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Open Access 01-12-2024 | Research

Uncovering hidden prosocial behaviors underlying aggression motivation in mice and young children

Authors: Chih-Lin Lee, Yu-Shan Su, Chi-Yu Chang, Tzu-Yun Kung, Yu-Kai Ma, Pei-Yun Zeng, Ching-Chuan Cheng, Yu-Jen Chang, Yu-Ju Chou, Tsung-Han Kuo

Published in: Behavioral and Brain Functions | Issue 1/2024

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Abstract

Background

Animals exhibit a wide range of social behaviors, including positive actions that promote social cohesion and negative behaviors associated with asserting dominance. While these behaviors are often viewed as opposites, they can also exist independently or coexist in complex ways, necessitating further investigation into their interrelationships.

Results

To study the interplay between these two types of behaviors, we examined mouse social behaviors using resident-intruder assays and revealed a negative correlation between social aggression and prosocial allogrooming. Suppressing aggressive motivation through various manipulations, including social subordination, olfaction ablation, and inhibition of aggressive neural circuits, led to an increased display of allogrooming behavior. The mouse findings prompted us to further explore the relationship between aggression and prosocial behaviors in preschool children. Similarly, we observed a negative association between aggression and prosocial behaviors, which were potentially influenced by their inhibitory control abilities.

