Research Papers Underlined Altruism

Introduction

Many social interactions are self-beneficial if we behave positively and pro-cooperatively towards others. Opportunities to benefit from cooperation are widespread, and reflect the extrinsic fact that the natural environment is often best harvested, insofar as rewards can be accrued and threats avoided, by working together. But the decision to cooperate is not always straightforward, as in some situations it leaves us vulnerable to exploitation by others.

Game theory specifies a set of potential social interactions in which outcomes of cooperation and defection systematically differ, allowing both experimentalists and theoreticians to probe an individual’s propensity for cooperation in different situations (Camerer, 2003 ). These outcomes typically vary in the extent to which competitive actions may seem preferable and where a short-sighted temptation to exploit the cooperativeness of others has a capacity to subvert cooperation later. Fortunately, the ability to look beyond the immediate returns of defection towards longer-term cooperation allows humans to escape from otherwise competitive equilibria, and this can be viewed as a hallmark of rational, sophisticated behaviour.

However, humans appear to behave positively towards each other in situations in which there is no capacity to benefit from long-term cooperation: for instance, when they play single games in which they never meet the same opponent again, and when their identities are kept anonymous (Fehr et al., 1993 ; Berg et al., 1995 ; Fehr and Fischbacher, 2003 ). This removes the capacity for both direct reciprocity (tit-for-tat) (Trivers, 1971 ; Axelrod, 1984 ), and the ability to earn a cooperative and trustworthy reputation that can be communicated by a third-party (Harbaugh, 1998 ; Bateson et al., 2006 ; Ariely and Norton, 2007 ). Furthermore, they will do this even if it is costly to themselves (Xiao and Houser, 2005 ; Henrich et al., 2006 ). From an economic perspective this appears to be genuinely altruistic, being strictly irrational since it incurs a direct personal cost with no conceivable long-term benefit.

Arguments against altruistic interpretations of experimentally observed behaviour include suggestions that individuals do not understand the rules of the game, are prone to misbelieve they (or their kin) will interact with opponents again in the future, or falsely infer they are being secretly observed and accordingly act to preserve their reputation in the eyes of experimenters (Smith, 1976 ). However, the widespread observation of altruism (both rewarding and punishing) across cultures (Henrich et al., 2001 ), and within meticulously designed experiments conducted by behavioural economists provide compelling support for its presence as a clear behavioural disposition. Furthermore, in fMRI experiments, altruistic actions correlate with brain activity, suggesting that they derive from some sort of intended or motivated behaviour and are not an expression of mere ‘effector noise’ (i.e. decision error) (de Quervain et al., 2004 ).

The very existence of altruism raises the difficult question as to why evolution has allowed otherwise highly sophisticated brains to behave so selflessly. This directs attention towards the decision-making systems that subserve economic and social behaviour (Lee, 2006 , 2008 ; Behrens et al., 2009 ), and questions whether they are structured in such a way that yields altruism either inadvertently, or necessarily. The broader consequence is that if they do, then this reframes the question regarding the ultimate (evolutionary) causes of altruism towards the evolution of these very decision systems, and away from the phenomenological reality of altruism per se.

In this paper, we first review the structure of distinct human decision-making systems by considering a goal-directed (cognitive) system, a habitual system, and an innate (Pavlovian) action system and their interactions. We consider how these systems might operate in social contexts where the key problem is how to make optimal decisions when outcomes depend on the uncertainty associated with other agents and their motives. In the face of such computational complexity, we then consider how optimal actions can be approximated by habit-based decision-making when outcomes are reliably predicted. In this context – through habits – altruism emerges as a consequence of a net economy of computational cost. We also consider the problem of evaluating the best policy when the payoff matrix is unknown but where individuals have an opportunity to learn from others. Observational learning rests upon inferences that might utilise such conspicuous attributes as their personal wealth. We frame observation as an inverse reinforcement learning problem, and consider value functions (including goals and subgoals) that are inferred from others actions, as well as by simpler strategies such as imitation. Notably, with incomplete information – a consequence of not being around to observe the long-term benefits of pro-cooperative behaviours, altruistic outcomes may be inferred as surrogate goals. In this context, altruism arises through optimal inference with incomplete information.

The Architecture of Decision-Making

Studies of decision-making in behavioural neuroscience and psychology have tended to concentrate on elemental decision-making problems, such as reward accrual in simple, stochastic, non-social environments. This enterprise has been very successful and has combined ingenious experimental designs with more classical focal brain lesion paradigms to yield insights into the underlying structure of decision-making systems. One key emerging insight is the likelihood that there is no singly monolithic decision-making system in the brain. Indeed, the best evidence suggest there are at least three distinct decision-making systems comprising a goal-directed, habitual, and innate (Pavlovian) system – with behavioural control being an admixture of cooperation or independence (Dickinson and Balleine, 2002 ; Dayan, 2008 ).

Goal-directed decision-making systems function by building an internal model of the environment. In the simplest case this may simply involve representing the identity of the expected outcome. In more complicated instances, it involves detailed knowledge of the structure of the environment and one’s position within it. Although a goal-directed system may subsume several distinct sub-mechanisms, a wide variety of evidence suggest it localises to prefrontal cortex (Daw et al., 2006 ; Kim et al., 2006 ; Valentin et al., 2007 ), hippocampus (Corbit and Balleine, 2000 ; Kumaran and Maguire, 2006 ; Lengyel and Dayan, 2007 ) and dorsomedial striatum (Balleine and Dickinson, 1998 ; Corbit et al., 2003 ; Yin et al., 2005 ).

Habits, on the other hand, lack specific knowledge of the outcome of their decisions. In the parlance of computer science their values are ‘cached’, and represent only a scalar quantity which describes how good or bad an action is (Daw et al., 2005 ). In animal learning, such values are characterised by their insensitivity to devaluation: changes in state (e.g. moving from hunger to satiety) do not alter the value of the action, since there is no access to the new value of the goal (Dickinson and Balleine, 1994 ; Daw et al., 2005 ). Habits are acquired through experience, and ‘rationalised’ on account of their reliability in predicting rewarding outcomes. This efficiency derives entirely from the way in which they learn: rewards reinforce actions that are statistically predictive of their occurrence, with reinforced actions acquiring value through simple associative learning rules (Rescorla and Wagner, 1972 ; Holman, 1975 ; Adams and Dickinson, 1981 ). These are well described by Reinforcement Learning algorithms (such as Q learning and SARSA; Sutton and Barto, 1998 ), and localise to dorsolateral striatum (O’Doherty et al., 2003 ; Tricomi et al., 2009 ) and dopaminergic projections from substantia nigra.

