Individual differences in social information gathering revealed through Bayesian hierarchical models.

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.

Dorsomedial and dorsolateral striatum exhibit distinct phasic neuronal activity during alcohol self-administration in rats.

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 an 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.

Neuroethology of primate social behavior.

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.

Social information signaling by neurons in primate striatum.

Social decisions depend on reliable information about others. Consequently, social primates are motivated to acquire information about the identity, social status, and reproductive quality of others. Neurophysiological and neuroimaging studies implicate the striatum in the motivational control of behavior. Neuroimaging studies specifically implicate the ventromedial striatum in signaling motivational aspects of social interaction. Despite this evidence, precisely how striatal neurons encode social information remains unknown. Therefore, we probed the activity of single striatal neurons in monkeys choosing between visual social information at the potential expense of fluid reward. We show for the first time that a population of neurons located primarily in medial striatum selectively signals social information. Surprisingly, representation of social information was unrelated to simultaneously expressed social preferences. A largely nonoverlapping population of neurons that was not restricted to the medial striatum signaled information about fluid reward. Our findings demonstrate that information about social context and nutritive reward are maintained largely independently in striatum, even when both influence decisions to execute a single action.

Social attention and the brain.

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.

Mirroring of attention by neurons in macaque parietal cortex.

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.

Neural correlates of social target value in macaque parietal cortex.

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.