Conclusions

Through this cross-species study, we uncovered the inhibitory impact of aggressive neural circuits on mouse allogrooming and established a link between aggression and prosocial behaviors in children. These insights offer valuable implications for understanding and potentially influencing social interactions in both animal and human contexts, with potential applications in preschool education practices.
Appendix
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Literature
1.
go back to reference Eron LD, Huesmann LR. The relation of prosocial behavior to the development of aggression and psychopathology. Aggressive Behav. 1984;10:201–11.CrossRef Eron LD, Huesmann LR. The relation of prosocial behavior to the development of aggression and psychopathology. Aggressive Behav. 1984;10:201–11.CrossRef
2.
go back to reference Dugatkin LA. Principles of animal behavior. Third ed. W. W. Norton & Company, Inc.; 2014. Dugatkin LA. Principles of animal behavior. Third ed. W. W. Norton & Company, Inc.; 2014.
3.
go back to reference Eivers AR, Brendgen M, Vitaro F, Borge AI. Concurrent and longitudinal links between children’s and their friends’ antisocial and prosocial behavior in preschool. Early Child Res Q. 2012;27:137–46.CrossRef Eivers AR, Brendgen M, Vitaro F, Borge AI. Concurrent and longitudinal links between children’s and their friends’ antisocial and prosocial behavior in preschool. Early Child Res Q. 2012;27:137–46.CrossRef
4.
go back to reference Pulkkinen L, Tremblay RE. Patterns of boys’ social adjustment in two cultures and at different ages: a longitudinal perspective. Int J Behav Dev. 1992;15:527–53.CrossRef Pulkkinen L, Tremblay RE. Patterns of boys’ social adjustment in two cultures and at different ages: a longitudinal perspective. Int J Behav Dev. 1992;15:527–53.CrossRef
5.
go back to reference Feshbach S, Feshbach ND. Aggression and altruism: a personality perspective. Altruism and aggression: Biological and social origins, 189–217 (1986). Feshbach S, Feshbach ND. Aggression and altruism: a personality perspective. Altruism and aggression: Biological and social origins, 189–217 (1986).
6.
go back to reference Persson G. Developmental perspectives on prosocial and aggressive motives in preschoolers’ peer interactions. Int J Behav Dev. 2005;29:80–91.CrossRef Persson G. Developmental perspectives on prosocial and aggressive motives in preschoolers’ peer interactions. Int J Behav Dev. 2005;29:80–91.CrossRef
7.
go back to reference Nantel-Vivier A, Pihl RO, Côté S, Tremblay RE. Developmental association of prosocial behaviour with aggression, anxiety and depression from infancy to preadolescence. J Child Psychol Psyc. 2014;55:1135–44.CrossRef Nantel-Vivier A, Pihl RO, Côté S, Tremblay RE. Developmental association of prosocial behaviour with aggression, anxiety and depression from infancy to preadolescence. J Child Psychol Psyc. 2014;55:1135–44.CrossRef
8.
go back to reference Hay DF, et al. Prosocial and aggressive behavior: a longitudinal study. Monogr Soc Res Child. 2021;86:7–103.CrossRef Hay DF, et al. Prosocial and aggressive behavior: a longitudinal study. Monogr Soc Res Child. 2021;86:7–103.CrossRef
9.
go back to reference Chen X, Huang X, Chang L, Wang L, Li D. Aggression, social competence, and academic achievement in Chinese children: a 5-year longitudinal study. Dev Psychopathol. 2010;22:583–92.PubMedCrossRef Chen X, Huang X, Chang L, Wang L, Li D. Aggression, social competence, and academic achievement in Chinese children: a 5-year longitudinal study. Dev Psychopathol. 2010;22:583–92.PubMedCrossRef
10.
go back to reference Obsuth I, Eisner MP, Malti T, Ribeaud D. The developmental relation between aggressive behaviour and prosocial behaviour: a 5-year longitudinal study. BMC Psychol. 2015;3:1–15.CrossRef Obsuth I, Eisner MP, Malti T, Ribeaud D. The developmental relation between aggressive behaviour and prosocial behaviour: a 5-year longitudinal study. BMC Psychol. 2015;3:1–15.CrossRef
11.
go back to reference Logis HA, Rodkin PC, Gest SD, Ahn HJ. Popularity as an organizing factor of preadolescent friendship networks: beyond prosocial and aggressive behavior. J Res Adolescence. 2013;23:413–23.CrossRef Logis HA, Rodkin PC, Gest SD, Ahn HJ. Popularity as an organizing factor of preadolescent friendship networks: beyond prosocial and aggressive behavior. J Res Adolescence. 2013;23:413–23.CrossRef
12.
go back to reference Koolhaas JM et al. The resident-intruder paradigm: a standardized test for aggression, violence and social stress. J Vis Exp, 2013;33:e4367. Koolhaas JM et al. The resident-intruder paradigm: a standardized test for aggression, violence and social stress. J Vis Exp, 2013;33:e4367.
14.
go back to reference Blanchard DC, Summers CH, Blanchard RJ. The role of behavior in translational models for psychopathology: functionality and dysfunctional behaviors. Neurosci Biobehav Rev. 2013;37:1567–77.PubMedPubMedCentralCrossRef Blanchard DC, Summers CH, Blanchard RJ. The role of behavior in translational models for psychopathology: functionality and dysfunctional behaviors. Neurosci Biobehav Rev. 2013;37:1567–77.PubMedPubMedCentralCrossRef