Control over decisions is often dynamic and frequently transfers from goal-directed mechanisms (early in a task) to a habit-based system (late in a task). Indeed, this transfer can be manipulated by selective lesions to the neural substrates that underlie each of these systems (Balleine et al., 2009 ). In formalising accounts of how these systems interact current views centre on the idea of control being mediated by the respective uncertainties with which each system predicts outcomes, a view that provides a reasonable normative account of experimental findings (Daw et al., 2005 ). At a broader level, the evolutionary rationale for such a dual system is based on computational cost, since habits are vastly less resource demanding than goal-directed mechanisms.

Lastly, animals including humans have an innate, ‘hard-wired’, decision system. This is often referred to as a Pavlovian system, characterised by the expression of values and responses acquired through simple state-based associative learning. Unconditioned and conditioned Pavlovian responses represent an evolutionarily acquired behavioural repertoire that reflect basic, reliable knowledge gleaned from an organisms evolutionary history: embodying such knowledge structures that approaching sweet tasting fruit and withdrawing from bitter tasting fruit are inherently useful responses to enact. But whereas, on average, this inbuilt knowledge structure is enormously valuable to a naïve individual, it may also be a curse in the (usually) uncommon situations in which it is incorrect. The competitive (inhibitory) interaction between decisions based on experience (instrumental habit and goal-directed mechanisms) and those based on Pavlovian impulse localises to brain regions such as the amygdala and ventral striatum (Cardinal et al., 2002 ; Seymour and Dolan, 2008 ). This interaction reflects the classic tension between apparently emotional irrational and rational cognitive systems whereby the emotional expresses an apparent irrationality by way of some peculiarity of the environment.

Decision-Making in Games

A challenge for decision neuroscience is to understand how basic decision-making systems operate within socially interactive environments. Consider the game in Table 1 : the repeated Prisoner’s dilemma. Subjects must choose between one of two actions: cooperate or defect, and their payoff depends on this and the choice of the opponent. Now consider a goal-directed, cognitive decision-making policy in the game, which has the ability to consider multiple future hypothetical scenarios (Figure 1 A). If you neither know, nor care, what the other player does then the best strategy is to defect on the first round, since the outcome is always better regardless of what the other player does. For the same reason, even if you know what he/she will do, it is still better to defect.

Figure 1. Goal-directed learning of Prisoner’s dilemma.(A) In goal-directed learning, players learn the probability of other player’s action: cooperation (C) or defection (D) based on the history of their actions (H) as p(C|H) and p(D|H). They estimate the value of their own actions: V(C) and V(D) using the prediction from the learned model and the expected reward from the pair of actions. (B) In social games, the model of others leads a recursive process: my model of your action includes a model of your estimate of my actions, and so on. Cooperation in the Prisoner’s dilemma depends on these recursive representations; since when I decide to cooperate this time, I must estimate that you are going to cooperate next time as you believe that I am going to cooperate with you.

However, it is also clear that in the long run, both players are better off if they cooperate: this mutually prescribes the best exploitation of environmental resources. Clearly, you need some way of both knowing that your opponent is committed to cooperation as well as a means of signalling to him/her your intention to cooperate. That is, you need to know that she is sophisticated enough to realise that cooperation is worthwhile, and you yourself need to be sophisticated enough to realise this. There is nothing truly altruistic about this, since you are both just trying to maximise your own payoff in an environment that contains another intelligent agent.

Thus, the existence of another intelligent agent in the environment makes the problem more complex than simpler decision-making problems that exploit inanimate environments. In the latter, the payoff probability usually depends fully on the observable states (they are ‘fully observable Markov decision problems’; Bellman, 1957 ). That is, although the payoff may be probabilistic (either involving risk or ambiguity or both), your predictions depend in no way on how you came to arrive at that state in the first place. In social interactions, this assumption does not apply because outcomes depend on what the state thinks about you. If you have recently behaved uncooperatively, then this history negatively influences the payoff you expect to receive. That is, the outcome depends on unobservable states in the environment (making the problem ‘partially observable’). If you find yourself in a seemingly identical state to a previous occasion, for instance playing opponent x in the game y, then the expected payoffs are not independent of how you got there, since opponent x may have a memory of you.

Consequently, social decision-making benefits greatly from constructing some sort of internal model of the key aspects of the environment. In social games this model needs to capture the intentions of the other player (a component of ‘Theory of Mind’). Indeed, your model should also include your opponent’s estimate of your intentions: with this model, you can strategically plan to signal to your opponent your intention to cooperate, knowing that it will change their model of you (Figure 1 B). Accordingly, they should then be more willing to cooperate with you, and you will both be better off in the long run.

It can be seen that this sort of model of others’ intentions, and their model of your intentions, captures features of reciprocity, trust, and reputation formation. Indeed maintaining cooperation is in everyone’s selfish interest in repeated games when the end of play is not in sight. It does, however, require players to be able to resist the short-term temptation to exploit this mutual reciprocity by the treachery of defection.

Of course, there is no reason why an internal representation of an other-agent’s belief model need stop at a knowing the representation of your intentions in their mind. At the next level, it could include your understanding that they know that you know that they know your intentions, and so on. That there are infinite levels of embedded beliefs that make any perfect decision-policy intractable, has inspired models of strategic behaviour that either bound the upper limit of reciprocal beliefs (an example of ‘bounded rationality’) (Camerer et al., 2004a ; Hampton et al., 2008 ), or estimate the level of reciprocal belief in their opponent directly (Yoshida et al., 2008 ).

Experimental evidence indicates that in repeated games with the same opponent, people reliably cooperate, as theory predicts. Critically, however, the theory predicts that people shouldn’t cooperate towards the end of repeated exchanges, when they play people that they will never meet again and who can’t communicate with others that can. The observation that people do cooperate in these situations suggests something is either incorrect about the goal-directed model, or as we suggest, other decision-making systems compete to bias behaviour.

Habitisation

In simple environments, habits allow you to navigate towards goals and avoid harm with speed and computational efficiency. Habits operate by allowing recently experienced rewards to reinforce actions that are statistically predictive of them. If an outcome is reliably predicted by an action, then the value of that action becomes high. The action set available to an individual at any one time is elicited by the configuration of cues and contexts in the environment, which represents the current ‘state’. Importantly, habits don’t themselves have access to any specific representation of their outcome, they merely know their value on an ordinal value scale.

Now consider action control in social games. Imagine you are playing a selfish but sophisticated opponent in endless rounds of the Prisoner’s dilemma. Early in the game, your model-based system has the ability to consider multiple future rounds of the game, in which mutual cooperation is evaluated as valuable, since you know your opponent also knows this. Accordingly, mutual cooperation is rewarded as the game dictates. After a few rounds, actions associated with ‘cooperate’ begin to reliably predict rewarding outcomes, and so the habit learning system, operating concurrently with goal-orientated systems, acquires greater predictive certainty. As this accrues, control is transferred to the habit system, and the computational cost of considering multiple future rounds is relieved. In simple terms, cooperation becomes more ‘automatic’.

