Abstract
Although the use of neuroimaging techniques has revealed much about the neural correlates of social decision making (SDM) in humans, it remains poorly understood how social stimuli are represented, and how social decisions are implemented at the neural level in humans and in other species. To address this issue, the establishment of novel animal paradigms allowing a broad spectrum of neurobiological causal manipulations and neurophysiological recordings provides an exciting tool to investigate the neural implementation of social valuation in the brain. Here, we discuss the potential of a rodent model, Rattus norvegicus, for the understanding of SDM and its neural underpinnings. Particularly, we consider recent data collected in a rodent prosocial choice task within a social reinforcement framework and discuss factors that could drive SDM in rodents.
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Notes
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The term “antisocial” needs to be interpreted with caution, because rats’ choices may have been motivated by nonsocial factors that were unrelated to malicious, egocentric, or other “antisocial” motives. We use the term “antisocial” agnostically to describe the negative effect of social context on social preferences.
References
Adolphs R (2009) The social brain: neural basis of social knowledge. Annu Rev Psychol 60:693–716
Adolphs R (2010) What does the amygdala contribute to social cognition? Ann N Y Acad Sci 1191:42–61. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2871162&tool=pmcentrez&rendertype=abstract. Accessed 10 Dec 2014
Atsak P, Orre M, Bakker P, Cerliani L, Roozendaal B, Gazzola V, Moita M, Keysers C (2011) Experience modulates vicarious freezing in rats: a model for empathy. PloS one 6:e21855. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3135600&tool=pmcentrez&rendertype=abstract. Accessed 29 May 2013
Baenninger LP (1966) The reliability of dominance orders in rats. Anim Behav 14:367–371. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0003347266800994
Barnett SA, Spencer MM (1951) Feeding, social behaviour and interspecific competition in wild rats. Behaviour 229–242. Available at: http://psycnet.apa.org/psycinfo/1952-01970-001. Accessed 27 Mar 2012
Behrens TEJ, Hunt LT, Woolrich MW, Rushworth MFS (2008) Associative learning of social value. Nature 456:245–249
Bartal IBA, Rodgers DA, Sarria MSB, Decety J, Mason P (2014) Pro-social behavior in rats is modulated by social experience. Elife 3:e01385. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3884117&tool=pmcentrez&rendertype=abstract. Accessed January 20, 2014
Bhanji JP, Delgado MR (2013) The social brain and reward: social information processing in the human striatum. WIRE Cogn Sci
Brennan PA, Kendrick KM (2006) Mammalian social odours: attraction and individual recognition. Philos Transac Royal Soc Lond Ser B, Biol Sci 361:2061–2078
Brosnan SF, de Waal FBM (2014) Evolution of responses to (un)fairness. Science. Published online before print. Available at: http://www.sciencemag.org/cgi/doi/10.1126/science.1251776. Accessed 16 Oct 2014
Bunch GB, Zentall TR (1980) Imitation of a passive avoidance response in the rat. Bull Psychon Soc 15:73–75. Available at: http://link.springer.com/10.3758/BF03334469
Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J (2008) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 122:357–367. Available at: http://doi.apa.org/getdoi.cfm?doi=10.1037/a0012889
Carrillo M, Migliorati F, Bruls R, Han Y, Heinemans M, Pruis I, Gazzola V, Keysers C (2015) Repeated Witnessing of Conspecifics in Pain: effects on emotional contagion. Plos One 10:e0136979. Available at: http://dx.plos.org/10.1371/journal.pone.0136979
Chang SWC, Winecoff AA, Platt ML (2011) Vicarious reinforcement in rhesus macaques (Macaca Mulatta). Front Neurosci 5:10
Crockett MJ, Fehr E (2014) Social brains on drugs: tools for neuromodulation in social neuroscience. Soc Cogn Affect Neurosci 9:250–254
Crowley PH, Zentall TR (eds) (2013) Comparative decision making, 1 edition. Oxford University Press, New York, 27 Feb 2013