16.
go back to reference Wang F, et al. Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science. 2011;334:693–7.PubMedCrossRef Wang F, et al. Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science. 2011;334:693–7.PubMedCrossRef
17.
go back to reference Spruijt BM, van Hooff JA, Gispen WH. Ethology and neurobiology of grooming behavior. Physiol Rev. 1992;72:825–52.PubMedCrossRef Spruijt BM, van Hooff JA, Gispen WH. Ethology and neurobiology of grooming behavior. Physiol Rev. 1992;72:825–52.PubMedCrossRef
18.
go back to reference Schino G, Aureli F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol Lett. 2010;13:45–50.PubMedCrossRef Schino G, Aureli F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol Lett. 2010;13:45–50.PubMedCrossRef
19.
go back to reference Ventura R, Majolo B, Koyama NF, Hardie S, Schino G. Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. Am J Primatol. 2006;68:1138–49.PubMedCrossRef Ventura R, Majolo B, Koyama NF, Hardie S, Schino G. Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. Am J Primatol. 2006;68:1138–49.PubMedCrossRef
21.
22.
go back to reference Schweinfurth MK, Taborsky M. Reciprocal trading of different commodities in Norway rats. Curr Biol. 2018;28:594–9.PubMedCrossRef Schweinfurth MK, Taborsky M. Reciprocal trading of different commodities in Norway rats. Curr Biol. 2018;28:594–9.PubMedCrossRef
23.
go back to reference Stopka P, Graciasová R. Conditional allogrooming in the herb-field mouse. Behav Ecol. 2001;12:584–9.CrossRef Stopka P, Graciasová R. Conditional allogrooming in the herb-field mouse. Behav Ecol. 2001;12:584–9.CrossRef
24.
go back to reference Wallace KJ, Dupeyron S, Li MT, Kelly AM. Early life social complexity shapes adult neural processing in the communal spiny mouse. Psychopharmacology (2023). Wallace KJ, Dupeyron S, Li MT, Kelly AM. Early life social complexity shapes adult neural processing in the communal spiny mouse. Psychopharmacology (2023).
25.
go back to reference Abreu JAG et al. Species-typical group size differentially influences social reward neural circuitry during nonreproductive social interactions. Iscience 25 (2022). Abreu JAG et al. Species-typical group size differentially influences social reward neural circuitry during nonreproductive social interactions. Iscience 25 (2022).
27.
go back to reference Matsumoto M, et al. Indispensable role of the oxytocin receptor for allogrooming toward socially distressed cage mates in female mice. J Neuroendocrinol. 2021;33:e12980.PubMedPubMedCentralCrossRef Matsumoto M, et al. Indispensable role of the oxytocin receptor for allogrooming toward socially distressed cage mates in female mice. J Neuroendocrinol. 2021;33:e12980.PubMedPubMedCentralCrossRef
28.
go back to reference Fraser D, Waddell MS. The importance of social and self-grooming for the control of ectoparasitic mites on normal and dystrophic laboratory mice. Lab Pract. 1974;23:58–9.PubMed Fraser D, Waddell MS. The importance of social and self-grooming for the control of ectoparasitic mites on normal and dystrophic laboratory mice. Lab Pract. 1974;23:58–9.PubMed
29.
go back to reference Piras E, et al. Cell-specific expression of CYP2A5 in the mouse respiratory tract: effects of olfactory toxicants. J Histochem Cytochem. 2003;51:1545–55.PubMedPubMedCentralCrossRef Piras E, et al. Cell-specific expression of CYP2A5 in the mouse respiratory tract: effects of olfactory toxicants. J Histochem Cytochem. 2003;51:1545–55.PubMedPubMedCentralCrossRef
30.
go back to reference John JAS, Key B. Axon Mis-targeting in the olfactory bulb during regeneration of olfactory neuroepithelium. Chem Senses. 2003;28:773–9.PubMedCrossRef John JAS, Key B. Axon Mis-targeting in the olfactory bulb during regeneration of olfactory neuroepithelium. Chem Senses. 2003;28:773–9.PubMedCrossRef
31.
go back to reference Ma YK, et al. Lack of social touch alters anxiety-like and social behaviors in male mice. Stress. 2022;25:134–44.PubMedCrossRef Ma YK, et al. Lack of social touch alters anxiety-like and social behaviors in male mice. Stress. 2022;25:134–44.PubMedCrossRef
32.
33.
go back to reference Friard O, Gamba M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol. 2016;7:1325–30.CrossRef Friard O, Gamba M. BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol. 2016;7:1325–30.CrossRef
34.
go back to reference MacLellan A, Nazal B, Young L, Mason G. Waking inactivity as a welfare indicator in laboratory mice: investigating postures, facial expressions and depression-like states. Royal Soc Open Sci. 2022;9:221083.CrossRef MacLellan A, Nazal B, Young L, Mason G. Waking inactivity as a welfare indicator in laboratory mice: investigating postures, facial expressions and depression-like states. Royal Soc Open Sci. 2022;9:221083.CrossRef
