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The neurobiology of punishment

Key Points

  • Punishment is common across species, where it often serves to protect the personal interests of the animal concerned. In humans, it seems to promote and preserve cooperative behaviour, according to culturally acquired (moral) norms of behaviour. This extends to the existence of altruistic punishment, in which the act of punishing is personally costly to the punisher, but protects the cooperative interests of the group.

  • An account of the proximate basis of punishment focuses attention on the behavioural and neurobiological basis of motivation, and an understanding how basic learning and action selection systems deal with outcomes that involve other individuals.

  • Appetitive and aversive systems motivate actions through Pavlovian, habit-based and goal-directed actions, which are acquired in specific ways. Particularly important for social and altruistic actions may be learning through observation, in which naïve observers learn actions from others. This reflects the cultural acquisition of behaviour, and may be an underlying component of social norm development.

  • In social decision-making situations, individuals often benefit from cooperation. However, many cooperative situations give rise to the temptation to free-ride on the cooperative behaviour of others. This can be deterred by punishing non-cooperative free-riding behaviour. This pays off in the long run if the punisher interacts with the reformed free-rider again, but is costly if they do not.

  • Altruistic punishment appears to be common across diverse human cultures. It extends to third-party situations, in which passive observers punish those that they witness acting unfairly. It may be especially powerful in promoting cooperation when combined with other forms of punishment that arise from direct and indirect modes of reciprocity.

  • In the brain, recent functional MRI studies have highlighted key areas involved in the recognition and representation of unfairness (anterior insula), in the establishment of retributive goals (orbitofrontal cortex), and in the execution of punishing actions (striatum).

  • We outline a neurobiological model of punishment, in which an amygdala-centred pathway mediates impulsive, retaliative punishment, and a striatal system mediates instrumental punishment. This latter system may mediate goal-directed punishing actions that involve forward planning (that is, reciprocity-based punishment), as well as more habit-like punishing actions as experience becomes more extensive.

  • Consideration of the learning systems that underlie punishment predict that selfish reciprocity is likely to generalize to altruistic (strong) reciprocity. Accordingly, it may not be necessary to assume that altruistic retributive goals are inherited unconditioned appetitive stimuli.

  • Future research needs to focus on exploring more precisely the type actions that underlie altruistic punishment (at a proximate level), and understanding how learning and evolution interact in shaping cooperative behaviour (at an ultimate level).

Abstract

Animals, in particular humans, frequently punish other individuals who behave negatively or uncooperatively towards them. In animals, this usually serves to protect the personal interests of the individual concerned, and its kin. However, humans also punish altruistically, in which the act of punishing is personally costly. The propensity to do so has been proposed to reflect the cultural acquisition of norms of behaviour, which incorporates the desire to uphold equity and fairness, and promotes cooperation. Here, we review the proximate neurobiological basis of punishment, considering the motivational processes that underlie punishing actions.

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Figure 1: Appetitive and aversive excitators and inhibitors.
Figure 2: Different mechanisms of learning and action.
Figure 3: Punishment in a public goods game.
Figure 4: Putative neurobiological substrates of punishment.
Figure 5: Fairness related outcome representations.

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Acknowledgements

B.S. and R.D. are supported by a Wellcome Trust Programme Grant to R.D. T.S. was supported by the Medical Research Council. The authors thank N. Daw, P. Dayan and the anonymous reviewers for comments on the manuscript.

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Glossary

Kin selection

Evolutionary models which predict that animals should be motivated to protect their relatives, to ultimately preserve their genetic inheritance.

Direct reciprocity

So called 'tit-for-tat reciprocity', in which a beneficial act to another individual is likely to be reciprocated by that individual.

Indirect reciprocity

Sometimes to referred to as reputation formation, this involves acquiring a reputation as being beneficial towards others, and therefore being treated favourably by them.

Altruistic punishment

Punishing that involves a selfless personal cost to the punisher, which is never likely to be recovered.

Pavlovian learning

Learning that a previously neutral environmental cue predicts a motivational salient outcome.

Instrumental learning

Learning that a particular action predicts a motivational salient outcome.

Credit assignment problem

This refers to the problem of attributing value to intermediate states and actions in sequential learning.

Ultimate basis

The ultimate basis of an observed behaviour refers to the overall reason for the existence of the behaviour, typically approached in terms of its evolutionary basis.

Proximate basis

The proximate basis of an observed behaviour refers to its immediate cause, such as the underlying neurobiological process.

Conditioned reinforcement

The process by which a Pavlovian-acquired value can reinforce instrumental action.

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Seymour, B., Singer, T. & Dolan, R. The neurobiology of punishment. Nat Rev Neurosci 8, 300–311 (2007). https://doi.org/10.1038/nrn2119

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