary and social).”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationSome evidence suggests that rats will self-administer the playback of frequency modulated 50 kHz calls if given the possibility.
“Rats emit these frequency modulated 50 kHz calls in both conspecific and heterospecific play contexts ('tickling' administered by the experimenter; Panksepp & Burgdorf, 1999), and some evidence suggests that they will self-administer the playback of such calls if given the possibility to do so (Burgdorf et al., 2008).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Burgdorf et al., 2008
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). May combine two claims.
PremisecitationLocomotor-rotational play is expressed by rats and consists of 'run' and 'jerk-jump' behaviors.
“Locomotor-rotational play, though less studied, is also expressed by this species and consists of a number of 'run' and 'jerk-jump' behaviors (Pellis & Pellis, 1983).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Pellis & Pellis, 1983 source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPlay has been associated with terms such as 'fun', 'pleasure' and 'joy', which imply the subjective experience of positive emotions.
“Indeed, play has been associated with terms such as 'fun' (Bekoff, 2001;Spinka et al., 2001;Vanderschuren, 2010), 'pleasure' (Vanderschuren, 2010) and 'joy' (Panksepp, 2005), which imply the subjective experience of positive emotions (Boissy et al., 2007;Burgdorf & Panksepp, 2006;Fraser & Duncan, 1998).”
Quote in the paperNot a substantial claim0 of 3 sources checkedClassified as probably not a substantial claim.
PremisecitationVocalizations during play in rats have been proposed to represent accurate and measurable indicators of acute emotional state.
“Secondly, vocalizations during play in rats have been proposed to represent accurate and measurable indicators of acute emotional state (Burgdorf, Panksepp, & Moskal, 2011;Knutson, Burgdorf, & Panksepp, 2002).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Burgdorf, Panksepp, & Moskal, 2011
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Knutson, Burgdorf, & Panksepp, 2002 source
May combine two claims.
PremisecitationPanksepp and Burgdorf (1999) found a positive association between initiations of social play and vocalizations during tickling at 44 days old, but not at 58 days old.
“While Panksepp and Burgdorf (1999) found a positive association between initiations of social play and vocalizations during tickling at 44 days old, this was not found at 58 days old, and little or no evidence was found for associations with other play behaviors (i.e., 'pinning').”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Panksepp and Burgdorf (1999)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Classified as probably not a substantial claim.
PremisecitationPlayful contexts produce different types of play (e.g., solitary and/or social play) which are characterized by repeated yet non-stereotypic sequences of behavior.
“Playful contexts produce different types of play (e.g., solitary and/or social play) which are characterized by repeated yet non-stereotypic sequences of behavior (Burghardt, 2005).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Burghardt, 2005 source
Probably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationFrequency modulated 50 kHz calls reflect positively valenced emotional states.
“In particular, frequency modulated 50 kHz calls have been suggested to reflect positively valenced emotional states (Burgdorf et al., 2008;2011).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Burgdorf et al., 2008
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [2011]
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).
Study design and conductnone givenThe experimental design and methods were approved by the responsible authorities of the Canton of Bern, Switzerland (License no. BE 63/12).
“The experimental design and methods were approved by the responsible authorities of the Canton of Bern, Switzerland (License no.BE 63/12).”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPlay fighting in rats has been thoroughly studied and characterized.
“Play fighting in rats has been thoroughly studied and characterized (Pellis & McKenna, 1992;Pellis et al., 1997), and is distinguishable from aggressive behavior (Pellis & Pellis, 1987).”
Quote in the paperNot a substantial claim0 of 2 sources checkedMay combine two claims.
InterpretationreasoningBoth conspecific and heterospecific play have positive valence.
“While the above findings indicate that both conspecific and heterospecific play have positive valence, individual consistency of play across these contexts has been scarcely investigated in rats.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
InterpretationreasoningSome animals might have been involved in high levels of conspecific social play without this reflecting positive affect and therefore not relating to positive vocalizations at tickling.