35.
go back to reference Keenan RJ, Chan J, Donnelly PS, Barnham KJ, Jacobson LH. The social defeat/overcrowding murine psychosocial stress model results in a pharmacologically reversible body weight gain but not depression - related behaviours. Neurobiol Stress. 2018;9:176–87.PubMedPubMedCentralCrossRef Keenan RJ, Chan J, Donnelly PS, Barnham KJ, Jacobson LH. The social defeat/overcrowding murine psychosocial stress model results in a pharmacologically reversible body weight gain but not depression - related behaviours. Neurobiol Stress. 2018;9:176–87.PubMedPubMedCentralCrossRef
37.
go back to reference Ammassari-Teule M, Passino E, Restivo L, De Marsanich B. Fear conditioning in C57/BL/6 and DBA/2 mice: variability in nucleus accumbens function according to the strain predisposition to show contextual- or cue-based responding. Eur J Neurosci. 2000;12:4467–74.PubMed Ammassari-Teule M, Passino E, Restivo L, De Marsanich B. Fear conditioning in C57/BL/6 and DBA/2 mice: variability in nucleus accumbens function according to the strain predisposition to show contextual- or cue-based responding. Eur J Neurosci. 2000;12:4467–74.PubMed
38.
go back to reference Paxinos G, Franklin KB. Paxinos and Franklin’s the mouse brain in stereotaxic coordinates. Academic; 2019. Paxinos G, Franklin KB. Paxinos and Franklin’s the mouse brain in stereotaxic coordinates. Academic; 2019.
40.
go back to reference Lin YS, C. JL. The relations among young children’s behavioral regulation, social skills, and aggression. Early Child Educ. 2010;298:42–60. Lin YS, C. JL. The relations among young children’s behavioral regulation, social skills, and aggression. Early Child Educ. 2010;298:42–60.
41.
go back to reference Crick NR, Casas JF, Mosher M. Preschool Social Behavior Scale–Teacher Form. Developmental Psychology (1997). Crick NR, Casas JF, Mosher M. Preschool Social Behavior Scale–Teacher Form. Developmental Psychology (1997).
42.
go back to reference Chao SPJ. J. The effects of prosocial learning strategies program to promote preschooler’s prosocial behavior. J Study Child Educ. 2010;6:1–39. Chao SPJ. J. The effects of prosocial learning strategies program to promote preschooler’s prosocial behavior. J Study Child Educ. 2010;6:1–39.
43.
go back to reference Tsai C-L, Thorell LB, Siu AF, Hsu Y-H, Lin H-L. Taiwanese Traditional-Chinese Childhood Executive Functioning Inventory: Revision, Investigation of Psychometric properties, and establishing of norms. Psychol Test. 2020;67:119–43. Tsai C-L, Thorell LB, Siu AF, Hsu Y-H, Lin H-L. Taiwanese Traditional-Chinese Childhood Executive Functioning Inventory: Revision, Investigation of Psychometric properties, and establishing of norms. Psychol Test. 2020;67:119–43.
44.
go back to reference Kalueff AV, Minasyan A, Keisala T, Shah ZH, Tuohimaa P. Hair barbering in mice: implications for neurobehavioural research. Behav Processes. 2006;71:8–15.PubMedCrossRef Kalueff AV, Minasyan A, Keisala T, Shah ZH, Tuohimaa P. Hair barbering in mice: implications for neurobehavioural research. Behav Processes. 2006;71:8–15.PubMedCrossRef
45.
go back to reference Kudryavtseva NN, Bondar NP, Alekseyenko OV. Behavioral correlates of learned aggression in male mice. Aggressive Behav. 2000;26:386–400.CrossRef Kudryavtseva NN, Bondar NP, Alekseyenko OV. Behavioral correlates of learned aggression in male mice. Aggressive Behav. 2000;26:386–400.CrossRef
46.
go back to reference Kudryavtseva NN, Lipina TV, Koryakina LA. Effects of haloperidol on communicative and aggressive behavior in male mice with different experiences of aggression. Pharmacol Biochem Behav. 1999;63:229–36.PubMedCrossRef Kudryavtseva NN, Lipina TV, Koryakina LA. Effects of haloperidol on communicative and aggressive behavior in male mice with different experiences of aggression. Pharmacol Biochem Behav. 1999;63:229–36.PubMedCrossRef
47.
go back to reference Corridi P, Chiarotti F, Bigi S, Alleva E. Familiarity with conspecific odor and isolation-induced aggressive behavior in male mice (Mus domesticus). J Comp Psychol. 1993;107:328–35.PubMedCrossRef Corridi P, Chiarotti F, Bigi S, Alleva E. Familiarity with conspecific odor and isolation-induced aggressive behavior in male mice (Mus domesticus). J Comp Psychol. 1993;107:328–35.PubMedCrossRef
48.
go back to reference Wang Z, et al. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J Neurosci. 2006;26:7375–9.PubMedPubMedCentralCrossRef Wang Z, et al. Pheromone detection in male mice depends on signaling through the type 3 adenylyl cyclase in the main olfactory epithelium. J Neurosci. 2006;26:7375–9.PubMedPubMedCentralCrossRef
49.
go back to reference Stowers L, Holy TE, Meister M, Dulac C, Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science. 2002;295:1493–500.PubMedCrossRef Stowers L, Holy TE, Meister M, Dulac C, Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science. 2002;295:1493–500.PubMedCrossRef
