Social reward among juvenile mice

Abstract

Mammalian social relationships, such as mother–offspring attachments and pair bonds, can directly affect reproductive output. However, conspecifics approach one another in a comparatively broad range of contexts, so conceivably there are motivations for social congregation other than those underlying reproduction, parental care or territoriality. Here, we show that reward mediated by social contact is a fundamental aspect of juvenile mouse sociality. Employing a novel social conditioned place preference (SCPP) procedure, we demonstrate that social proximity is rewarding for juvenile mice from three inbred strains (A/J, C57BL/6J and DBA/2J), while mice from a fourth strain (BALB/cJ) are much less responsive to social contact. Importantly, this strain‐dependent difference was not related to phenotypic variability in exploratory behavior or contextual learning nor influenced by the genetic background associated with maternal care or social conditioning. Furthermore, the SCPP phenotype was expressed early in development (postnatal day 25) and did not require a specific sex composition within the conditioning group. Finally, SCPP responses resulted from an interaction between two specifiable processes: one component of the interaction facilitated approach toward environments that were associated with social salience, whereas a second component mediated avoidance of environmental cues that predicted social isolation. We have thus identified a genetically prescribed process that can attribute value onto conditions predicting a general form of social contact. To our knowledge, this is the first definitive evidence to show that genetic variation can influence a form of social valuation not directly related to a reproductive behavior.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 78

1. 1.

   Agmo A, Gomez M. Sexual reinforcement is blocked by infusion of naloxone into the medial preoptic area. Behav Neurosci. 1993;107:812-818.

   Not in our library10.1037//0735-7044.107.5.812

2. 2.

   Bardo MT, Bevins RA. Conditioned place preference: what does it add to our preclinical understanding of drug reward? Psychopharmacology (Berl). 2000;153:31-43.

   Not in our library10.1007/s002130000569

3. 3.

   Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev. 1998;28:309-369.

   Not in our library10.1016/s0165-0173(98)00019-8

4. 4.

   Berridge KC, Robinson TE. Parsing reward. Trends Neurosci. 2003;26:507-513.

   Not in our library10.1016/s0166-2236(03)00233-9

5. 5.

   Berton O, McClung CA, Dileone RJ, Krishnan V, Renthal W, Russo SJ, Graham D, Tsankova NM, Bolanos CA, Rios M, Monteggia LM, Self DW, Nestler EJ. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science. 2006;311:864-868.

   Not in our library10.1126/science.1120972

6. 6.

   Bielsky IF, Hu SB, Ren X, Terwilliger EF, Young LJ. The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron. 2005;47:503-513.

   Not in our library10.1016/j.neuron.2005.06.031

7. 7.

   Bouwknecht JA, Paylor R. Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res. 2002;15:489-501.

   Not in our library10.1016/s0166-4328(02)00200-0

8. 8.

   Brodkin ES. BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav Brain Res. 2006.

   Not in our library10.1016/j.bbr.2006.06.025

9. 9.

   Brodkin ES, Hagemann A, Nemetski SM, Silver LM. Social approach avoidance behavior of inbred mouse strains towards DBA/2 mice. Brain Res. 2004;1002:151-157.

   Not in our library10.1016/j.brainres.2003.12.013

10. 10.

    Broekman M, de Bruin M, Smeenk J, Slob AK, van der Schoot P. Partner preference behavior of estrous female rats affected by castration of tethered male incentives. Horm Behav. 1988;22:324-337.

    Not in our library10.1016/0018-506x(88)90005-0

11. 11.

    Bucan M, Abel T. The mouse: genetics meets behaviour. Nat Rev Genet. 2002;3:114-123.

    Not in our library10.1038/nrg728

12. 12.

    Byrom AE, Krebs CJ. Natal dispersal of juvenile arctic ground squirrels in the boreal forest. Can J Zool. 1999;77:1048-1059.

    Not in our library

13. 13.

    Calcagnetti DJ, Schechter MD. Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav. 1992;51:667-672.

    Not in our library10.1016/0031-9384(92)90101-7

14. 14.

    Camacho F, Sandoval C, Paredes RG. Sexual experience and conditioned place preference in male rats. Pharmacol Biochem Behav. 2004;78:419-425.

    Not in our library10.1016/j.pbb.2004.04.015

15. 15.

    Cohen RM, Kang A, Gulick C. Quantitative trait loci affecting the behavior of A/J and CBA/J intercross mice in the elevated plus maze. Mamm Genome. 2001;12:501-507.

    Not in our library10.1007/s00335-001-2047-5

16. 16.

    Crawley JN, Belknap JK, Collins A, Crabbe JC, Frankel W, Henderson N, Hitzemann RJ, Maxson SC, Miner LL, Silva AJ, Wehner JM, Wynshaw-Boris A, Paylor R. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl). 1997;132:107-124.

    Not in our library10.1007/s002130050327

17. 17.

    Deak T, Panksepp J. Play behavior in rats pretreated with scopolamine: increased play solicitation by the non-injected partner. Physiol Behav. 2006;87:120-125.

    Not in our library10.1016/j.physbeh.2005.09.009

18. 18.

    Deaner RO, Khera AV, Platt ML. Monkeys pay per view: adaptive valuation of social images by rhesus macaques. Curr Biol. 2005;15:543-548.