“In this way, some animals might have been involved in high levels of conspecific social play without this reflecting positive affect and therefore not relating to positive vocalizations at tickling.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationIf two individuals have similar motivation to play they are both more likely to perform high levels of play, while individuals with divergent motivation to play could result in the less motivated animal not necessarily participating in play, but rather avoiding it if given the possibility to do so.
“it has been suggested that if two individuals have similar motivation to play they are both more likely to perform high levels of play, while individuals with divergent motivation to play could result in the less motivated animal not necessarily participating in play, but rather avoiding it if given the possibility to do so (Douglas et al., 2004;Varlinskaya et al., 1999;Vanderschuren, 2010).”
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.
PremisecitationDuring conspecific play, the vast majority of vocalizations were positive, suggesting that any potential negative component of play may be minimal.
“Also, Burgdorf et al. (2008) found that during conspecific play, the vast majority of vocalizations were positive, suggesting that any potential negative component of play may be minimal.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Burgdorf et al. (2008)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Classified as probably not a substantial claim.
PremisecitationPlay mates may vary in their intrinsic motivation to play.
“play mates may vary in their intrinsic motivation to play (Pellis & McKenna, 1992)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis & McKenna, 1992 source
Probably not a substantial claim: may not pass S3 (load-bearing).
InterpretationreasoningSocial deprivation may have favored a correlation between heterospecific play vocalizations and conspecific play behavior by drastically increasing the motivation towards any social contact.
“In addition, since in previous studies rats were individually housed since weaning (Burgdorf et al., 2008;Panksepp & Burgdorf, 1999), it is possible that social deprivation may have favored a correlation between heterospecific play vocalizations and conspecific play behavior by drastically increasing the motivation towards any social contact.”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Burgdorf et al., 2008
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites Panksepp & Burgdorf, 1999
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim: may not pass S4 (based).
Interpretationnone givenRats in the present study prioritized social play after a period of isolation.
“This is most likely due to the fact that rats in the present study prioritized social play after a period of isolation”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
InterpretationcitationThis result may relate to hierarchy formation, the onset of which already occurs during adolescence, and might be driven by repetitions of Pinning by the animals which are to become dominant.
“This result may relate to hierarchy formation, the onset of which already occurs during adolescence (Pellis & McKenna, 1992), and might be driven by repetitions of Pinning by the animals which are to become dominant (Pellis & McKenna, 1992;Pellis et al., 1997).”
Quote in the paperNot a substantial claim0 of 2 sources checkedProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationFecal boli is a more widely used proxy measure of anxiety.
“Production of fecal boli, being a more widely used proxy measure of anxiety (Archer, 1973;Ennaceur, Michalikova, & Chazot, 2006), was used to investigate relationships with play contexts.”
Quote in the paperNot a substantial claim0 of 2 sources checkedClassified as probably not a substantial claim. May combine two claims.
Study design and conductreasoningThe Play-In-Pairs test and the Tickling test were performed 13 days apart from each other, so developmental changes in play behavior during this period could have masked a potential relationship between the two tests.
“Finally, since the Play-In-Pairs test and the Tickling test were performed 13 days apart from each other, it cannot be excluded that developmental changes in play behavior during this period could have masked a potential relationship between the two tests.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataSocial play encounters were characterized by reiteration of either Pinning or Being Pinned behaviors, which occurred more frequently than inversions of play roles.
“indicating that social play encounters were characterized by reiteration of either Pinning or Being Pinned behaviors, which occurred more frequently than inversions of play roles.”
Quote in the paperSubstantial claimMay combine two claims.
Study design and conductown dataPreliminary observations indicated that initiations of play (dorsal contacts) and pinning behavior largely overlapped in this study, possibly due to the relatively small space available in the home cage.
“Since preliminary observations indicated that initiations of play (i.e., dorsal contacts) and pinning behavior largely overlapped in this study, possibly due to the relatively small space available in the home cage, a comparison with previous studies in which dorsal contacts and pinning were analyzed separately is more difficult to make.”
Quote in the paperSubstantial claimMay combine two claims.
InterpretationcitationTickling is rewarding and is associated with positive affect.
“confirming previous research showing that tickling is rewarding and is associated with positive affect (Burgdorf & Panksepp, 2001).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Burgdorf & Panksepp, 2001 source
May combine two claims.