The critical feature of this type of habit learning is what defines the state by which the habit can be elicited. In animal learning theory, this is termed the ‘discriminative stimulus’, and is typically experimentally determined by the presence of a cue (Mackintosh, 1983 ). However, the discriminative stimulus in social games is more complex, and in principle could be determined by the nature of the game being played (Prisoner’s dilemma, stag-hunt and so on) or by the identity of the opponent. Below, we consider both possibilities:

Imagine that you ignore the identity of your opponent, and by good fortune play the prisoners dilemma with multiple cooperative opponents: i.e. you exist within a population of sophisticated cooperators (Figure 2 A). Different types of social interaction will have distinct payoff matrices: some will benefit cooperation, others will not. If you know which game you are playing when you engage in an action, then if your action (e.g. to cooperate) is reliably rewarded it will be accessible to acquisition by a habit learning system that simply encodes that in a given game, cooperation or competition is reliably beneficial.

Figure 2. Habitual learning of Prisoner’s dilemma.(A) Habit learning in specific games. An agent plays an action a when in a particular state that is defined by the game type, e.g. game y1. If the outcome is rewarded, then the action is reinforced, and is more likely to be emitted when the same state is encountered again. (B) Habit learning with specific opponents. An agent (in green) plays action a (cooperate) when interacting with a particular agent (who defines the state, or discriminative stimulus SD as x1, for example). If the outcome is rewarding, then the reward reinforces action a, such that it’s value V(x1,a) increases, and is more likely to be chosen again in the same state in future.

Indeed even if the payoff matrix is not known, for instance in a novel game in an uncertain environment, a reasonable strategy may be to play by trial and error. This entails exploring different actions and seeing what the outcome is, in which case actions can be reinforced directly by habit systems. Simulation studies demonstrate how readily cooperative equilibria can be reached by simple associative algorithms (such as Q learning) without any model-based control at all (Littman, 1994 ; Claus and Boutilier, 1998 ; Hu and Wellman, 2004 ).

Alternatively, you may choose to ignore the payoff matrix of the game, but concentrate instead on the identity of your opponent (Figure 2 B). For instance, if you play a specific opponent in a variety of games, and she reliably cooperates with you to your benefit, then you may learn the habitual action to cooperate whenever you play her. In this way, she becomes a positive discriminative stimulus that evokes actions that engage pro-cooperatively with her.

The above mechanisms may acquire control of behaviour if several criteria are satisfied: the state and/or opponent are clearly discernable; the game (i.e. its payoff matrix) is relatively static (or changes slowly) allowing equilibria to be reached; and your internal preferences are stable. However, habit mechanisms are less reliable in the face of perceptual uncertainty, in which case an internal belief model of possible states may be required; if there are sudden changes in the environment that require rapid new learning, or a search for causal antecedents; or if your motivational state changes substantially (cooperation for food becomes less valuable when you are sated). Note that there is no evidence that habit systems ‘switch off’ in situations in which they behave poorly, rather their influence on control diminishes when their predictions become unreliable (Daw et al., 2005 ).

Although providing a plausible mechanism for social decision-making it turns out that, to date, evidence for habitised control of social behaviour is largely indirect. First, simple reinforcement learning algorithms do a remarkably good job at predicting behaviour in experiments across a variety of games (Erev and Roth, 1998 , 2007 ). Second, neuroimaging studies show opponent-specific value-related responses accruing according to opponents’ cooperativity/competitiveness in games (Singer et al., 2004 ). Third, neuroimaging studies have also identified dynamic reinforcement learning-like (prediction error) signals during games (King-Casas et al., 2005 ). Fourth, in single neuron recordings from non-human primates, lateral inter-parietal sulcus neurons in monkeys appear to encode value signals predicted by reinforcement learning in mixed-strategy games (Seo et al., 2009 ), which adds to previous observations that neurons in dorsolateral prefrontal and anterior cingulate cortex encode quantities related to choice and reinforcement history, respectively (Barraclough et al., 2004 ; Seo and Lee, 2008 ).

In reality, humans might be expected to habitise their actions in the context of state information that incorporates both opponent and game type. Although a diversity of subtly different payoff matrices may be common in experiments, it is likely that social interactions in different scenarios represent a relatively discrete set of payoff matrices. When there are small differences between different games, habit systems may generalise across salient features that have characteristic predictive power for beneficial outcomes.

Observational Learning

One especially important social scenario arises when a person interacts with others who are significantly more expert at social interaction. This can occur for a number of reasons: if the payoff matrix that defines the interaction is unknown to us but known to others – either through their experience or private information; because information about other players is known to them but not to us – again through either experience or their own vicariously acquired knowledge; of if they are more sophisticated – for instance they are more mature or intellectually able. In these situations, you have the choice to engage in interactions and acquire the information directly through your own experience or, better, to observe apparently successful social agents and vicariously acquire knowledge.

As long as success is discernable, as a hallmark of social expertise, then observational learning is likely to yield useful information. The computational problem becomes how to interpret the actions of others, and use observed actions to optimise your own. Computationally, inverse reinforcement learning describes this problem of how to reverse engineer observed actions to evaluate their values and goals, and is particularly difficult in situations in which actions do not immediately lead to their benefits. Unfortunately social interactions often display exactly this property: the benefits of cooperation are often long-term, through reputation formation and establishment of trust, and unless an observer has observational access to extended sequences of actions and their ultimate outcomes, the problem becomes even harder.

In general, there are two broad classes of solution. The first is simply to imitate others (Price and Boutilier, 2003 ). Imitation is the observational twin of habit learning, insofar as the resulting action has no specific representation of the outcome: it simply learns that a particular action is reliably performed in state s. The actions it bears are habit-like, elicited by a discriminative state that represents the environment in which they were learned. Accordingly, the ease of imitation depends on the discernability of the state of the observer. In Figure 3 A, we illustrate this for a situation in which the state is defined by the game type: as long as it is clear to the subject that they are playing, say Game y = Prisoners Dilemma, then the imitated action will be ‘cooperate when playing game y’. The imitated state-action pair could equally well be defined by the identity of the opponent. In this case, the resulting action will be ‘cooperate when playing opponent x’. Note that the values of the actions can also be inferred by the frequency with which they are elicited by observation, allowing imitation to encode action values, and not just stimulus-responses.

