The role of serotonergic action in amygdala in rodent prosocial behavior
Final Report Abstract
Humans are social animals. We accept costs to help others, even if we don’t obtain immediate or future benefits from our altruistic actions, even if we don’t know the recipient of our help, and even if the recipient will never repay the favour. Such social behaviour is a puzzle for economists, psychologists and evolutionary biologists alike: why do people consider the well‐being of others? Why do they voluntarily reduce their own evolutionary fitness to increasing someone else’s? Interestingly, not only human decision‐makers, but also non‐human animals often reveal social preferences. Judging by face validity, humans and some animal species have very similar, maybe even identical social cognitions. Therefore, one promising avenue to understand the cognitive, neural and evolutionary underpinnings of social decision‐making is to investigate animal social behavior. This was the primary goal of the projects conducted during the two funding period. In these two funding periods, we developed a Rodent Prosocial Choice Task (PCT) to investigate a special type of prosocial behavior in rats - mutual‐reward preferences (preference for a reward distribution that benefit the ‘actor’ rat and a conspecific over a distribution that benefits only the actor rat, not the conspecific). Using this task, we provided evidence that rats show advantageous (aversion against being better off than a conspecific and disadvantageous inequity aversion (aversion against being worse off than a conspecific. We argued that mutualreward preferences do not necessarily require empathy, but may be the result of social reinforcement learning where social signals, e.g., ultrasonic vocalizations, emitted by the conspecific receiving reward might reinforce those behaviors in the actor rat that produce rewards to conspecifics. We furthermore found that the integrity of basolateral amygdala (BLA) was necessary for expressing mutual‐reward preferences. This finding has translational value as a potential animal model for studying callousness – a trait characteristic for several psychiatric conditions, including conduct disorder and psychopathy. The role of the amygdala in orchestrating social behavior was corroborated in another study showing that lesions of BLA abolished the behavioral responses to ultrasonic vocalizations - the main candidate for social reinforcement learning in the PCT. We also demonstrated that psychopharmacological microinjections of a serotonin receptor agonist locally into BLA, boosting serotonin action in the amygdala, increased rat mutual‐reward tendencies in the PCT. Finally, we found no evidence for a correlation between mutual‐reward preferences and time preferences (delay discounting), possibly because of power concerns (too small effect size for a manageable sample size). In summary, our set of studies demonstrated that rats reveal two special kinds of social preferences - mutual‐reward preferences and inequity aversion which are likely the result of social reinforcement learning. Mutual‐reward preferences are amygdala‐dependent and can be fostered by increasing serotonin‐action in the amygdala. The two funding period resulted in the completion of two doctorates (Dr. Julen Hernandez‐Lallement, PhD defense in 2016 and Dr. Lina Oberließen, PhD defense in 2019).
Publications
- (2015) Rats prefer mutual rewards in a prosocial choice task. Frontiers in Neuroscience 8:1‐9
Hernandez‐Lallement J, Van Wingerden M, Marx C, Srejic M, Kalenscher T
(See online at https://doi.org/10.3389/fnins.2014.00443) - (2016) Basolateral amygdala lesions abolish mutual reward preferences in rats. Neurobiol Learn Mem 127:1‐9
Hernandez‐Lallement J, van Wingerden M, Schable S, Kalenscher T
(See online at https://doi.org/10.1016/j.nlm.2015.11.004) - (2016) Inequity aversion in rats, Rattus norvegicus. Anim Behav 115:157‐166
Oberließen L, Hernandez‐Lallement J, Schäble S, van Wingerden M, Seinstra M, Kalenscher T
(See online at https://doi.org/10.1016/j.anbehav.2016.03.007) - (2017) A Social Reinforcement Learning Hypothesis of Mutual Reward Preferences in Rats. Curr Top Behav Neurosci 30:159‐176
Hernandez‐Lallement J, van Wingerden M, Schable S, Kalenscher T
(See online at https://doi.org/10.1007/7854_2016_436) - (2018) Towards an animal model of callousness. Neurosci Biobehav Rev 91:121‐129
Hernandez‐Lallement J, van Wingerden M, Kalenscher T
(See online at https://doi.org/10.1016/j.neubiorev.2016.12.029) - (2019) Social and Non‐social Mechanisms of Inequity Aversion in Non‐human Animals. Front Behav Neurosci 13:1‐11
Oberließen L, Kalenscher T
(See online at https://doi.org/10.3389/fnbeh.2019.00133) - (2020) 5‐HT1A receptor agonism in the basolateral amygdala increases mutual‐reward choices in rats. Sci Rep. 10: 16622
Schönfeld LM, Schäble S, Zech MP, Kalenscher T
(See online at https://doi.org/10.1038/s41598-020-73829-z) - (2020) How the Brain Attends to the Joys and Pains of Others. Curr Biol 30: R1076‐R1078
Kalenscher T
(See online at https://doi.org/10.1016/j.cub.2020.07.051) - (2020) Lesions of the rat basolateral amygdala reduce the behavioral response to ultrasonic vocalizations. Behav Brain Res 378:112274
Schönfeld LM, Zech MP, Schable S, Wöhr M, Kalenscher T
(See online at https://doi.org/10.1016/j.bbr.2019.112274) - (2020) Vicarious reward unblocks associative learning about novel cues in male rats. eLife 9: e60755
van Gurp S, Hoog J, Kalenscher T, van Wingerden M
(See online at https://doi.org/10.7554/eLife.60755)