Interpretationown dataMeasures of play in conspecific contexts appeared to be unrelated to heterospecific play as measured by positive vocalizations induced by tickling, suggesting that the two play contexts may be independent.
“Measures of play in conspecific contexts, however, appeared to be unrelated to heterospecific play as measured by positive vocalizations induced by tickling, suggesting that the two play contexts may be independent.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationown dataHierarchy formation was present and affected the play bouts already at the age of 41-43 days.
“This may support the fact that, although alternations of play roles are characteristic of social play in adolescent rats (Pellis et al., 1997), hierarchy formation was present and affected the play bouts already at the age of 41-43 days.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Pellis et al., 1997 source
Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
PremisecitationMä llo et al. (2007) reported emissions of negative vocalizations, which were more frequent in female compared to male rats.
“This is in contrast to Mä llo et al. (2007) who reported emissions of negative vocalizations, which however were more frequent in female compared to male rats”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Mä llo et al. (2007)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
May combine two claims.
Interpretationown dataSolitary play is not associated with the quantity of social play of the player or with the subsequent play behaviors of the play mate, at least for the play behaviors investigated in this study.
“This suggests that solitary play, which is not immediately directed at or induced by another individual, is not associated with the quantity of social play of the player or with the subsequent play behaviors of the play mate, at least for the play behaviors investigated in this study.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationPanksepp and Burgdorf (2000) previously demonstrated that rats show a higher rate of 50 kHz vocalizations in anticipation of tickling in a conditioned place preference test.
“Panksepp and Burgdorf (2000) previously demonstrated that rats show a higher rate of 50 kHz vocalizations in anticipation of tickling in a conditioned place preference test.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Panksepp and Burgdorf (2000) source
May combine two claims.
PremisecitationMä llo et al. (2007) did not find a difference in anxiety between high and low tickle responders, but frequency modulated 50 kHz vocalizations were not distinguished from flat 50 KHz ones, and the tickling procedure itself was found to have an anxiolytic effect in different test situations.
“Mä llo et al. (2007) did not find a difference in anxiety between high and low tickle responders, but frequency modulated 50 kHz vocalizations were not distinguished from flat 50 KHz ones, and the tickling procedure itself was found to have an anxiolytic effect in different test situations.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites Mä llo et al. (2007)
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).
PremisecitationBurgdorf et al. (2009) reported that rats produced fecal boli during tickling.
“and with Burgdorf et al. (2009) who reported that rats produced fecal boli during tickling.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Burgdorf et al. (2009)
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
The paper relies on this without support.
The intrinsic propensity to play (playfulness) is a stable trait that can be measured across contexts.
“The intrinsic propensity to play (i.e., the personality trait 'playfulness') across contexts may shed light on whether these are part of the same play dimension.”
The paper relies on this without support.
Approach behavior directed towards the experimenter's hand is a measure of positive affect in the tickling test.
“On d 53 and d 54, it was recorded whether an animal approached the experimenter's hand immediately after each tickling bout, and a combined Approach Behavior score (maximum 4 Approach Behaviors across 2 days) was calculated.”
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?
Play is not displayed continuously by young rats, but appears in peaks of relatively short duration across the day.
“Play is not displayed continuously by young rats, but appears in peaks of relatively short duration across the day (Melotti et al., 2014;Lampe et al., 2019).”
From Social Play Behavior Is Critical for the Development of Prefrontal Inhibitory Synapses and Cognitive Flexibility in Rats (2022) · cites this paper as Melotti et al., 2014
In “Relationships Between Home Cage Social Play and Other Play Contexts” (page not provided), the paper reports that 93.7% of the social play observed during the first hour of darkness occurred in its first 30 minutes. This supports a brief concentration of play rather than continuous play during that observation period, but the study did not observe play across the day or establish multiple daily peaks. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe patterns and correlations between USVs and specific behaviours are known to vary across contexts.
“For example, the patterns and correlations between USVs and specific behaviours are known to vary across contexts ( Burke et al., 2022; Melotti et al., 2014).”