Figure 3. Observation learning of Prisoner’s dilemma. Observers learn the strategy from the observation of other players playing a game. (A) Imitation learning. An observer estimates the value of action a from other players’ actions and simply imitates an action which maximises the payoff in a particular environment, which can be defined by game or opponent (or both). Here we show an example in which the environment is ‘game = y’ and it does not take into account the opponent’s type (x) who they are playing with. (B) Inverse reinforcement learning. An observer estimates the players’ value from their actions, for example using subgoals. This means the observer assumes that the players using a model-based learning; i.e. they have a forward model of their opponents. For example, in a repeated Prisoner’s dilemma, cooperative actions (a1) will predict a state of the other players’ happiness (s1) which leads mutual cooperation in the future. The value of action a is calculated as the value of state (e.g. other player’s emotional state), V(s), multiplied by the probability of occurrence of the state followed by the action, p(s|a).

The second strategy is more complex, and involves trying to reverse engineer actions so as to evaluate their value or actual outcome (Ng and Russell, 2000 ). This requires constructing some sort of internal model of the action. For sequential actions, a computationally useful strategy is to represent subgoals – intermediate outcome states that appear to be reliable pre-requisites to eventual success (Abbeel and Ng, 2004 ). In the case of cooperative games, these subgoals ought to include the welfare of the other cooperators, since this is a powerful determinant of future cooperation. For example, in a repeated Prisoner’s dilemma, sophisticated cooperators will themselves predict reward when their opponents cooperate with them, since they have a forward model of future beneficial interactions. Assuming their reward-predicting state is discernable by observations of their emotional state s (their happiness), then this state becomes a statistically reliable subgoal. That is, it follows that the inference that eliciting the state of happiness in another player is a valid predictor of an agent’s success (Figure 3 B).

Although in the case of the agent being observed this is merely an intermediary state in ultimately selfish reciprocal interactions, this information (and its selfishness) is not available to the observer. Even so, it is still valuable knowledge as long as the observer is fortunate enough to use the information in situations in which it actually is beneficial: i.e. in repeated social exchanges. As long as repeated social exchanges outnumber un-repeated exchanges, then observational inference is likely to be a better strategy than ignoring others.

Observational learning in games, and especially putative inverse reinforcement learning, remains relatively under-explored. It is well known that humans use both model-free (imitative) and model-based (inverse-inference) strategies when learning non-social actions through observation (Heyes and Dawson, 1990 ). Recent imaging evidence shows that people learn values through instruction using similar neural mechanisms involved in personal experience based learning (Behrens et al., 2008 ), and make inferences about values by pure third-party observation (Klucharev et al., 2009 ). Furthermore, pro-social feelings towards others (empathic reward), and it’s neural representation, have been shown to be modulated by perceived similarity with that person (Mobbs et al., 2009 ), as one might predict from perspective-taking theories of social observation (Wolpert et al., 2003 ).

Discussion

We have argued that consideration of the neurobiological mechanisms of learning and decision-making in humans can yield an explanatory account of true altruism. At the heart of this account are the learning systems that allow the brain to optimise reward and efficiency in complex environments. Critically, since evolution is likely to operate primarily over learning and decision mechanisms, and not the content of those systems – how they learn, not what they learn, the ensuing altruistic behaviours are perfectly permissible, despite the fact that they may in some instances become strictly irrational. This is strengthened by the fact that habit-based and observational learning systems have uses way beyond social decision-making per se. The latter, for instance, is elegantly utilised in complex behaviours such as food preparation, tool use, and even language. Hence evolutionary selection for such mechanisms may be driven by a much broader range of decision-making problems than purely social interaction. Accordingly, such learning based accounts may offer both proximate and ultimate explanations for altruism.

The value of the inherent flexibility of learning systems is that it allows them to adapt to a wide range of potentially new and unexpected situations, appropriate for the diversity of the natural environment. But this flexibility carries the cost of inadvertently allowing individually economically disadvantageous actions to emerge, albeit rarely. However, we propose that on average these costs are heavily outweighed by benefits. Part of this supposition incorporates the fact that an innate representation of the caveats of flexible learning in social decision-making (for instance: don’t cooperate in one-shot, anonymous exchanges in large groups) is itself cripplingly complex and maladaptive to novelty (it itself becomes a form of impulsivity). In other words, any social decision-making system that attempted to capture the enormous range of possible encounters and interactions, and individually specify optimal policies, would impair rather than augment decision-making under uncertainty. As such, efficient learning based systems are likely to be selected in the course of evolution.

Learning based accounts differ from the conventional approach of studying cooperation in behavioural economics, which often considers static, heuristic decision-policies, such as ‘tit-for-tat’, ‘cooperate and punish’, and ‘free-ride’. Such models typically succumb to free-riders, including sophisticated (higher-order) free-riders that cooperate but don’t enforce or encourage cooperation in others. However, a valuable insight of these models has been the recognition that resistance to free-riders can be provided by acquisition (and defence) of cultural norms of behaviour (Boyd and Richerson, 1988 ; Boyd et al., 2003 ; Bowles and Gintis, 2004 ). Key underlying components of norm-abidance are likely to be observational learning and inference based mechanisms, since these form simple elements of cultural learning. The current paucity of biologically implemented algorithmic models and mechanisms of observational and cultural learning is therefore likely to be an important area of future research. In particular, the relative privacy of culturally acquired information within specific groups is likely to be an important factor in the development of parochialism, which may further allow group-based selection of altruistic behaviour (Bernhard et al., 2006 ; Choi and Bowles, 2007 ).

Learning based accounts do not negate innate mechanisms of altruism in the brain. Such mechanisms are thought to underlie many aspects of human impulsivity and irrationality, through their occasionally inflexible competition with instrumental actions (Dayan et al., 2006 ). If cooperation was so consistently advantageous through human social evolution, that it is quite possible there might be some innate coding. Indeed, the environment in which the social brain evolved is likely to have had a much higher proportion of repeated interactions with the same individuals than our modern environment in which cooperation can occasionally be economically disadvantageous. Innate actions can be thought of as action priors over and above which more sophisticated goal-directed instrumental actions can assume control as experience accrues. Their Achilles heel, however, is the fact that they appear often difficult to overcome (inhibit) completely: they have a residual and significant weight that consistently biases actions in their favour. If such innate coding of cooperation exists in the human brain, then it follows that altruism would be akin to more basic forms of impulsivity.

We note that control by innate systems is characterised by the intrinsic (typically ‘emotional’) value of a stimulus, as well as by the action it elicits. Accordingly, the states associated with putatively pro-social innate actions could include that following the act of sharing, generosity or generation of equity (Tomasello et al., 2005 ). In this way, they become intrinsic internal rewards that, phenomenologically, are elicited because they are personally satisfying (and akin to non-social innate behaviours such as novelty-seeking (Wittmann et al., 2008 )).

