Neural responses are typically characterized by computing the mean firing rate. Yet response variability can exist across trials. Many studies have examined the impact of a stimulus on the mean response, yet few have examined the impact on response variability. We measured neural variability in 13 extracellularly-recorded datasets and one intracellularly-recorded dataset from 7 areas spanning the four cortical lobes. In every case, stimulus onset caused a decline in neural variability. This occurred even when the stimulus produced little change in mean firing rate. The variability decline was observable in membrane potential recordings, in the spiking of individual neurons, and in correlated spiking variability measured with implanted 96-electrode arrays. The variability decline was observed for all stimuli tested, regardless of whether the animal was awake, behaving, or anaesthetized. This widespread variability decline suggests a rather general property of cortex: that its state is stabilized by an input.

The anterior cingulate cortex (ACC) is implicated in a broad range of behaviors and cognitive processes, but it has been unclear what contribution, if any, the ACC makes to social behavior. We argue that anatomical and functional evidence suggests that a specific sub-region of ACC—in the gyrus (ACCg)—plays a crucial role in processing social information. We propose that the computational properties of the ACCg support a contribution to social cognition by estimating how motivated other individuals are and dynamically updating those estimates when further evidence suggests they have been erroneous. Notably this model, based on vicarious motivation and error processing, provides a unified account of neurophysiological and neuroimaging evidence that the ACCg is sensitive to costs, benefits, and errors during social interactions. Furthermore, it makes specific, testable predictions about a key mechanism that may underpin variability in socio-cognitive abilities in health and disease.

Social decisions play a crucial role in the success of individuals and the groups they compose. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders like autism and sociopathy. We studied how neurons in three frontal cortical areas encode the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, reward allocations to oneself, or both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or no one. Within this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerges as a key nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.

People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms. O xytocin (OT) (1) is a mammalian neurosecretory hormone, synthesized by hypothalamic neurons, which regulates the hypothalamic-pituitary-adrenal axis (2). The most well-understood role of OT in mammals is in female reproduction, with peripheral OT influencing parturition and lactation (3), and central OT affecting mother-offspring bonding and recognition (4, 5). More recently, OT has been found to influence nonparental social behavior in a species-specific manner. For example, OT promotes pair-bonding between males and females in monogamous prairie voles (Microtus ochrogaster) (6, 7) but can also increase aggression (i.e., mate-guarding behavior) and decrease social interaction among females after brief exposure to a male (8). In humans, OT also influences more complex forms of social behavior and cognition (9-14). For example, inhaled OT enhances trusting behavior toward other individuals in economic games, potentially by suppressing aversion to betrayal risk (15), and promotes cooperation within groups (16). However, inhaled OT also provokes cultural and racial biases (17). OT inhalation also enhances sensitivity to the experiences of others by promoting vicarious reward and empathic pain (10,18,19). Recently, OT-mediated processes have been implicated in disorders attended by dysfunctional social behavior, including autism, fragile X syndrome, and schizophrenia (19)(20)(21)(22). Notably, OT treatment improves social skills in individuals with autism (21, 23, 24), a spectrum of disorders with marked deficits in sensitivity to what happens to others, including impai...