From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Melotti et al., 2014
The Discussion reports that conspecific rough-and-tumble play was unrelated to vocalizations during heterospecific tickling, while the Heterospecific ‘Tickling’ Test reports an association between approach behavior and positive vocalizations. These findings support context-dependent associations between behavior and vocalizations, but the paper does not directly compare patterns of USV emission across contexts. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Statistics recomputed
Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.
- Consistentt(20) = 7.55reported p < .001 · recomputed p < .001
“t(20) = 7.55, p < .001”
- ConsistentF(2, 40) = 0.27reported n.s. · recomputed p = .765
“F(2,40) = 0.27, n.s.”
- Consistentt(20) = 9.89reported p < .001 · recomputed p < .001
“t(20) = 9.89, p < .001”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Self-check results appear here once an independent check has confirmed them.
Cites
Tests for emotionality in rats and mice: A review
Archer, J. (1973) · Animal Behaviour · doi:10.1016/s0003-3472(73)80065-x · Cited by 1,577 · cited 3× · see citing works
“The number of fecal boli and the latency to eat the sweetened cereal were recorded and used as indicators of anxiety, with higher counts of fecal boli and higher latencies to eat corresponding to higher levels of anxiety (Archer, 1973; Bodnoff et al., 1989).”
MethodAssessment of positive emotions in animals to improve their welfare
Boissy, A., Manteuffel, G., Jensen, M. B., Moe, R. O., Spruijt, B., Keeling, L. J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.02.003 · Cited by 1,486 · see citing works
The Genesis of Animal Play: Testing the Limits
Burghardt, G. M. (2005) · doi:10.7551/mitpress/3229.001.0001 · Cited by 1,094 · see citing works
Fagen, R. M. (1981) · Cited by 860 · see citing works
Mammalian Play: Training for the Unexpected
Spinka, M., Newberry, R. C., & Bekoff, M. (2001) · The Quarterly Review of Biology · doi:10.1086/393866 · Cited by 817 · cited 1× · see citing works
“Indeed, play has been associated with terms such as ‘fun’ (Bekoff, 2001; Spinka et al., 2001; Vanderschuren, 2010), ‘pleasure’ (Vanderschuren, 2010) and ‘joy’ (Panksepp, 2005), which imply the subjective experience of positive emotions (Boissy et al.”
BackgroundThe neurobiology of positive emotions
Burgdorf, J., & Panksepp, J. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.001 · Cited by 677 · see citing works
Ultrasonic vocalizations as indices of affective states in rats
Knutson, B., Burgdorf, J., & Panksepp, J. (2002) · Psychological Bulletin · doi:10.1037/0033-2909.128.6.961 · Cited by 618 · cited 1× · see citing works
“22 kHz calls are emitted in the face of threat stimuli and during avoidance behavior, while 50 kHz calls have been shown to be associated with high behavioral arousal and positive appetitive behavior (Knutson et al., 2002).”
BackgroundAnimal play and animal welfare
Held, S. D. E., & Špinka, M. (2011) · Animal Behaviour · doi:10.1016/j.anbehav.2011.01.007 · Cited by 583 · see citing works
Panksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537 · cited 1× · see citing works
“Such properties of play have been studied extensively in rats (Douglas, Varlinskaya, & Spear, 2004; Knutson, Burgdorf, & Panksepp, 1998; Panksepp, 1981; Pellis, Field, Smith, & Pellis, 1997; Pellis & McKenna, 1992; Pellis & Pellis, 1987; Vanderschuren, 2010), and rats can serve as a promising model for the study of pl…”
BackgroundBurgdorf, J., Kroes, R. A., Moskal, J. R., Pfaus, J. G., Brudzynski, S. M., & Panksepp, J. (2008) · Journal of Comparative Psychology · doi:10.1037/a0012889 · Cited by 469 · cited 6× · see citing works
“While studies have reported that the same positive vocalizations produced during play (and sex) are also emitted during tickling (Burgdorf et al., 2008), only two studies have investigated whether conspecific social play (Rough-and-Tumble play) is related to vocalizations induced by tickling (Panksepp & Burgdorf, 1999…”
BackgroundMethodResultInfluentialAnticipation of play elicits high-frequency ultrasonic vocalizations in young rats.