The complexity of different putative accounts of human altruism appeals to neuroscience as an arbitrator (Camerer et al., 2004b ). Distinguishing different decision systems purely on anatomical grounds may be difficult, however: brain regions such as the striatum, orbitofrontal cortex, amygdala and hippocampus for instance, appear to be convergence areas for all decision systems. For example the observation of activation of striatum in a study on altruistic punishment (de Quervain et al., 2004 ), whilst providing a convincing illustration of the fact that such behaviour has a clear proximate basis, says little about the nature of that behaviour in terms of whether it is innate or learned. This underlines the importance for brain imaging techniques that have the ability to distinguish between competing models based on identifying coding of their underlying central parameters (O’Doherty et al., 2007 ), in situations in which behaviour alone is necessarily ambiguous (Yoshida et al., 2008 ).

Both habit-based and observation-based accounts of pro-social behaviour make specific experimental predictions. First, if the identities of others can act as discriminative stimuli, then cooperation should carry over between different games with the same individual. Second, if game types can act as discriminative stimuli, then cooperation should carry over between the same game with different individuals. Third, the duration of play should predict the degree of unfolding of cooperation towards the end of repeated games, since extended durations permit stronger habit formation and less susceptibility to anticipatory defection. Fourth, the operation of associative learning mechanisms should be determinable by the use of co-incident cues associated with previous cooperative or uncooperative players, which ought to bias individuals behaviour in future games: in fact evidence already exists for this (Vlaev and Chater, 2006 ; Chater et al., 2008 ). Fifth, observational learning can be studied directly by allowing individuals to passively watch interactions between others before engaging in similar games, or different games with the observed opponents. Indeed evidence does exist that previous observation has an influence on future social behaviour, in that people do seem to be biased towards the behaviour of others. What is more difficult to establish is exactly how this information is represented: either as a cached imitated value, or as a model-based representation.

Finally, we note that learning based accounts of altruism are by no means immune to exploitation by selfish and intelligent learning agents. Any sophisticated model of other agents’ behaviour can incorporate the fact that they are habit and observational learners. Consequently, highly sophisticated models of other agents could in theory incorporate representations of their different decision systems: thus knowing that people are habit learners gives predictive insight into what is likely to guide their behaviour in various situations. Whereas determining this might not always be simple to an agent from passive observation, it might be in part revealed by probing: intentionally behaving in a certain way (such as maliciously cultivating pro-social cultures) to manipulate how values are acquired by others, so that they can be exploited later.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Abstract

Findings from twin studies yield heritability estimates of 0.50 for prosocial behaviours like empathy, cooperativeness and altruism. First molecular genetic studies underline the influence of polymorphisms located on genes coding for the receptors of the neuropeptides, oxytocin and vasopressin. However, the proportion of variance explained by these gene loci is rather low indicating that additional genetic variants must be involved. Pharmacological studies show that the dopaminergic system interacts with oxytocin and vasopressin. The present experimental study tests a dopaminergic candidate polymorphism for altruistic behaviour, the functional COMT Val158Met SNP. N  = 101 healthy Caucasian subjects participated in the study. Altruism was assessed by the amount of money donated to a poor child in a developing country, after having earned money by participating in two straining computer experiments. Construct validity of the experimental data was given: the highest correlation between the amount of donations and personality was observed for cooperativeness ( r  = 0.32, P  ≤ 0.001). Carriers of at least one Val allele donated about twice as much money as compared with those participants without a Val allele ( P  = 0.01). Cooperativeness and the Val allele of COMT additively explained 14.6% of the variance in donation behaviour. Results indicate that the Val allele representing strong catabolism of dopamine is related to altruism.

altruism, COMT Val158Met, dopamine, prosocial behaviour, genetics

INTRODUCTION

Social neuroscience is a rather new scientific discipline examining the biological basis of behaviour in social contexts. It mainly has its origins in social psychology and sociology, but instead of establishing algorithms valid for each individual on how behaviour is modulated by group dynamics and social contexts, social neuroscience tries to identify biological factors accounting for individual differences in social behaviour. The origin of all behaviour (including social behaviour) can be linked to cognitive, motivational and affective processes located in the brain. These processes are influenced by biological and environmental factors, which in turn interact with each other. Besides social cognition, interpersonal exchange and group interactions, prosocial behaviour––including empathy, cooperativeness and altruism––is a core research field in this area.

Altruism is defined as selfless concern for the welfare of others. However, there is a great debate in the literature if true altruism really exists ( Fehr and Fischbacher, 2003 ). Pure altruism is giving without regard to reward or the benefits of recognition and need. People who doubt the existence of pure altruism argue that helping others is intrinsically rewarding for altruistic persons and therefore they are exercising their personal interest to benefit their own selves rather than others. In other words, helping others makes them feel good. This line of argumentation overcomes the seemingly incompatibility with economic concepts like the homo economicus postulating that humans are selfish rational beings motivated through self-interest ( Ng and Tseng, 2008 ). However, it is widely acknowledged that there exist dramatic individual differences in the proclivity for altruistic behaviour. The crucial question arises if altruism represents a trait with a strong genetic impact or if it is a learned behaviour influenced by upbringing, education and other environmental factors like, e.g. religiosity. Findings from twin studies yield mean heritability estimates of about 0.50 for prosocial behaviours like empathy, cooperativeness and altruism indicating that nature and nurture have an equal impact on prosocial behaviour. These behavioural genetic studies mostly rely on self-report data: a twin study by Rushton et al . (1986) of 563 pairs of monozygous (MZ) and dizygous (DZ) twins, using an altruism and an emotional empathy scale, reported that 50% of the variance in altruism and empathy was due to genes and the other 50% to environmental factors. Noteworthy, the total environmental variance came from non-shared environmental sources and not from shared ones. Another study by Matthews et al . (1981) found 72% heritability for a self-report adjective checklist measure of empathy in 114 MZ and 116 DZ middle-aged male twins. In an additional twin study of 322 pairs of twins, Rushton (2004) replicated the strong genetic effects on prosocial behaviour. They found that heritability estimates of 0.40 for females and of 0.50 for males for social responsibility. In contrast to the study of 1986, shared environmental factors accounted for about 23% of the variance, whereas in the previous studies the environmental effects were exclusively due to non-shared environmental effects. Findings show that prosocial behaviours have a strong genetic influence and find support from a recent longitudinal study in 409 pairs of young twins that were investigated between 14 and 36 months of age ( Knafo et al ., 2008 ). Although, no genetic effects were observable at the age of 14 months, heritability estimates for empathy, which is a prerequisite for altruism, increased with the age. At the age of 24 and 36 months, genetics accounted for 34–47% of the variance in a global empathy factor. Shared environmental effects decreased from 0.69 at 14 months to 0.00 at 36 months, whereas non-shared environment accounted for 31–53% of the variance across ages. Even though these data were obtained in early infancy, the results are comparable with those of Rushton et al . (1986) based on the data of the adults.