50.
go back to reference Hong W, Kim DW, Anderson DJ. Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell. 2014;158:1348–61.PubMedPubMedCentralCrossRef Hong W, Kim DW, Anderson DJ. Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell. 2014;158:1348–61.PubMedPubMedCentralCrossRef
52.
go back to reference Gower AL, Lingras KA, Mathieson LC, Kawabata Y, Crick NR. The role of Preschool Relational and Physical Aggression in the transition to Kindergarten: Links with Social-Psychological Adjustment. Early Educ Dev. 2014;25:619–40.PubMedPubMedCentralCrossRef Gower AL, Lingras KA, Mathieson LC, Kawabata Y, Crick NR. The role of Preschool Relational and Physical Aggression in the transition to Kindergarten: Links with Social-Psychological Adjustment. Early Educ Dev. 2014;25:619–40.PubMedPubMedCentralCrossRef
53.
go back to reference Woolley ML, Haman M, Higgins GA, Ballard TM. Investigating the effect of bilateral amygdala lesions on fear conditioning and social interaction in the male Mongolian gerbil. Brain Res. 2006;1078:151–8.PubMedCrossRef Woolley ML, Haman M, Higgins GA, Ballard TM. Investigating the effect of bilateral amygdala lesions on fear conditioning and social interaction in the male Mongolian gerbil. Brain Res. 2006;1078:151–8.PubMedCrossRef
54.
go back to reference Monette S, Bigras M, Lafrenière MA. Structure of executive functions in typically developing kindergarteners. J Exp Child Psychol. 2015;140:120–39.PubMedCrossRef Monette S, Bigras M, Lafrenière MA. Structure of executive functions in typically developing kindergarteners. J Exp Child Psychol. 2015;140:120–39.PubMedCrossRef
55.
go back to reference Romero-López M, Pichardo MC, Justicia-Arráez A, Bembibre-Serrano J. Reducing aggression by developing emotional and inhibitory control. Int J Environ Res Public Health. 2021;18:5263.PubMedPubMedCentralCrossRef Romero-López M, Pichardo MC, Justicia-Arráez A, Bembibre-Serrano J. Reducing aggression by developing emotional and inhibitory control. Int J Environ Res Public Health. 2021;18:5263.PubMedPubMedCentralCrossRef
56.
go back to reference Roseth CJ, et al. Preschoolers’ Bistrategic Resource Control, Reconciliation, and peer regard. Soc Dev. 2010;20:185–211.CrossRef Roseth CJ, et al. Preschoolers’ Bistrategic Resource Control, Reconciliation, and peer regard. Soc Dev. 2010;20:185–211.CrossRef
57.
go back to reference Roth-Hanania R, Davidov M, Zahn-Waxler C. Empathy development from 8 to 16 months: early signs of concern for others. Infant Behav Dev. 2011;34:447–58.PubMedCrossRef Roth-Hanania R, Davidov M, Zahn-Waxler C. Empathy development from 8 to 16 months: early signs of concern for others. Infant Behav Dev. 2011;34:447–58.PubMedCrossRef
58.
go back to reference Dunn J, Munn P. Siblings and the development of Prosocial Behaviour. Int J Behav Dev. 1986;9:265–84.CrossRef Dunn J, Munn P. Siblings and the development of Prosocial Behaviour. Int J Behav Dev. 1986;9:265–84.CrossRef
59.
go back to reference Ornaghi V, Grazzani I, Cherubin E, Conte E, Piralli F. Let’s talk about emotions!’. The Effect of Conversational Training on preschoolers’ emotion comprehension and Prosocial Orientation. Soc Dev. 2015;24:166–83.CrossRef Ornaghi V, Grazzani I, Cherubin E, Conte E, Piralli F. Let’s talk about emotions!’. The Effect of Conversational Training on preschoolers’ emotion comprehension and Prosocial Orientation. Soc Dev. 2015;24:166–83.CrossRef
60.
go back to reference Flook L, Goldberg SB, Pinger L, Davidson RJ. Promoting prosocial behavior and self-regulatory skills in preschool children through a mindfulness-based kindness curriculum. Dev Psychol. 2015;51:44–51.PubMedCrossRef Flook L, Goldberg SB, Pinger L, Davidson RJ. Promoting prosocial behavior and self-regulatory skills in preschool children through a mindfulness-based kindness curriculum. Dev Psychol. 2015;51:44–51.PubMedCrossRef
61.
go back to reference Chou YJ et al. Potential cross-species correlations in social hierarchy and memory between mice and young children. Commun Biol 5 (2022). Chou YJ et al. Potential cross-species correlations in social hierarchy and memory between mice and young children. Commun Biol 5 (2022).
62.
go back to reference Tsai H-L, Chou Y-J. Young Children’s Social Dominance, influencing factors, and resources Control Strategies. Bull Educational Psychol. 2019;50:685–705. Tsai H-L, Chou Y-J. Young Children’s Social Dominance, influencing factors, and resources Control Strategies. Bull Educational Psychol. 2019;50:685–705.
Metadata
Title
Uncovering hidden prosocial behaviors underlying aggression motivation in mice and young children
Authors
Chih-Lin Lee
Yu-Shan Su
Chi-Yu Chang
Tzu-Yun Kung
Yu-Kai Ma
Pei-Yun Zeng
Ching-Chuan Cheng
Yu-Jen Chang
Yu-Ju Chou
Tsung-Han Kuo
Publication date
01-12-2024
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2024
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/s12993-024-00260-z