The neural correlates of reciprocity are sensitive to prior experience of reciprocity

Highlights

• Non-reciprocity was associated with precentral gyrus and culmen activation.

• Altruism was associated with lingual gyrus activation.

• Reciprocity was associated with activity in distinct neural networks.

Abstract

Reciprocity is central to human relationships and is strongly influenced by multiple factors including the nature of social exchanges and their attendant emotional reactions. Despite recent advances in the field, the neural processes involved in this modulation of reciprocal behavior by ongoing social interaction are poorly understood. We hypothesized that activity within a discrete set of neural networks including a putative moral cognitive neural network is associated with reciprocity behavior. Nineteen healthy adults underwent functional magnetic resonance imaging scanning while playing the trustee role in the Trust Game. Personality traits and moral development were assessed. Independent component analysis was used to identify task-related functional brain networks and assess their relationship to behavior. The saliency network (insula and anterior cingulate) was positively correlated with reciprocity behavior. A consistent array of brain regions supports the engagement of emotional, self-referential and planning processes during social reciprocity behavior.

Introduction

Social reciprocity, defined as behavioral response to a positive action with another positive action, is central to an individual’s development of healthy interpersonal relationships, learning of social norms and normative ethics, and integration into society [1]. Reciprocity and other prosocial behaviors, such as altruism, fairness, and cooperation, are adaptive behaviors common to many cultures and religious traditions. Human subjects engage in prosocial behaviors even at their own expense [2], and thus reciprocity can overlap with altruistic behavior. However, reciprocity and other prosocial behaviors are multi-determined and dissociable products of complex and dynamic transactional processes [3]. For instance, reciprocity can be seen as self-serving, whether by promoting the benefit of future reciprocity, increasing one’s social status or reputation, resolving the conflict of seeing somebody else suffer, enabling redemption or release from guilt, or even by increasing reproductive population fitness [2], [4], [5], [6], [7].

The pervasive human distinction between “us” and “others” is traditionally based on kinships but tends to be determined by social proximity and contact. Personal interaction with others makes decision making less utilitarian and more emotionally driven [8]. For example, when research subjects believe they are interacting with other humans (rather than computers) neuroimaging has shown greater engagement of the ventral striatum and ventromedial prefrontal cortex (VMPFC), brain regions that are both associated with reward processing [9], [10]. However, the neural processes underlying the modulating effects of social interaction, either positive or negative, on basic reciprocal behavior are largely unknown.

Monetary exchange paradigms have yielded valuable insight into the neurobiology of cooperation [11], trust [12], [13], and agency [14]. In the present study, we sought to further characterize the neural mechanisms underlying individual variation in reciprocity behavior during a monetary decision making task, the Trust Game. Variations in task conditions allowed to assess the behavioral and neural processing correlates of reciprocating a gift before and after a social exchange in which a gift to another was or was not reciprocated. We hypothesized that reciprocity correlates with the engagement of neural processing networks including a putative moral cognitive neural network composed of the frontal pole, anterior cingulate cortex (ACC), superior temporal cortex (STS), precuneus, and posterior cingulate cortex (PCC) [15], [16], [17].