There is also evidence for a genetic influence on reciprocating behaviour measured by trust and ultimatum games ( Wallace et al ., 2007 ; Cesarini et al ., 2008 ). The latter two studies stem from the field of neuroeconomics and made use of experimental instead of self-report data. The paradigms used have high ecological validity because participants’ choices were related to real monetary loss and gain. Heritability estimates for trust range between 10% and 20%, and >40% of subjects’ rejection behaviour in the ultimatum game (rejection of unfair offers in a bargain situation that ends in personal costs) is explained by additive genetic variance.

However, not all studies in the literature are supportive for the claim that prosocial behaviour is highly heritable. Krueger et al . (2001) reported no genetic effect at all for altruism in a study on 170 pairs of MZ and 106 pairs of DZ males, although Krueger applied only a slightly modified version of the Self-Report-Altruism Scale used in the study by Rushton et al . (1986) . Furthermore, Bouchard and Loehlin (2001) failed to find any evidence of genetic influence on self-assessed altruism. However in sum, the balance of evidence suggests a genetic effect on prosocial behaviours, especially on altruism.

Whereas quantitative genetics try to prove and estimate heritability of a given phenotype, molecular genetics, the second branch of behavioural genetics, is indebted to identify those genes that build the basis of heritability. Candidate genes for this endeavour stem from animal as well as human studies highlighting the prominent role of the nonapeptides, oxytocin and vasopressin for prosocial behaviours like attachment and pair bonding (for a review see Ebstein et al ., 2010 ; Insel, 2010 ). Prosocial behaviours include a broad class of phenotypes that include those sorts of behaviours that are characterized by a positive view on man, helping, trusting and caring. A prerequisite for prosocial behaviour to occur is the ability to have empathy. Due to the fact that genetic association studies on prosocial behaviours are scarce, we try to give examples of the first pioneer studies in this field. First genetic association studies have successfully linked polymorphisms of the oxytocin receptor gene (OXTR) and the vasopressin 1a receptor gene (AVPR1A) to prosocial behaviours ( Prichard et al ., 2007 ; Israel et al ., 2008 , 2009 ; Lerer et al ., 2008 ; Meyer-Lindenberg et al ., 2008 ; Levin et al ., 2009 ). However, the proportion of variance explained by these gene loci is rather low indicating the involvement of additional genetic variants in the expression of prosocial behaviour.

The dopaminergic system is another target for the investigation of the genetic basis of prosocial behaviours because dopamine has been related to parenting behaviour ( Lee et al ., 2008 ; van IJzendoorn et al ., 2008 ), affective modulation of emotional stimuli ( Montag et al ., 2008 ) and personality traits of positive emotionality ( Reuter and Hennig, 2005 ; Reuter et al ., 2006 ). There is also evidence that vasopressin interacts with dopamine in the genesis of prosocial behaviour: meadow voles characterized by promiscuity in contrast to the monogamous prairie voles, also show monogamous behaviour after injection of an AVPR1a vector into the pallidum. However, administration of a dopamine antagonist before the injection of the AVPR1a vector prevents this shift from promiscuous to monogamous behaviour in these animals ( Lim et al ., 2004 ). In the same line, facilitation of partner preference formation in voles by the activation of oxytocin receptors is not effective when dopamine D2 receptors are blocked ( Liu and Wang, 2003 ). Therefore, it is plausible that dopaminergic gene variants have also an influence on other prosocial behaviours besides pair bonding. In the context of the dopaminergic neurotransmission, especially the COMT Val158Met polymorphism is an interesting candidate polymorphism because this gene locus has turned out to be functional. Catechol- O -methyltransferase is an enzyme which plays a crucial role in the metabolism of catecholamines by inactivating them in the synaptic cleft, mostly in the prefrontal cortex. A single nucleotide polymorphism (SNP), a G→A transition in codon 158 of the COMT gene located at the q11 band of human chromosome 22 (rs4680), results in 3- to 4-fold reduction in COMT enzyme activity by coding for the synthesis of the amino acid methionine (MET) instead of valine (VAL). Carriers of the Val/Val genotype have highest, carriers of the Met/Met genotype lowest and heterozygotes (Val/Met genotype) have intermediate levels of COMT activity ( Lachman et al ., 1996 ).

The aim of the present study was to extend current knowledge of the molecular genetic basis of prosocial behaviours by investigating the potential role of the COMT Val158Met polymorphism for altruism. This was done in an experimental approach by studying human donation behaviour under conditions of high ecological validity.

METHODS

Participants

N  = 101 healthy Caucasian students of German origin with no present or former ICD-10 diagnosis of psychopathology (26 males: age: mean = 23.88, s.d. = 4.60; 74 females: age: mean = 22.42, s.d. = 4.56) studying at the University of Bonn, Germany, participated in the study.

Participants gave written consent and were debriefed after the study was completed. They were given the opportunity to get excluded from the study if desired. The study was approved by the ethics committee of the German Psychologist Association and was conducted in accordance to the ethical standards of the Declaration of Helsinki.

Personality assessment

Cloninger’s ‘Temperament and Character Inventory (TCI)’ was administered in order to assess personality ( Cloninger et al ., 1993 ). The TCI consists of 240 dichotomous variables and measures the four temperaments ‘novelty seeking’, ‘harm avoidance’, ‘reward dependence’ and ‘persistence’ and the three characters ‘cooperativeness’, ‘self-directedness’ and ‘self-transcendence’. The rationale for using trait measures of personality were as follows: due to the fact that most genetic studies on prosocial behaviour were based on self-report data, it was intended to obtain validation data for questionnaire data by means of our experimental measure of altruism. If the magnitude of donations represents altruism, it is expected that we also find positive correlations with the cooperativeness scale of the TCI (measuring prosocial behaviour) and should observe non-significant correlations to the other TCI personality dimensions.

Genetic analyses

DNA was extracted from buccal cells. Automated purification of genomic DNA was conducted by means of the MagNA Pure® LC system using a commercial extraction kit (MagNA Pure LC DNA isolation kit; Roche Diagnostics, Mannheim, Germany). Genotyping of the COMT Val158Met polymorphism (rs4680) was performed by real time PCR using fluorescence melting curve detection analysis by means of the Light Cycler System (Roche Diagnostics, Mannheim, Germany). By means of the melting curve analyses, SNPs can be detected without conducting gel electrophoresis or ensuing sequencing after amplification. The primers and hybridization probes (TIB MOLBIOL, Berlin, Germany) and the PCR protocol for rs4680 are as follows:

  • forward primer: 5′-GGGCCTACTGTGGCTACTCA-3′;

  • reverse primer: 5′-GGCCCTTTTTCCAGGTCTG-3′;

  • anchor hybridization probe: 5′-LCRed640-TGTGCATGCCTGACCCGTTGTCA-phosphate-3′ and

  • sensor hybridization probe: 5′-ATTTCGCTGGCATGAAGGACAAG -fluorescein-3′.