Daniel WJ (1942) Cooperative problem solving in rats. J Comp Psychol 34:361–368. Available at: http://content.apa.org/journals/com/34/3/361
Daniel WJ (1943) Higher order cooperative problem solving in rats. J Comp Psychol 35:297–305. Available at: http://content.apa.org/journals/com/35/3/297
Decety J, Chen C, Harenski C, Kiehl KA (2013) An fMRI study of affective perspective taking in individuals with psychopathy: imagining another in pain does not evoke empathy. Front Human Neurosci 7:489. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3782696&tool=pmcentrez&rendertype=abstract
Gadziola MA, Grimsley JMS, Faure PA, Wenstrup JJ (2012a) Social vocalizations of big brown bats vary with behavioral context. PLoS ONE 7
Gadziola MA, Grimsley JMS, Shanbhag SJ, Wenstrup JJ (2012b) A novel coding mechanism for social vocalizations in the lateral amygdala. J Neurophysiol 107:1047–1057
Galef B, Whiskin E (2008) “Conformity” in Norway rats? Animal Behav 75:2035–2039. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0003347208001000. Accessed 21 July 2011
Galef BG (1985) Direct and indirect behavioral pathways to the social transmission of food avoidance. Ann N Y Acad Sci 443:203–215. Available at: http://www.ncbi.nlm.nih.gov/pubmed/2990282
Gardner R, Corbin TL, Beltramo J, Nickell G (1984) The prisoner’s dilemma game and cooperation in the rat. Psychol Rep 55:687–696
Grimsley JMS, Hazlett EG, Wenstrup JJ (2013) Coding the meaning of sounds: contextual modulation of auditory responses in the basolateral amygdala. J Neurosci 33:17538–17548. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3812514&tool=pmcentrez&rendertype=abstract
Hastings PD, Utendale WT, Sullivan C (2007) The socialization of prosocial development. In: Grusec JE, Hastings PD (eds) Handbook of socialization: theory and research, the Guilfo. Guilford Publications, New York, pp 638–664
Hernandez-Lallement J, Kuss K, Trautner P, Weber B, Falk A, Fliessbach K (2014) Effort increases sensitivity to reward and loss magnitude in the human brain. Social cogn Affect Neurosci. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23202663
Hernandez-Lallement J, van Wingerden M, Marx C, Srejic M, Kalenscher T (2015) Rats prefer mutual rewards in a prosocial choice task. Front Neurosci 8:1–9. Available at: http://www.frontiersin.org/Decision_Neuroscience/10.3389/fnins.2014.00443/abstract. Accessed 16 Jan 2015
Hernandez-Lallement J, van Wingerden M, Schäble S, Kalenscher T (2016) Basolateral amygdala lesions abolish mutual reward preferences in rats. Neurobiol Learn Mem 127:1–9
Izuma K, Saito DN, Sadato N (2008) Processing of social and monetary rewards in the human striatum. Neuron 58:284–294
Kalenscher T, van Wingerden M (2011) Why we should use animals to study economic decision making—a perspective. Fron Neurosci 5:82. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3118901&tool=pmcentrez&rendertype=abstract. Accessed 21 July 2011
Kashtelyan V, Lichtenberg NT, Chen ML, Cheer JF, Roesch MR (2014) Observation of reward delivery to a conspecific modulates dopamine release in ventral striatum. Curr Biol 24:2564–2568. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0960982214011361. Accessed 24 Oct 2014
Kim EJ, Kim ES, Covey E, Kim JJ (2010) Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PloS one 5:e15077. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2995742&tool=pmcentrez&rendertype=abstract. Accessed 14 June 2011
Knoch D, Pascual-Leone A, Meyer K, Treyer V, Fehr E (2006) Diminishing reciprocal fairness by disrupting the right prefrontal cortex. Science (New York, NY) 314:829–832. Available at: http://www.ncbi.nlm.nih.gov/pubmed/17023614. Accessed 19 July 2011
Knutson B, Burgdorf J, Panksepp J (1999) High-frequency ultrasonic vocalizations index conditioned pharmacological reward in rats. Physiol Behav 66:639–643. Available at: http://www.ncbi.nlm.nih.gov/pubmed/10386908
Lahvis GP, Panksepp JB, Kennedy BC, Wilson CR, Merriman DK (2015) Social conditioned place preference in the captive ground squirrel Ictidomys tridecemlineatus: social reward as a natural phenotype. J Comp Psychol 129:291–303