Knutson, B. D., Burgdorf, J. S., & Panksepp, J. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.1.65 · Cited by 456 · see citing works
Social deprivation and play in rats
Panksepp, J., & Beatty, W. W. (1980) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(80)91077-8 · Cited by 409 · see citing works
Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004) · Developmental Psychobiology · doi:10.1002/dev.20025 · Cited by 389 · cited 1× · see citing works
“On the one hand, play mates may vary in their intrinsic motivation to play (Pellis & McKenna, 1992), and it has been suggested that if two individuals have similar motivation to play they are both more likely to perform high levels of play, while individuals with divergent motivation to play could result in the less m…”
BackgroundWright, J. M., Gourdon, J. C., & Clarke, P. B. S. (2010) · Psychopharmacology · doi:10.1007/s00213-010-1859-y · Cited by 362 · cited 2× · see citing works
“Negative vocalizations were defined as vocalizations with near-constant frequency ranging from 20 to 25 kHz and lasting from 200 to 2000 ms (Poel & Miczek, 1991; Wright et al., 2010).”
BackgroundPanksepp, J., & Burgdorf, J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00238-2 · Cited by 362 · see citing works
‘Pleasures’,'Pains’ and Animal Welfare: Toward a Natural History of Affect
Fraser, D., & Duncan, I. J. H. (1998) · Animal Welfare · doi:10.1017/s0962728600020935 · Cited by 335 · see citing works
Tickling induces reward in adolescent rats.
Burgdorf, J., & Panksepp, J. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00411-x · Cited by 269 · see citing works
The genesis of animal play: testing the limits
(2005) · Choice Reviews Online · doi:10.5860/choice.43-0314 · Cited by 251 · cited 5× · see citing works
“Similarly to humans, play has been found to occur in a large variety of animal species, mainly within mammals and birds (Held & Spinka, 2011; Spinka, Newberry, & Bekoff, 2001), and while specific play behaviors may differ, the properties of play are maintained and generalizable across species (Burghardt, 2005; Graham…”
BackgroundInfluentialPELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234 · cited 6× · see citing works
“, attacks to the nape) almost exclusively led to pinning behavior, with very few instances of other playful defensive strategies such as partial rotation and evasion (preliminary experimenter’s observations; see also Pellis & Pellis, 1991; Pellis et al., 1997).”
BackgroundInfluentialCurrent Perspectives on the Biological Study of Play: Signs of Progress
Graham, K. L., & Burghardt, G. M. (2010) · The Quarterly Review of Biology · doi:10.1086/656903 · Cited by 229 · see citing works
Rough-and-Tumble Play and the Development of the Social Brain
Pellis, S. M., & Pellis, V. C. (2007) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2007.00483.x · Cited by 225 · see citing works
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“The number of fecal boli and the latency to eat the sweetened cereal were recorded and used as indicators of anxiety, with higher counts of fecal boli and higher latencies to eat corresponding to higher levels of anxiety (Archer, 1973; Bodnoff et al., 1989).”
MethodSocial Behavior and Social Motivation in Adolescent Rats
Varlinskaya, E. I., Spear, L. P., & Spear, N. E. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00285-6 · Cited by 194 · cited 1× · see citing works
“On the one hand, play mates may vary in their intrinsic motivation to play (Pellis & McKenna, 1992), and it has been suggested that if two individuals have similar motivation to play they are both more likely to perform high levels of play, while individuals with divergent motivation to play could result in the less m…”
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Beyond a Joke: From Animal Laughter to Human Joy?
