Distinct contributions of frontal areas to emotion and social behaviour in the rat

Although the lesions of patients with impaired social behaviour encompass both orbitofrontal and anterior cingulate cortex (OFC and ACC), attempts to model such impairments in animals have focused on the OFC. However, recent neuroimaging attempts to identify the neural correlates of social interaction have emphasized the relative importance of ACC. Here we report the effect of circumscribed excitotoxic lesions of either OFC or ACC on ethological, unconditioned tests of emotion and social behaviour in the Lister hooded rat. OFC lesions altered emotional responsiveness to stimuli in non-social, fear-inducing situations (hyponeophagia test), and produced a small but statistically significant increase in aggression to other rats, but did not compromise other aspects of social interaction and appraisal. ACC lesions did, however, affect the utilization of social information. Specifically, ACC lesions diminished interest in other individuals and caused a relative reduction in memory for social stimuli. Whereas normal animals habituated to repeated presentations of the same individual, the poor performance of ACC animals entailed continued higher levels of responsiveness to repeated presentations of the same individual. The ACC impairment cannot simply be attributed to a general reduction in arousal, or a general impairment in recognition memory. Neither lesion affected anxiety per se (successive alleys test). Further analyses were conducted to investigate whether the changes in aggressive and social behaviour were related to different aspects of decision-making. Although the relationship between changes in social interaction and decision-making after ACC lesions is unclear, OFC impairments in emotionality were correlated with increased impulsive choice.