(Project 4, Gothard) Despite the great diversity of species-specific social behaviors, many of the fundamental building blocks of social behavior are shared across species. For example, correct identification of individuals allows animals to learn the unique rewards or adverse outcomes expected from interacting with different individuals. The sensory modalities involved in discriminating between individuals may be different across species, but the neural mechanisms of social discrimination may be shared. Oxytocin (OT) emerged recently as a universal factor that governs social behaviors in multiple mammalian species. In this project, we explore the role of OT in shaping basic neural processes during social learning in non-human primates, such as the discrimination of individuals and the associations of individuals with different levels of reward. The experiments converge on the central hypothesis that during social learning, OT enhances the functional coupling between the basolateral amygdala (BLA) and nucleus accumbens (NAc). Consequently, neurons in the BLA are expected to show greater selectivity for unique combinations of individuals and rewards, while the neural activity across populations of neurons in the amygdalo-striatal networks are expected to show higher oscillatory coherence. To test these hypotheses we designed a conditioned social discrimination task that takes advantage of the visual abilities of macaques to discriminate between individuals presented in videos. This approximates the ability of humans to become highly familiar and accurately predict the behaviors of individuals even without real-life interactions, a process that is impaired in many psychiatric disorders, including autism. As this reward-driven task has both perceptual and operant components, it is expected to involve activation of and communication between the BLA and NAc. The task, therefore, will generate brain states that are conducive to capture the neural signature of interactions in the amygdalo-striatal networks. We will measure and compare both single unit activity and local field potential in the BLA and NAc while monkeys perform the task after local BLA infusion of OT or vehicle. In the primates, OT receptors (OXTR) are synthesized in the nucleus basalis of Meynert (NBM), not in the BLA. This inspired our secondary hypothesis that the neurophysiological effects of OT in the BLA are mediated by cholinergic (Ach) mechanisms. The mechanisms are driven by OXTR signaling on NBM neurons that project to the BLA. The ACh system enhances learning and memory across species and we hypothesize that during social learning, OT amplifies ACh release in the BLA, thereby increasing salience of social stimuli. The precise contribution and the synergy between the OT and Ach systems in the BLA will be tested by neurophysiological recordings coupled with direct injections of OT and cholinergic agonist/antagonists into the BLA or NBM. This project is highly integrated with the rodent studies in Project 3, which investigates OT/ACh interactions in social discrimination conditioned by extrinsic reward by simultaneous recordings of local field potentials and units in the BLA and NAc of rats.

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National Institute of Mental Health (NIMH)
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Emory University
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Dobolyi, Arpad; Cservenák, Melinda; Young, Larry J (2018) Thalamic integration of social stimuli regulating parental behavior and the oxytocin system. Front Neuroendocrinol 51:102-115
Rogers, Christina N; Ross, Amy P; Sahu, Shweta P et al. (2018) Oxytocin- and arginine vasopressin-containing fibers in the cortex of humans, chimpanzees, and rhesus macaques. Am J Primatol 80:e22875
Ortiz, Juan J; Portillo, Wendy; Paredes, Raul G et al. (2018) Resting state brain networks in the prairie vole. Sci Rep 8:1231
Putnam, Philip T; Young, Larry J; Gothard, Katalin M (2018) Bridging the gap between rodents and humans: The role of non-human primates in oxytocin research. Am J Primatol 80:e22756
Bosch, Oliver J; Young, Larry J (2018) Oxytocin and Social Relationships: From Attachment to Bond Disruption. Curr Top Behav Neurosci 35:97-117
Andari, Elissar; Hurlemann, Rene; Young, Larry J (2018) A Precision Medicine Approach to Oxytocin Trials. Curr Top Behav Neurosci 35:559-590
Miranda-Dominguez, Oscar; Feczko, Eric; Grayson, David S et al. (2018) Heritability of the human connectome: A connectotyping study. Netw Neurosci 2:175-199
Li, Gaizhi; Liu, Penghong; Andari, Elissar et al. (2018) The Role of Amygdala in Patients With Euthymic Bipolar Disorder During Resting State. Front Psychiatry 9:445
Walum, Hasse; Young, Larry J (2018) The neural mechanisms and circuitry of the pair bond. Nat Rev Neurosci 19:643-654
Pohl, Tobias T; Young, Larry J; Bosch, Oliver J (2018) Lost connections: Oxytocin and the neural, physiological, and behavioral consequences of disrupted relationships. Int J Psychophysiol :

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