Panksepp, J. (2005) · Science · doi:10.1126/science.1112066 · Cited by 158 · cited 2× · see citing works
“…play has been associated with terms such as ‘fun’ (Bekoff, 2001; Spinka et al., 2001; Vanderschuren, 2010), ‘pleasure’ (Vanderschuren, 2010) and ‘joy’ (Panksepp, 2005), which imply the subjective experience of positive emotions (Boissy et al., 2007; Burgdorf & Panksepp, 2006; Fraser & Duncan,…”
Rough-and-Tumble Play and the Development of the Social Brain
Pellis, S. M., Himmler, B. T., Himmler, S. M., & Pellis, V. C. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804036-2.00012-1 · Cited by 150 · see citing works
Pellis, S. M., & McKenna, M. M. (1992) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80295-5 · Cited by 134 · see citing works
Influence of environmental factors on social play behavior of juvenile rats
Vanderschuren, L. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00385-i · Cited by 128 · see citing works
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Ennaceur, A., Michalikova, S., & Chazot, P. L. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.03.016 · Cited by 117 · see citing works
van der Poel, A. M., & Miczek, K. A. (1991) · Behaviour · doi:10.1163/156853991x00409 · Cited by 112 · see citing works
Developmental analyses of social play behavior in juvenile rats
Thor, D. H., & Holloway, W. R. (1984) · Bulletin of the Psychonomic Society · doi:10.3758/bf03333916 · Cited by 105 · see citing works
Burgdorf, J. S., Panksepp, J., Brudzyński, S. M., Beinfeld, M. C., Cromwell, H. C., Kroes, R. A., & Moskal, J. R. (2008) · Developmental Psychobiology · doi:10.1002/dev.20343 · Cited by 101 · see citing works
Mällo, T., Matrov, D., Herm, L., Kõiv, K., Eller, M., Rinken, A., & Harro, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.06.015 · Cited by 100 · see citing works
Consumer demand theory and the assessment of animal welfare
Lawrence, A. B. (1987) · Animal Behaviour · doi:10.1016/s0003-3472(87)80236-1 · Cited by 99 · cited 1× · see citing works
“Although the properties of play may render its study rather challenging, its use as a potential indicator of good animal welfare is becoming increasingly relevant (Boissy et al., 2007; Fagen, 1981; Held & Spinka, 2011; Lawrence, 1987; Oliveira, Rossi, Silva, Lau, & Barreto, 2010).”
BackgroundSocial play alters regional brain opioid receptor binding in juvenile rats
Vanderschuren, L. J. M. J., Stein, E. A., Wiegant, V. M., & Van Ree, J. M. (1995) · Brain Research · doi:10.1016/0006-8993(95)00256-p · Cited by 88 · see citing works
Himmler, B. T., Kisko, T. M., Euston, D. R., Kolb, B., & Pellis, S. M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.04.014 · Cited by 87 · see citing works
Play behaviour in nonhuman animals and the animal welfare issue
Oliveira, A. F. S., Rossi, A. O., Silva, L. F. R., Lau, M. C., & Barreto, R. E. (2009) · Journal of Ethology · doi:10.1007/s10164-009-0167-7 · Cited by 86 · see citing works
Laughing Rats? Playful Tickling Arouses High-Frequency Ultrasonic Chirping in Young Rodents
Panksepp, J., & Burgdorf, J. S. (2010) · American journal of play · Cited by 84 · see citing works
Housing and welfare in laboratory rats: time-budgeting and pathophysiology in single-sex groups
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Pellis, S. M., & Pellis, V. C. (1983) · Developmental Psychobiology · doi:10.1002/dev.420160403 · Cited by 71 · see citing works
(2010) · American journal of play · Cited by 65 · see citing works
The effects of stress on play and home cage behaviors in adolescent male rats
Klein, Z. A., Padow, V. A., & Romeo, R. D. (2009) · Developmental Psychobiology · doi:10.1002/dev.20413 · Cited by 51 · see citing works
Webber, E. S., Harmon, K. M., Beckwith, T. J., Peña, S., Burgdorf, J., Panksepp, J., & Cromwell, H. C. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.012 · Cited by 39 · cited 1× · see citing works
“, 2008), only two studies have investigated whether conspecific social play (Rough-and-Tumble play) is related to vocalizations induced by tickling (Panksepp & Burgdorf, 1999; Webber et al., 2012).”
BackgroundBekoff, M. (2001) · Zygon: Journal of Religion and Science · doi:10.1111/0591-2385.00388 · Cited by 36 · cited 1× · see citing works
“Indeed, play has been associated with terms such as ‘fun’ (Bekoff, 2001; Spinka et al., 2001; Vanderschuren, 2010), ‘pleasure’ (Vanderschuren, 2010) and ‘joy’ (Panksepp, 2005), which imply the subjective experience of positive emotions (Boissy et al.”
