No abstract

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...

We have evaluated the role of the Drosophila mushroom bodies (MBs) in courtship conditioning, in which experience with mated females causes males to reduce their courtship toward virgins (Siegel and Hall, 1979). Whereas previous studies indicated that MB ablation abolished learning in an olfactory conditioning paradigm (deBelle and Heisenberg, 1994), MB-ablated males were able to learn in the courtship paradigm. They resumed courting at naive levels within 30 min after training, however, while the courtship of control males remained depressed 1 hr after training. We also describe a novel courtship conditioning paradigm that established long-term memory, lasting 9 days. In MB-ablated males, memory dissipated completely within 1 day. Our results indicate that the MBs are not required for learning and immediate recall of courtship conditioning but are required for consolidation of short-term and long-term associative memories.

Neuroeconomics applies models from economics and psychology to inform neurobiological studies of choice. This approach has revealed neural signatures of concepts like value, risk, and ambiguity, which are known to influence decision-making. Such observations have led theorists to hypothesize a single, unified decision process that mediates choice behavior via a common neural currency for outcomes like food, money, or social praise. In parallel, recent neuroethological studies of decision-making have focused on natural behaviors like foraging, mate choice, and social interactions. These decisions strongly impact evolutionary fitness and thus are likely to have played a key role in shaping the neural circuits that mediate decision-making. This approach has revealed a suite of computational motifs that appear to be shared across a wide variety of organisms. We argue that the existence of deep homologies in the neural circuits mediating choice may have profound implications for understanding human decision-making in health and disease.