Social hierarchies guide behavior in many species, including humans, where status also has an enormous impact on motivation and health. However, little is known about the underlying neural representation of social hierarchies in humans. In the present study, we identify dissociable neural responses to perceived social rank using functional magnetic resonance imaging (fMRI) in an interactive, simulated social context. In both stable and unstable social hierarchies, viewing a superior individual differentially engaged perceptual-attentional, saliency, and cognitive systems, notably dorsolateral prefrontal cortex. In the unstable hierarchy setting, additional regions related to emotional processing (amygdala), social cognition (medial prefrontal cortex), and behavioral readiness were recruited. Furthermore, social hierarchical consequences of performance were neurally dissociable and of comparable salience to monetary reward, providing a neural basis for the high motivational value of status. Our results identify neural mechanisms that may mediate the enormous influence of social status on human behavior and health.

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The mesolimbic dopaminergic system has long been known to be involved in the processing of rewarding stimuli, although recent evidence from animal research has suggested a more specific role of signaling errors in the prediction of rewards. We tested this hypothesis in humans, using functional magnetic resonance imaging (fMRI) and an operant conditioning paradigm for the discrete delivery of small quantities of fruit juice, along with a control experiment in which juice was substituted with a neutral visual stimulus. A local estimation of the activity in the ventral striatum showed a significant differentiation when the juice was withheld at the expected time of delivery; this finding was not replicated in the case of visual stimulation, providing evidence for time-locked processing of reward prediction errors in human ventral striatum.

While the striatum has been implicated in reward processing, an alternative view contends that the striatum processes salient events in general. Using fMRI, we investigated human striatal responses to monetary reward while modulating the saliency surrounding its receipt. Money was maximally salient when its receipt depended on a correct response (active) and minimally salient when its receipt was completely independent of the task (passive). The saliency manipulation was confirmed by skin conductance responses and subjective ratings of the stimuli. Significant caudate and nucleus accumbens activations occurred following the active compared to passive money. Such activations were attributed to saliency rather than the motor requirement associated with the active money because striatal activations were not observed when the money was replaced by inconsequential, nonrewarding stimuli. The present study provides evidence that the striatum's role in reward processing is dependent on the saliency associated with reward, rather than value or hedonic feelings.

Given the choice of waiting for an adverse outcome or getting it over with quickly, many people choose the latter. Theoretical models of decision-making have assumed that this occurs because there is a cost to waiting-i.e., dread. Using functional magnetic resonance imaging, we measured the neural responses to waiting for a cutaneous electric shock. Some individuals dreaded the outcome so much that, when given a choice, they preferred to receive more voltage rather than wait. Even when no decision was required, these extreme dreaders were distinguishable from those who dreaded mildly by the rate of increase of neural activity in the posterior elements of the cortical pain matrix. This suggests that dread derives, in part, from the attention devoted to the expected physical response and not simply from fear or anxiety. Although these differences were observed during a passive waiting procedure, they correlated with individual behavior in a subsequent choice paradigm, providing evidence for a neurobiological link between the experienced disutility of dread and subsequent decisions about unpleasant outcomes.Making decisions about gains and losses is one of the archetypal problems that all animals face, but when the outcome is temporally delayed from the decision, the problem becomes considerably more complex than simply choosing the course of action with the better expected outcome. Standard economic theory posits that preferences for outcomes that occur at different times can be represented by an expected utility of the future outcomes discounted by the amount of time one must wait for them (1). These theories typically apply discounting under the assumption that people care less about outcomes that are more remote in the future than those that are more imminent, which leads to the prediction that people should want to expedite desired experiences and delay undesirable experiences for as long as possible. A wide range of findings, however, shows that people often exhibit the opposite pattern: They prefer to delay gratifications and to speed up the occurrence of unpleasant outcomes. If people do, indeed, discount the future, then why do they so often exhibit patterns of preference that are the opposite of the predictions of time discounting? The answer, we suggest, lies in the fact that the act of waiting may itself bring subjective benefits or costs, such as the joyous anticipation of waiting for a birthday present or the misery of waiting for a dentist's appointment. In the case of bad outcomes, the problem can be reduced to the utility of dread (2).In contrast to standard discounted utility theory, another type of decision-making model posits that waiting enters the utility function separately from the outcome (3, 4). Here, an individual's preference for waiting at any point in time reflects the relative weight of two considerations:

Although one proposed function of both the striatum and its major dopamine inputs is related to coding rewards and reward-related stimuli, an alternative view suggests a more general role of the striatum in processing salient events, regardless of their reward value. Here we define saliency as an event that both is unexpected and elicits an attentional-behavioral switch (i.e., arousing). In the present study, human striatal responses to nonrewarding salient stimuli were investigated. Using functional magnetic resonance imaging (fMRI), the blood oxygenation level-dependent signal was measured in response to flickering visual distractors presented in the background of an ongoing task. Distractor salience was manipulated by altering the frequency of distractor occurrence. Infrequently presented distractors were considered more salient than frequently presented distractors. We also investigated whether behavioral relevance of the distractors was a necessary component of saliency for eliciting striatal responses. In the first experiment (19 subjects), the distractors were made behaviorally relevant by defining a subset of them as targets requiring a button press. In the second experiment (17 subjects), the distractors were not behaviorally relevant (i.e., they did not require any response). The fMRI results revealed increased activation in the nucleus accumbens after infrequent (high salience) relative to frequent (low salience) presentation of distractors in both experiments. Caudate activity increased only when the distractors were behaviorally relevant. These results demonstrate a role of the striatum in coding nonrewarding salient events. In addition, a functional subdivision of the striatum according to the behavioral relevance of the stimuli is suggested.

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The neuropeptides oxytocin and vasopressin have increasingly been identified as modulators of human social behaviors and associated with neuropsychiatric disorders characterized by social dysfunction, such as autism. Identifying the human brain regions that are impacted by oxytocin and vasopressin in a social context is essential to fully characterize the role of oxytocin and vasopressin in complex human social cognition. Advances in human non-invasive neuroimaging techniques and genetics have enabled scientists to begin to elucidate the neurobiological basis of the influence of oxytocin and vasopressin on human social behaviors. Here we review the findings to-date from investigations of the acute and chronic effects of oxytocin and vasopressin on neural activity underlying social cognitive processes using “pharmacological fMRI” and “imaging genetics”, respectively.