Litvin Y, Blanchard DC, Blanchard RJ (2007) Rat 22 kHz ultrasonic vocalizations as alarm cries. Behav Brain Res 182:166–172. Available at: http://www.ncbi.nlm.nih.gov/pubmed/17173984. Accessed 5 Nov 2011
Łopuch S, Popik P (2011) Cooperative behavior of laboratory rats (Rattus norvegicus) in an instrumental task. J Comp Psychol (Washington, DC: 1983) 125:250–253. Available at: http://www.ncbi.nlm.nih.gov/pubmed/21341907. Accessed 6 Mar 2013
Marcuella H, Owens K (1975) Cooperative problem solving by albino rats: a re-evaluation. Psychol Rep 37:591–598
Margittai Z, Strombach T, van Wingerden M, Joëls M, Schwabe L, Kalenscher T (2015) A friend in need: time-dependent effects of stress on social discounting in men. Horm Behav 73:75–82. Available at: http://www.scopus.com/inward/record.url?eid=2-s2.0-84935493433&partnerID=40&md5=a43a37fa689897eaac7e52a6fcef99e9
Marquez C, Moita M (2012) Rats cooperate in the absence of direct benefit: development of a new behavioural task. In: Society for neuroscience, pp 14–15. New Orleans
Márquez C, Rennie SM, Costa DF, Moita MA (2015) Prosocial choice in rats depends on food-seeking behavior displayed by recipients. Curr Biol 1–10. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0960982215005928
Masuda A, Aou S (2009) Social transmission of avoidance behavior under situational change in learned and unlearned rats. PloS one 4:e6794. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2728840&tool=pmcentrez&rendertype=abstract. Accessed 11 Nov 2013
Naumann RT, Kanwal JS (2011) Basolateral amygdala responds robustly to social calls: spiking characteristics of single unit activity. J Neurophysiol 105:2389–2404
Niv Y, Montague PR (2008) Theoretical and empirical studies of learning. Learning 329–350
Panksepp JB, Lahvis GP (2011) Rodent empathy and affective neuroscience. Neurosci Biobehav Rev 35:1864–1875. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3183383&tool=pmcentrez&rendertype=abstract. Accessed 26 Sept 2013
Parsana AJ, Li N, Brown TH (2012) Positive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala. Behav Brain Res 226:77–86. Available at: http://dx.doi.org/10.1016/j.bbr.2011.08.040
Peterson DC, Wenstrup JJ (2012) Selectivity and persistent firing responses to social vocalizations in the basolateral amygdala. Neuroscience 217:154–171. Available at: http://dx.doi.org/10.1016/j.neuroscience.2012.04.069
Pfeiffer T, Rutte C, Killingback T, Taborsky M, Bonhoeffer S (2005) Evolution of cooperation by generalized reciprocity. Proc Biol Sci Royal Soc 272:1115–1120. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1559812&tool=pmcentrez&rendertype=abstract. Accessed 26 July 2011
Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187. Available at: http://www.ncbi.nlm.nih.gov/pubmed/16242399. Accessed 10 July 2014
Rilling JK, Sanfey AG (2011) The neuroscience of social decision-making. Ann Rev Psychol 62:23–48. Available at: http://www.ncbi.nlm.nih.gov/pubmed/20822437. Accessed 11 June 2011
Ruff CC, Fehr E (2014) The neurobiology of rewards and values in social decision making. Nat Rev Neurosci 15:549–562. Available at: http://www.ncbi.nlm.nih.gov/pubmed/24986556. Accessed 9 July 2014
Rutte C, Taborsky M (2007a) The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. Behav Ecol Sociobiol 62:499–505. Available at: http://www.springerlink.com/index/10.1007/s00265-007-0474-3. Accessed 5 July 2011
Rutte C, Taborsky M (2007b) Generalized reciprocity in rats. PLoS Biol 5:e196. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1914408&tool=pmcentrez&rendertype=abstract. Accessed 14 June 2011
Schneeberger K, Dietz M, Taborsky M (2012) Reciprocal cooperation between unrelated rats depends on cost to donor and benefit to recipient. BMC Evol Biol 12:41. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3340299&tool=pmcentrez&rendertype=abstract. Accessed 13 Nov 2012
Schoenbaum G, Chiba AA, Gallagher M (1999) Neural encoding in orbitofrontal cortex and basolateral amygdala during olfactory discrimination learning. The J Neurosci Official J Soc Neurosci 19:1876–1884
