Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats

Abstract Background Play is a common and developmentally important behaviour in young mammals. Specifically in Norway rats (Rattus norvegicus), reduced opportunity to engage in rough-and-tumble (RT) play has been associated with impaired development in social competence. However, RT play is a comple...

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Main Authors: Quanxiao Liu, Tereza Ilčíková, Mariia Radchenko, Markéta Junková, Marek Špinka
Format: Article
Language:English
Published: BMC 2023-10-01
Series:Frontiers in Zoology
Subjects:
Online Access:https://doi.org/10.1186/s12983-023-00512-0
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author Quanxiao Liu
Tereza Ilčíková
Mariia Radchenko
Markéta Junková
Marek Špinka
author_facet Quanxiao Liu
Tereza Ilčíková
Mariia Radchenko
Markéta Junková
Marek Špinka
author_sort Quanxiao Liu
collection DOAJ
description Abstract Background Play is a common and developmentally important behaviour in young mammals. Specifically in Norway rats (Rattus norvegicus), reduced opportunity to engage in rough-and-tumble (RT) play has been associated with impaired development in social competence. However, RT play is a complex behaviour having both a kinematic aspect (i.e., performing complex 3D manoeuvres during play fights) and a social aspect (interacting with a playful partner). There has been little research so far on disentangling the two aspects in RT play, especially on how these two aspects affect the affective appraisal of the intense physical contact during play. Results To examine the developmental effects of kinematic and social play reduction on affective appraisal in rats, we subjected male Long-Evans rats from 21 days old to RT play experience that was reduced either kinematically (through playing in a low ceiling environment) or socially (through playing with a less playful Fischer-344 rat). Starting at 35 days, we measured their production of positively (50-kHz) and negatively (22-kHz) valenced ultrasonic vocalisations (USVs) in a 2-min standardised human-rat play procedure that mimicked the playful sequences of nape contact, pinning, and belly stimulation (‘tickling’) for ten days. We hypothesised that the rats with kinematically or socially reduced play would perceive the ‘tickling’ less positively and thus emit positive ultrasonic vocalisations at lower rates compared to control rats with non-reduced play experience. Our results confirmed that each of the treatments reduced play differently: while the kinematic reduction abolished playful pinnings entirely, the social reduction decreased the pinnings and made play highly asymmetric. During the tickling procedure, rats mostly produced 50 kHz USV, indicating that they appraised the procedure as positive. There was a wide inter individual variance and high individual consistency in rats’ USV responses to ‘tickling’. Crucially, neither the kinematically nor the socially reduced play experience affected either type of USV production when rats were ‘tickled’. Conclusions This finding indicates that the ability to appraise play-like interactions as positive remains unaffected even when the kinematic or the social aspect of play experience was substantially curtailed.
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spelling doaj.art-430d246865804dc585271dcedc9b052b2023-11-20T10:24:51ZengBMCFrontiers in Zoology1742-99942023-10-0120111310.1186/s12983-023-00512-0Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in ratsQuanxiao Liu0Tereza Ilčíková1Mariia Radchenko2Markéta Junková3Marek Špinka4Department of Ethology and Companion Animal Science, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life SciencesDepartment of Ethology and Companion Animal Science, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life SciencesDepartment of Ethology and Companion Animal Science, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life SciencesDepartment of Ethology and Companion Animal Science, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life SciencesDepartment of Ethology and Companion Animal Science, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life SciencesAbstract Background Play is a common and developmentally important behaviour in young mammals. Specifically in Norway rats (Rattus norvegicus), reduced opportunity to engage in rough-and-tumble (RT) play has been associated with impaired development in social competence. However, RT play is a complex behaviour having both a kinematic aspect (i.e., performing complex 3D manoeuvres during play fights) and a social aspect (interacting with a playful partner). There has been little research so far on disentangling the two aspects in RT play, especially on how these two aspects affect the affective appraisal of the intense physical contact during play. Results To examine the developmental effects of kinematic and social play reduction on affective appraisal in rats, we subjected male Long-Evans rats from 21 days old to RT play experience that was reduced either kinematically (through playing in a low ceiling environment) or socially (through playing with a less playful Fischer-344 rat). Starting at 35 days, we measured their production of positively (50-kHz) and negatively (22-kHz) valenced ultrasonic vocalisations (USVs) in a 2-min standardised human-rat play procedure that mimicked the playful sequences of nape contact, pinning, and belly stimulation (‘tickling’) for ten days. We hypothesised that the rats with kinematically or socially reduced play would perceive the ‘tickling’ less positively and thus emit positive ultrasonic vocalisations at lower rates compared to control rats with non-reduced play experience. Our results confirmed that each of the treatments reduced play differently: while the kinematic reduction abolished playful pinnings entirely, the social reduction decreased the pinnings and made play highly asymmetric. During the tickling procedure, rats mostly produced 50 kHz USV, indicating that they appraised the procedure as positive. There was a wide inter individual variance and high individual consistency in rats’ USV responses to ‘tickling’. Crucially, neither the kinematically nor the socially reduced play experience affected either type of USV production when rats were ‘tickled’. Conclusions This finding indicates that the ability to appraise play-like interactions as positive remains unaffected even when the kinematic or the social aspect of play experience was substantially curtailed.https://doi.org/10.1186/s12983-023-00512-0Affective appraisalAnimal developmentAnimal playKinematic playSocial playHuman-rat play
spellingShingle Quanxiao Liu
Tereza Ilčíková
Mariia Radchenko
Markéta Junková
Marek Špinka
Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats
Frontiers in Zoology
Affective appraisal
Animal development
Animal play
Kinematic play
Social play
Human-rat play
title Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats
title_full Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats
title_fullStr Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats
title_full_unstemmed Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats
title_short Effects of reduced kinematic and social play experience on affective appraisal of human-rat play in rats
title_sort effects of reduced kinematic and social play experience on affective appraisal of human rat play in rats
topic Affective appraisal
Animal development
Animal play
Kinematic play
Social play
Human-rat play
url https://doi.org/10.1186/s12983-023-00512-0
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