Further details of the PCR protocol are described elsewhere ( Reuter et al ., 2006 ).

Experimental data

The total study consisted of three parts: first, subjects were paid 5 € for participating in a working memory experiment (n-back task, Weinberger et al ., 1996 ). Next, they had the chance to increase their endowment in a gambling experiment (Iowa Gambling Task, IGT, Bechara et al ., 2000 ). Finally, in the third and essential part of the study, participants had the choice to either keep all their money for themselves or to donate the money in part or in total to a poor child in a developing country. Participants were shown a picture of a cute little girl, Lina from Peru, and a bracelet that was knitted by her. The stimulus material was taken from advertisement material of a charity organization. Donations were made optional and in pretended anonymity: After the study was completed, the experimenter announced the sum of the endowment to the participant and left him/her alone in the laboratory. The student could take the endowment from a money tray including 20 pieces of each possible Euro coin. The participant was free to give as much money as he/she wanted from his/her endowment into a piggy bank. The amount of money that was already in the savings box was known to the experimenter but participants were unaware of this. By that, the experimenter was able to reconstruct the amount of donated money after the participant had left the laboratory. The duration of the total study was about 30 min. After the completion of the study, we donated all the money to the charity organization from which we took the advertisement material.

The reason for conducting a demanding n-back task at the beginning was that participants should get the feeling that they had worked hard for their money, i.e. that they do not donate additional money that they got out of the blue. The additional administration of the IGT increased the variance in participants’ endowment and helped to answer the question if the amount of the participants’ endowment has an influence on the amount of their donations.

Statistical analyses

One-factorial ANOVA models were calculated to test the influence of the COMT Val158Met polymorphism on altruism. On the genotype levels the independent factor had three levels (Val/Val, Val/Met and Met/Met) and on the Val allele level there were two levels Val + (genotypes Val/Val and Val/Met) and Val (genotype Met/Met). Altruism as dependent variable was defined by the amount of money donated, first as raw data (amount of donated money) and second as the percentage of donated money, i.e. the percentage of each participant’s endowment that was donated to the little girl from a developing country. The later variable controls for differences in the endowment which are likely to influence the magnitude of the donation. Bivariate Pearson correlations between all personality variables and the two dependent variables ‘amount of money donated and percentage of money donated’ were calculated. In order to assess the cumulative predictive power of COMT Val158Met and personality, a hierarchical linear regression model with percentage of donated money as criterion was conducted.

RESULTS

Genotyping

The genotype frequencies of COMT Val158Met were as follows: Val/Val: n  = 24, Val/Met: n  = 49, Met/Met; n  = 28 and did not deviate from the Hardy–Weinberg equilibrium (χ 2  = 0.08, df = 1, n.s.). There were no differences in genotype distributions between both gender groups (χ 2  = 1.38, df = 2, P  = 0.501).

Altruism

The average endowment at the end of the experiment was 4.77 € (s.d. = 0.75). The three COMT Val158Met genotype groups did not differ significantly with respect to their endowment [ F (2,98) = 0.45, P  = 0.640] indicating no effect of the COMT SNP on the amount of money won in the Iowa Gambling task. However, results showed that the COMT Val158Met polymorphism was significantly related to the percentage of donated money [ F (2,98) = 4.18, P  = 0.018; see Figure 1 ] and showed a trend towards significance with respect to the total amount of donation [ F (2,98) = 2.84, P  = 0.063]. When analysing the results on the allele level by grouping subjects into Val + (genotypes Val/Val and Val/Met) and Val subjects (genotype Met/Met) it turned out that the effects became more robust [percentage of donated money: F (1,99) = 6.72, P  = 0.011; total amount of donation: F (1,99) = 4.96, P  = 0.028]. Carriers of the Val + group donated about half of their money (43%) for little Lina whereas the donation of the Val group (22%) was about half as high as in the Val + group. In order to illustrate this effect, the distribution of the percentage of donated money dependent on the allele group (Val and Val + ) was portrayed in Figure 2 . It becomes apparent that >20% of the Val + carriers donated their total endowment and that only a small percentage of Val carriers are located in the right half of the distribution (high donations). There was no effect of gender on donation amounts [percentage of donated money: F (1,99) = 2.53, P  = 0.115; total amount of donation: F (1,99) = 1.91, P  = 0.170].

Fig. 1

Percentage of participants’ endowment donated for a little girl in a developing country dependent on the COMT Val158Met polymorphism (rs4680). Results of the ANOVA: depicted are means and standard errors of means (s.e.m.)

Fig. 1

Percentage of participants’ endowment donated for a little girl in a developing country dependent on the COMT Val158Met polymorphism (rs4680). Results of the ANOVA: depicted are means and standard errors of means (s.e.m.)

Fig. 2

Frequency distribution of the percentage of participants’ endowment donated for a little girl in a developing country dependent on the Val allele of the COMT Val158Met polymorphism (rs4680).

Fig. 2

Frequency distribution of the percentage of participants’ endowment donated for a little girl in a developing country dependent on the Val allele of the COMT Val158Met polymorphism (rs4680).

Personality and altruism

None of the three temperaments of the TCI were significantly correlated with the percentage of donated money. However, the two character dimensions self-directedness and cooperativeness showed significant positive correlations ( r  = 0.22; P  = 0.028 and r  = 0.32; P  = 0.001, respectively) with donation behaviour. After Bonferroni correction for multiple testing only the correlation with cooperativeness remained significant.

Prediction of altruism by personality and COMT Val158Met

In order to test if the two predictors, cooperativeness and COMT Val158Met, explain additive or shared proportions of variance in donation behaviour a hierarchical multiple regression model was calculated. In the first block of the regression model the Val allele was added. The gene locus explained 5.8% of the variance in donation behaviour ( F  = 5.93, P  = 0.017). In a second block, the personality variable cooperativeness was added increasing the explained variance significantly by 8.9% (total R2  = 0.147; change in F  = 9.98, P  = 0.002). Adding the interaction term Val allele by cooperativeness in a third block into the regression model did not increase the explained variance significantly (incremental explained variance 0.06 %; F  = 0.69, P  = 0.410). It has to be mentioned that the COMT Val158Met SNP was not related to cooperativeness [ F (2,98) = 0.16, P  = 0.851).