Schoenbaum G, Setlow B, Saddoris MP, Gallagher M (2003) Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39:855–867
Schultz W (2006) Behavioral theories and the neurophysiology of reward. Ann Rev Psychol 57:87–115. Available at: http://www.ncbi.nlm.nih.gov/pubmed/16318590. Accessed 8 Mar 2012
Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599. Available at: http://www.sciencemag.org/cgi/doi/10.1126/science.275.5306.1593. Accessed 4 Oct 2012
Schuster R (2002) Cooperative coordination as a social behavior. Human Nat 13:47–83
Seffer D, Schwarting RKW, Wöhr M (2014) Pro-social ultrasonic communication in rats: Insights from playback studies. J Neurosci Methods 1–9. Available at: http://www.ncbi.nlm.nih.gov/pubmed/24508146. Accessed 3 April 2014
Sharp SP, McGowan A, Wood MJ, Hatchwell BJ (2005) Learned kin recognition cues in a social bird. Nature 434:1127–1130. Available at: http://www.ncbi.nlm.nih.gov/pubmed/15858573
Silk JB, House BR (2011) Evolutionary foundations of human prosocial sentiments. Proc National Acad Sci USA 108 Suppl:10910–10917. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3131813&tool=pmcentrez&rendertype=abstract. Accessed 19 March 2014
Strombach T, Weber B, Hangebrauk Z, Kenning P, Karipidis II, Tobler PN, Kalenscher T (2015) Social discounting involves modulation of neural value signals by temporoparietal junction. Proc National Acad Sci 112:1619–1624. Available at: http://www.pnas.org/lookup/doi/10.1073/pnas.1414715112
Taylor CJ (1975) Study of altruism in rats in an appetitive situation. Psychological reports 36:571–574. Available at: http://www.amsciepub.com/doi/abs/10.2466/pr0.1975.36.2.571
Viana DS, Gordo I, Sucena E, Moita MAP (2010) Cognitive and motivational requirements for the emergence of cooperation in a rat social game. PloS one 5:e8483. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2799661&tool=pmcentrez&rendertype=abstract. Accessed 14 Oct 2011
Wang Y, Fontanini A, Katz DB (2006) Temporary basolateral amygdala lesions disrupt acquisition of socially transmitted food preferences in rats. Learn Mem 13:794–800
Wesson DW (2013) Sniffing behavior communicates social hierarchy. Curr Biol 23:575–580. Available at: http://dx.doi.org/10.1016/j.cub.2013.02.012
Willuhn I, Tose A, Wanat MJ, Hart AS, Hollon NG, Phillips PEM, Schwarting RKW, Wöhr M (2014) Phasic dopamine release in the nucleus accumbens in response to pro-social 50 kHz ultrasonic vocalizations in rats. J Neurosci Official J Soc Neurosci 34:10616–10623. Available at: http://www.ncbi.nlm.nih.gov/pubmed/25100595. Accessed 7 Nov 2014
Wilson DS (2015) Altruism in everyday life. In: Does Altruism Exist?: culture, genes, and the welfare of others, pp 117–129. Yale University Press, January 13 2015
Wöhr M, Houx B, Schwarting RKW, Spruijt B (2008) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93:766–776. Available at: http://www.ncbi.nlm.nih.gov/pubmed/18191963. Accessed 7 Nov 2013
Wöhr M, Schwarting RKW (2007) Ultrasonic communication in rats: can playback of 50 kHz calls induce approach behavior? PLoS ONE 2:e1365. Available at: http://dx.plos.org/10.1371/journal.pone.0001365
Wöhr M, Schwarting RKW (2008) Ultrasonic calling during fear conditioning in the rat: no evidence for an audience effect. Animal Behav 76:749–760. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0003347208002108. Accessed 11 Dec 2011
Zentall T, Levine J (1972) Observational learning and social facilitation in the rat. Science (New York, NY) 178:1220–1221
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This work was supported by a grant from Deutsche Forschungsgemeinschaft (DFG Grant No. KA 2675/6-1). MvW was supported by the Volkswagen Stiftung “Freigeist” fellowship, AZ 88216.
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Hernandez-Lallement, J., van Wingerden, M., Schäble, S., Kalenscher, T. (2016). A Social Reinforcement Learning Hypothesis of Mutual Reward Preferences in Rats. In: Wöhr, M., Krach, S. (eds) Social Behavior from Rodents to Humans. Current Topics in Behavioral Neurosciences, vol 30. Springer, Cham. https://doi.org/10.1007/7854_2016_436
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