BackgroundBekoff, M., & Fagen, R. (1981) · Evolution · doi:10.2307/2408140 · Cited by 2
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8 of the 57 references couldn’t be matched to a known paper.
Research works printed but not linked: 1
- Garvey, C. (1990). Play. Cambridge, MA: Harvard University Press.
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Sorted by citations
Facial Indicators of Positive Emotions in Rats
Finlayson, K., Lampe, J. F., Hintze, S., Würbel, H., & Melotti, L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166446 · Cited by 97 · see citing works
Self-citationPlay fighting and the development of the social brain: The rat’s tale
Pellis, S. M., Pellis, V. C., Ham, J. R., & Stark, R. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105037 · Cited by 76 · see citing works
Is play a behavior system, and, if so, what kind?
Pellis, S. M., Pellis, V. C., Pelletier, A. N., & Leca, J. (2019) · Behavioural Processes · doi:10.1016/j.beproc.2018.12.011 · Cited by 77 · see citing works
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
“, 2019), with individuals initiating more play in a dyadic test also initiating more play in the home cage (Lampe et al., 2017; Melotti et al., 2014).”
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.0524-22.2022 · Cited by 54 · see citing works
Context-dependent individual differences in playfulness in male rats
Lampe, J. F., Burman, O., Würbel, H., & Melotti, L. (2017) · Developmental Psychobiology · doi:10.1002/dev.21509 · Cited by 30 · see citing works
Self-citationAnimal play and evolution: Seven timely research issues about enigmatic phenomena
Burghardt, G. M., Pellis, S. M., Schank, J. C., Smaldino, P. E., Vanderschuren, L. J. M. J., & Palagi, E. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105617 · Cited by 32 · see citing works
Who’s laughing? Play, tickling and ultrasonic vocalizations in rats.
Burke, C. J., Pellis, S. M., & Achterberg, E. J. M. (2022) · Philosophical Transactions of the Royal Society B · doi:10.1098/rstb.2021.0184 · Cited by 23 · see citing works
“First, there are individual differences among rats in both their motivation to engage in conspecific and heterospecific play, with rats that engage in more conspecific play not being the same as those that prefer to engage in heterospecific play [38].”
BackgroundResultWheat, C. H., & Temrin, H. (2020) · iScience · doi:10.1016/j.isci.2019.100811 · Cited by 21 · see citing works
Achterberg, E. J. M., Burke, C. J., & Pellis, S. M. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104933 · Cited by 20 · see citing works
“, 2021; present study), and whether observed in the home cage or in staged dyadic encounters (Melotti et al., 2014).”
Play like me: Similarity in playfulness promotes social play
Lampe, J. F., Ruchti, S., Burman, O., Würbel, H., & Melotti, L. (2019) · PLOS ONE · doi:10.1371/journal.pone.0224282 · Cited by 20 · see citing works
“Individual playfulness was measured via a Play-in-Pairs test [46, 45], after which rats were resorted into cages of similar (high, HHH; intermediate, III; low, LLL) or dissimilar (HII, LII) playfulness.”
BackgroundMethodInfluentialSelf-citationNon-random associations in group housed rats (Rattus norvegicus)
Proops, L., Troisi, C. A., Kleinhappel, T. K., & Romero, T. (2021) · Scientific Reports · doi:10.1038/s41598-021-94608-4 · Cited by 20 · 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
Relationships between play and responses to tickling in male juvenile rats.
Hammond, T., Bombail, V., Nielsen, B. L., Meddle, S. L., Lawrence, A. B., & Brown, S. M. (2019) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2019.104879 · Cited by 18 · see citing works
Sex differences in 50 kHz call subtypes emitted during tickling-induced playful behaviour in rats.
