Humans and other animals pay attention to other members of their groups to acquire valuable social information about them, including information about their identity, dominance, fertility, emotions, and likely intent. In primates, attention to other group members and the objects of their attention is mediated by neural circuits that transduce sensory information about others and translate that information into value signals that bias orienting. This process likely proceeds via two distinct but integrated pathways: an ancestral, subcortical route that mediates crude but fast orienting to animate objects and faces; and a more derived route involving cortical orienting circuits that mediate nuanced and context-dependent social attention.

Macaques, like humans, rapidly orient their attention in the direction other individuals are looking. Both cortical and subcortical pathways have been proposed as neural mediators of social gaze following, but neither pathway has been characterized electrophysiologically in behaving animals. To address this gap, we recorded the activity of single neurons in the lateral intraparietal area (LIP) of rhesus macaques to determine whether and how this area might contribute to gaze following. A subset of LIP neurons mirrored observed attention by firing both when the subject looked in the preferred direction of the neuron, and when observed monkeys looked in the preferred direction of the neuron, despite the irrelevance of the monkey images to the task. Importantly, the timing of these modulations matched the time course of gaze-following behavior. A second population of neurons was suppressed by social gaze cues, possibly subserving task demands by maintaining fixation on the observed face. These observations suggest that LIP contributes to sharing of observed attention and link mirror representations in parietal cortex to a well studied imitative behavior.gaze following ͉ imitation ͉ joint attention ͉ mirror neurons ͉ shared attention P eople naturally and intuitively share attention with each other. In a laboratory setting, people respond more quickly to targets that are the object of another's attention, even when this social cuing is brief or consistently misleading (1-3). Monkeys' attention also follows the gaze of others (4), and the similar magnitude and time course of gaze following by rhesus macaques and humans (5) implicates shared neural mechanisms. The ability to follow gaze is believed to be an important foundation for theory of mind (6, 7); thus, the neural processes governing gaze following are relevant both to the evolution of social cognition (8-10) and to clinical disorders, such as autism, associated with social attention deficits (11)(12)(13)(14). Although gaze following involves automatic ''mirroring'' of other's mental states, to our knowledge, mirror neurons (15, 16) for visual orienting have not previously been identified.Current evidence suggests that identification of where other individuals are looking is accomplished by neurons along the superior temporal sulcus (STS) (17)(18)(19)(20) (22), as well as the parietal cortex (28). These observations invite the simple hypothesis that gazefollowing behavior is mediated by a relatively straightforward system, beginning with the STS and proceeding directly to the attention-and gaze-control networks. Although intuitively appealing, this model raises several important questions.First, gaze-following behavior fits poorly into existing models of attention (1, 2), which dichotomize the underlying mechanism as either reflexively driven by exogenous stimuli or endogenously guided by internal goals (29, 30). Although there is some evidence that specific neural circuits mediate these processes (31-33), the precise contributions of neurons within different b...

A neuroethological approach to human and nonhuman primate behavior and cognition predicts biological specializations for social life. Evidence reviewed here indicates that ancestral mechanisms are often duplicated, repurposed, and differentially regulated to support social behavior. Focusing on recent research from nonhuman primates, we describe how the primate brain might implement social functions by coopting and extending preexisting mechanisms that previously supported nonsocial functions. This approach reveals that highly specialized mechanisms have evolved to decipher the immediate social context, and parallel circuits have evolved to translate social perceptual signals and nonsocial perceptual signals into partially integrated social and nonsocial motivational signals, which together inform general-purpose mechanisms that command behavior. Differences in social behavior between species, as well as between individuals within a species, result in part from neuromodulatory regulation of these neural circuits, which itself appears to be under partial genetic control. Ultimately, intraspecific variation in social behavior has differential fitness consequences, providing fundamental building blocks of natural selection. Our review suggests that the neuroethological approach to primate behavior may provide unique insights into human psychopathology.decision | evolution | reward | serotonin | oxytocin S ensitivity and responsiveness to information about others is critical for human health (1, 2), survival (3), and even financial success (4). To navigate our social worlds, we track the behavior of others and form models of their intentions and emotional states, we actively seek out and exchange information about others, and we flexibly alter our behavior in response to what we know about others. These faculties are so important to human behavior that their disruption constitutes psychopathology (5, 6). These specializations for social behavior reflect a rich evolutionary heritage of adaptation to group life (7-9). Like humans, many nonhuman primates also live in large groups characterized by patterns of social behaviors like grooming, imitative and cooperative foraging, differentiated affiliative relationships, ritualized courtship and mating behavior, and competitive interactions structured by social dominance (10, 11). Not surprisingly, the ability to deftly navigate the social environment has observable consequences for reproductive success in some nonhuman primates (12). Evolutionary Perspective on Social BehaviorSocial behavior places strong and unique demands on the nervous system. Across primate species, group size (a potential proxy of social complexity) is correlated with forebrain volume, after correcting for body size (9). Additional brain tissue beyond that required to maintain a body of a particular size is costly, in both developmental complexity and metabolic demands (7, 13-15). Indeed, social complexity and the elaboration of neural mechanisms to support it are associated with diets high in dependa...

