We propose a continuation and extension of studies designed to analyze the neurobiological basis of social behavior in macaque monkeys. The overarching goal of this program is to determine which neural systems are specialized to process socially relevant information and to guide social behavior. During the first four years of this program, we established the physical and personnel infrastructure to examine the effects of brain manipulations on conspecific social behavior in adult and infant rhesus monkeys. In particular, we established highly successful protocols of animal husbandry that allow infants, following lesions at two weeks of age, to be raised by their biological mothers and to participate in daily socialization that insures normal socioemotional development. Contrary to our initial hypothesis, investigations conducted thus far indicate that the amygdala is not essential for normal social behavior in the adult, and is not necessary for gaining social knowledge during development. Our findings are consistent with the hypothesis that the amygdala is a danger detector. It functions, in part, to evaluate objects and organisms in the environment as potential threats and then marshals an appropriate response. Interestingly, lesions of infant subjects produce greater social fear despite the absence of the amygdala and the lack of fear of objects! In the next funding period, we propose to follow the further development of socioemotional, sexual and maternal behavior of the 16 monkeys that received lesions of the amygdala or hippocampus at two weeks of age. We also propose to use high-resolution positron emission tomography (microPET) to evaluate brain plasticity resulting from the early lesions and to search for the neural substrates of the abnormal social fear that we observe in infant monkeys with amygdala lesions. We will also introduce a new genetic method, using viral transfection of the amygdala with the gene for the Drosophila allatostatin receptor, for producing selective and reversible inactivation of the amygdala in freely behaving monkeys. Finally, we will study adult animals with lesions of the orbitofrontal or medial dorsal frontal cortex in an attempt to define the neural network associated with normal social behavior. While these studies are designed to investigate the neural networks for normal socioemotional cognition, we believe that our findings will have important implications for disorders such as autism, social phobia and anxiety.
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