Tivey, E. K. L., Martin, J. E., Brown, S. M., Bombail, V., Lawrence, A. B., & Meddle, S. L. (2022) · Scientific Reports · doi:10.1038/s41598-022-19362-7 · Cited by 13 · see citing works
Individual play patterns stimulated by a familiar object are group-driven
Zupan, M., Rehn, T., de Oliveira, D., Malovrh, Š. P., & Keeling, L. J. (2019) · Scientific Reports · doi:10.1038/s41598-019-42382-9 · Cited by 10 · see citing works
Ham, J. R., & Pellis, S. M. (2025) · iScience · doi:10.1016/j.isci.2025.112562 · Cited by 5 · see citing works
“More-over, given that individual differences in playfulness tend to be stable over time and context, 27,30,31 and that the quality of play, especially turn taking and symmetry, seems to be important in rewarding playful interactions, 58,59 we predicted that rats should prefer high players as…”
Bombail, V., Brown, S. M., Beyts, C., Martin, J. E., Li, T., Meddle, S. L., Mendl, M., Robinson, E. S., Hammond, T. J., Nielsen, B. L., et al. (2025) · F1000Research · doi:10.12688/f1000research.166417.2 · Cited by 4 · see citing works
“For example, the patterns and correlations between USVs and specific behaviours are known to vary across contexts (Burke et al., 2022; Melotti et al., 2014).”
Post-natal maternal stress decreases locomotor play behaviors in Octodon degus pups
Malcangi, S., Lam, C., Sam, A., León, C., Ramírez‐Estrada, J., & Bauer, C. M. (2020) · Journal of Ethology · doi:10.1007/s10164-020-00642-6 · Cited by 4 · see citing works
Bijlsma, A., Omrani, A., Spoelder, M., Verharen, J. P. H., Bauer, L., Cornelis, C., de Zwart, B., van Dorland, R., Vanderschuren, L. J. M. J., & Wierenga, C. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.01.070540 · Cited by 4 · see citing works
“Play is not displayed continuously by young rats, but appears in peaks of relatively short duration across the day (Melotti et al., 2014; Lampe et al., 2019).”
BackgroundDisentangling developmental effects of play aspects in rat rough-and-tumble play
Liu, Q., Радченко, М., & Špinka, M. (2024) · Biology Letters · doi:10.1098/rsbl.2024.0037 · Cited by 1 · see citing works
Liu, Q., Ilčíková, T., Радченко, М., Junková, M., & Špinka, M. (2023) · Frontiers in Zoology · doi:10.1186/s12983-023-00512-0 · Cited by 2 · see citing works
“Previous study also suggested USVs production during tickling was not correlated with the number of pinning in RT play [70].”
BackgroundThe role of the dopamine D1 receptor in anticipatory pleasure and social play
Witt, K. M., Harper, D. N., & Ellenbroek, B. A. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110225 · Cited by 1 · see citing works
“Social play is typically defined as active, voluntary interaction with at least one other peer and is highly rewarding in nature (Achterberg & Vanderschuren, 2023; Melotti et al., 2014; Pellis et al., 2022b).”
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
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
Held, S. D. E. (2026) · Wiley eBooks · doi:10.1002/9781394182237.ch8
- Authors
- Melotti, L., Bailoo, J., Murphy, E., Burman, O., & Wurbel, H.
- Affiliations
- University of Bern (CH)
- Utrecht University (NL)
- University of Lincoln (GB)
- Corresponding author
- Melotti, Luca
- Venue
- Animal Behavior and Cognition
- Publisher
- Animal Behavior and Cognition
- Published
- 2014-11-01
- Volume
- 1
- Issue
- 4
- Pages
- 489-501
- ISSN
- 2372-4323 (ISSN-L)
- 2372-5052
- OpenAlex
- W2290467764
- Semantic Scholar
- 79737504ede1f66b145103da67835ea6a45e7d18
- Cited by
- 26
- References
- 57
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 4 · 2017: 1 · 2016: 1
- FWCI
- 0.90
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- cc-by
- Locations
- Animal Behavior and Cognition (publishedVersion, cc-by)
- Lincoln Repository (University of Lincoln) (acceptedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Topics
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- 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
- animal play, rats, social play, solitary play, play structure, Lister hooded rats, tickling, vocalizations
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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.
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