Animals as diverse as arthropods [1], fish [2], reptiles [3], birds [4], and mammals, including primates [5], depend on visually acquired information about conspecifics for survival and reproduction. For example, mate localization often relies on vision [6], and visual cues frequently advertise sexual receptivity or phenotypic quality [5]. Moreover, recognizing previously encountered competitors or individuals with preestablished territories [7] or dominance status [1, 5] can eliminate the need for confrontation and the associated energetic expense and risk for injury. Furthermore, primates, including humans, tend to look toward conspecifics and objects of their attention [8, 9], and male monkeys will forego juice rewards to view images of high-ranking males and female genitalia [10]. Despite these observations, we know little about how the brain evaluates social information or uses this appraisal to guide behavior. Here, we show that neurons in the primate lateral intraparietal area (LIP), a cortical area previously linked to attention and saccade planning [11, 12], signal the value of social information when this assessment influences orienting decisions. In contrast, social expectations had no impact on LIP neuron activity when monkeys were not required to make a choice. These results demonstrate for the first time that parietal cortex carries abstract, modality-independent target value signals that inform the choice of where to look.

The development of alcoholism may involve a shift from goal-directed to habitual drinking. These action control systems are distinct in the dorsal striatum, with the dorsomedial striatum (DMS) important for goal-directed behavior and the dorsolateral striatum (DLS) required for habit formation. Goal-directed behavior can be modeled in rats with a fixed ratio (FR) reinforcement schedule, while a variable interval (VI) schedule promotes habitual behavior (e.g., insensitivity to contingency degradation). Using extracellular recordings from chronically implanted electrodes, we investigated how DMS and DLS neurons encoded lever-press responses and conditioned cues during operant alcohol self-administration in these two models. In rats self-administering 10% alcohol on a FR schedule, the DMS neuronal population showed increased firing at the onset of start-of-session stimuli. During self-administration, the most prominent phasic firing patterns in the DMS occurred at the time of reinforcement and reinforcement-associated cues, while the most prominent phasic activity in the DLS surrounded the lever response. Neural recordings from an additional cohort of rats trained on a VI schedule revealed a similar pattern of results; however, phasic changes in firing were smaller and differences between the medial and lateral dorsal striatum were less marked. In summary, the DMS and DLS exhibited overlapping but specialized phasic firing patterns: DMS excitations were typically time-locked to reinforcement, while DLS excitations were generally associated with lever responses. Furthermore, the regional specificities and magnitudes of phasic firing differed between reinforcement schedules, which may reflect differences in behavioral flexibility, reward expectancy and the action sequences required to procure reinforcement.

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As studies of the neural circuits underlying choice expand to include more complicated behaviors, analysis of behaviors elicited in laboratory paradigms has grown increasingly difficult. Social behaviors present a particular challenge, since inter- and intra-individual variation are expected to play key roles. However, due to limitations on data collection, studies must often choose between pooling data across all subjects or using individual subjects' data in isolation. Hierarchical models mediate between these two extremes by modeling individual subjects as drawn from a population distribution, allowing the population at large to serve as prior information about individuals' behavior. Here, we apply this method to data collected across multiple experimental sessions from a set of rhesus macaques performing a social information valuation task. We show that, while the values of social images vary markedly between individuals and between experimental sessions for the same individual, individuals also differentially value particular categories of social images. Furthermore, we demonstrate covariance between values for image categories within individuals and find evidence suggesting that magnitudes of stimulus values tend to diminish over time.