Controlling for confounding variables

The performance in the n-back task was on no level correlated with donation behaviour (1-back: r  = 0.135, P  = 0.182; 2-back: r  = 0.151, P  = 0.135; 3-back: r  = 0.179, P  = 0.074; 4-back: r  = 169, P  = 0.093; total n-back performance: r  = 0.187, P  = 0.062). Although the association between executive control function (n-back) and altruism is only a small trend, the direction of the trend is plausible: Val + carriers show more altruism and many studies have shown that Val allele carriers exhibit better working memory performance ( Weinberger et al ., 1996 ). Therefore, the positive relation between altruism and n-back performance seems to be moderated by the Val allele.

Also the correlation between the net-score in the IGT was not significantly correlated with altruism ( r  = 0.164, P  = 0.101). There were also no significant effects of genotype or gender on IGT net-score or the performance in the n-back task (all P -values in the ANOVAs  > 0.4).

DISCUSSION

Prosocial behaviour is one of the prerequisites for the growth and prosperity of societies and is observable in many species besides primates ( Zak and Knack, 2001 ). Evolutionary theories have been shown to be useful to explain non-selfish behaviours by introducing the terms ‘inclusive fitness’ and ‘reciprocal altruism’ ( Hamilton, 1964 ; Trivers, 1971 ). It is known that there is great variability between and within societies in prosocial behaviour ( Henrich et al ., 2005 ). Especially, the latter one has been of scientific interest in humans because shared cultural background variables like norms and ethics of a given society cannot be the reason for such variability. Twin studies have disentangled genetic and environmental influences on prosocial behaviours indicating that ∼50% of the variance in altruism can be accounted by genetic effects ( Rushton et al ., 1986 ; Rushton, 2004 ). However, these heritability estimates were based on self-report data. The ecological validity of self-report data in science has often been questioned ( Brewer, 2000 ). Experimental settings, where decision making has direct costs or benefits for the participants are likely to be superior in this respect. Neuroeconomics often makes use of monetary rewards to increase the ecological validity of human decision making, because money is the most potent generalized secondary reinforcer available. Despite the ongoing debate on how social decision making and altruism as a specific form of prosocial behaviour is assessed adequately, there are no studies available investigating the molecular genetic basis of altruism (although molecular genetic studies on prosocial behaviour assessed by economic games are reported in the literature).

Therefore, the aim of the present study was to identify those gene loci that contribute to the heritability of altruism. Starting point were existing studies that demonstrated the influence of polymorphisms of the OXTR and the AVPR1A on social behaviours ( Prichard et al ., 2007 ; Israel et al ., 2008 , 2009 ; Lerer et al ., 2008 ; Meyer-Lindenberg et al ., 2008 ; Levin et al ., 2009 ). As known from other traits, many genes, additively or in interaction, contribute to the expression of complex phenotypes. Pharmacological studies have shown that the dopaminergic system interacts with the ‘prosocial’ hormones oxytocin and vasopressin (for a review see Skuse and Gallagher, 2008 ; Moos and Richard, 1982 ). The striatum is involved in reward-related learning ( Delgado, 2007 ) and both ventral and dorsal striatum contain vasopressin and oxytocin receptors, in addition to DA receptors. Oxytocin interacts with dopaminergic circuits in the nucleus accumbens shell (NAS) and in the ventral tegmental area (VTA). Most prominent evidence for the interplay of dopamine with the neuropeptides oxytocin and vasopressin comes from animal studies showing that administration of dopamine antagonists can influence pair-bond formation in voles that was beforehand influenced by centrally acting genetic neuropeptide vectors ( Liu and Wang, 2003 ; Lim et al ., 2004 ). Also, in studies in humans, a neural network has been identified underlying social behaviour including social cognition. The normal functioning of that network engages the neuropeptides oxytocin and vasopressin with activity of dopaminergic receptors in the striatum and the orbitofrontal cortex ( Kringelbach, 2005 ; Delgado, 2007 ). For example, oxytocin promotes interpersonal trust by inhibiting defensive behaviours and by linking this inhibition with the activation of dopaminergic reward circuits, enhancing the value of social encounters ( Campbell, 2008 ).

Given this interaction between neuropeptides and dopamine it is not surprising that also polymorphisms related to the dopaminergic system, especially the COMT Val158Met SNP, have been demonstrated to be related to prosocial behaviour like extraversion and positive emotionality ( Reuter and Hennig, 2005 ; Reuter et al. , 2006 ).

By means of an experimental approach human donation behaviour was assessed as a proxy for altruism. Participants who had previously worked hard for a monetary reward could decide to donate money for a poor little child in a developing country or to keep the endowment for themselves. It turned out that individual differences in altruism could be explained by the COMT Val158Met SNP. Carriers of at least one Val allele (Val + group) donated about twice as much money than those who were homozygous for the Met allele (Val group). This finding is in line with previous studies relating the Met allele to negative emotionality ( Goldman et al ., 2005 ; Reuter and Hennig, 2005 ). Persons with habitually more negative affect (Met allele carriers or worriers in terms of Goldman’s ‘warrior/worrier’ model) are putatively less likely to show prosocial behaviour because of being too much occupied with their own problems.

External validity for the experimental paradigm assessing altruism comes from self-report personality questionnaire data measuring the basic temperament and character dimensions of the TCI. Cooperativeness was the only personality trait that showed substantial correlations to donation behaviour. Most interestingly, both predictors, the Val allele of COMT Val158Met and cooperativeness, could explain together ∼15% of the variance in the percentage of donated money.

Unfortunately the study did not test for interaction effects between COMT Val158Met and polymorphisms on the OXTR and AVPR1a receptors. In this first attempt, we deliberately did not test multiple SNPs together to warrant the theory driven approach of the study. Testing multiple gene loci simultaneously harbours the risk of multiple testing and would give the study an exploratory approach. Furthermore, an even larger sample size is needed to test for such an epistasis effect. However, after successful replication of the present findings the interaction of COMT Val158Met and polymorphisms on the ‘prosocial’ genes OXTR and AVPR1a has to be tested. Further future directions in altruism research are the investigation of the interaction of the dopaminergic system and the nonapeptides oxytocin and vasopressin by means of fMRI or pharmacological challenge tests.

A further shortcoming of the study is that we did not control for the economic background of our participants. Although the variance in the financial situation of students is rather low it cannot be excluded that this might be a confounding influence on donation behaviour. However, this would imply that the financial background of the participants would also co-vary with COMT Val158Met.

It has to be pointed out that the nature of the study is explorative. Normally sample sizes in case–control studies are much larger. However, experimental studies investigating so called endophenotypes of broader traits tend to have more power and therefore could rely on smaller sample sizes. But this argument does not argue against the need for an independent replication study.

In sum, the present study demonstrates that the dopaminergic system influences altruism in an ecological valid experimental paradigm.

Conflict of Interest

None declared.

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