    Not in our library10.1016/j.cub.2005.01.044

19. 19.

    Depue RA, Morrone-Strupinsky JV. A neurobehavioral model of affiliative bonding: implications for conceptualizing a human trait of affiliation. Behav Brain Sci. 2005;28:313-350.

    Not in our library10.1017/s0140525x05000063

20. 20.

    Dickinson A, Balleine B, Pashler H, Gallistel R. The role of learning in the operation of motivational systems. Stevens’ Handbook of Experimental Psychology. 2002;3:497-533.

    Not in our library

21. 21.

    Douglas LA, Varlinskaya EI, Spear LP. Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation. Physiol Behav. 2003;80:317-325.

    Not in our library10.1016/j.physbeh.2003.08.003

22. 22.

    Douglas LA, Varlinskaya EI, Spear LP. Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol. 2004;45:153-162.

    Not in our library10.1002/dev.20025

23. 23.

    Drewett RF. Sexual behaviour and sexual motivation in the female rat. Nature. 1973;242:476-477.

    Not in our library10.1038/242476a0

24. 24.

    Drickamer LC, Wagner DM, Robinson AS. Double captures of house mice (Mus musculus) with information on genetic relatedness. Am Midl Nat. 2003;150:308-320.

    Not in our library

25. 25.

    Dugatkin LA. Animal cooperation among unrelated individuals. Naturwissenschaften. 2002;89:533-541.

    Not in our library10.1007/s00114-002-0379-y

26. 26.

    Ebensberger LA. A review of the evolutionary causes of group-living. Acta Theriol. 2001;46:115-144.

    Not in our library

27. 27.

    Edwards DA, Griffis KT, Tardivel C. Olfactory bulb removal: effects on sexual behavior and partner-preference in male rats. Physiol Behav. 1990;48:447-450.

    Not in our library10.1016/0031-9384(90)90342-2

28. 28.

    Fish EW, DeBold JF, Miczek KA. Escalated aggression as a reward: corticosterone and GABA(A) receptor positive modulators in mice. Psychopharmacology (Berl). 2005;182:116-127.

    Not in our library10.1007/s00213-005-0064-x

29. 29.

    Fitchett AE, Barnard CJ, Cassaday HJ. There’s no place like home: cage odours and place preference in subordinate CD-1 male mice. Physiol Behav. 2006;87:955-962.

    Not in our library10.1016/j.physbeh.2006.02.010

30. 30.

    Gerlach G. Impact of social ties on dispersal, reproduction and dominance in feral house mice. Ethology. 1998;104:487-499.

    Not in our library

31. 31.

    Glickman SE, Schiff BB. A biological theory of reinforcement. Psychol Rev. 1967;74:81-109.

    Not in our library10.1037/h0024290

32. 32.

    Hamilton WD. Geometry for the selfish herd. J Theor Biol. 1971;31:295-311.

    Not in our library10.1016/0022-5193(71)90189-5

33. 33.

    Ikemoto S, Panksepp J. The effects of early social isolation on the motivation for social play in juvenile rats. Dev Psychobiol. 1992;25:261-274.

    Not in our library10.1002/dev.420250404

34. 34.

    Ikemoto S, Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev. 1999;31:6-41.

    Not in our library10.1016/s0165-0173(99)00023-5

35. 35.

    Insel TR. Is social attachment an addictive disorder? Physiol Behav. 2003;79:351-357.

    Not in our library10.1016/s0031-9384(03)00148-3

36. 36.

    Jenkins WJ, Becker JB. Female rats develop conditioned place preferences for sex at their preferred interval. Horm Behav. 2003;43:503-507.

    Not in our library10.1016/s0018-506x(03)00031-x

37. 37.

    Kalivas PW, Volkow ND. The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry. 2005;162:1403-1413.

    Not in our library10.1176/appi.ajp.162.8.1403

38. 38.

    Kelley AE, Fellous J-M, Arbib MA. Neurochemical networks encoding emotion and motivation: an evolutionary perspective. Who Needs Emotions? The Brain Meets The Robot. 2005;29-77.

    Not in our library

39. 39.

    Kelley AE, Berridge KC. The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci. 2002;22:3306-3311.

    Not in our library10.1523/jneurosci.22-09-03306.2002

40. 40.

    Koch PC, Peters RH. Suppression of adult copulatory behaviors following LiCl-induced aversive contingencies in juvenile male rats. Dev Psychobiol. 1987;20:603-611.

    Not in our library10.1002/dev.420200606

Cited by papers we hold 7

• Role of VTA dopamine neurons and neuroligin 3 in sociability traits related to nonfamiliar conspecific interaction · 2018
  No notice
• To Group or Not to Group? Good Practice for Housing Male Laboratory Mice · 2017
  No notice
• Striatal Circuits as a Common Node for Autism Pathophysiology · 2016
  No notice
• Male mice song syntax depends on social contexts and influences female preferences · 2015
  No notice
• Adult Male Mice Emit Context-Specific Ultrasonic Vocalizations That Are Modulated by Prior Isolation or Group Rearing Environment · 2012
  No notice
• Empathy Is Moderated by Genetic Background in Mice · 2009
  No notice
• Affiliative Behavior, Ultrasonic Communication and Social Reward Are Influenced by Genetic Variation in Adolescent Mice · 2007
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.