A role for primate subgenual cingulate cortex in sustaining autonomic arousal
Significance Dysregulation of emotion is central to the etiology of mood disorders, such as depression. A causal understanding of how neural structures regulate emotion and arousal could help to improve treatments for these psychiatric disorders. Studies of patients with depression indicate that a particular part of the frontal lobe, the subgenual cingulate cortex, plays an important role in affective processing, though its precise contribution remains unclear. Here we show that, in macaque monkeys, this small part of the frontal cortex is necessary for sustaining elevated arousal in anticipation of positive emotional events. This finding suggests a mechanism for the contribution of this area to affective regulation, including an account for the lack of pleasure and passivity that characterizes mood disorders. The subgenual anterior cingulate cortex (subgenual ACC) plays an important role in regulating emotion, and degeneration in this area correlates with depressed mood and anhedonia. Despite this understanding, it remains unknown how this part of the prefrontal cortex causally contributes to emotion, especially positive emotions. Using Pavlovian conditioning procedures in macaque monkeys, we examined the contribution of the subgenual ACC to autonomic arousal associated with positive emotional events. After such conditioning, autonomic arousal increases in response to cues that predict rewards, and monkeys maintain this heightened state of arousal during an interval before reward delivery. Here we show that although monkeys with lesions of the subgenual ACC show the initial, cue evoked arousal, they fail to sustain a high level of arousal until the anticipated reward is delivered. Control procedures showed that this impairment did not result from differences in autonomic responses to reward delivery alone, an inability to learn the association between cues and rewards, or to alterations in the light reflex. Our data indicate that the subgenual ACC may contribute to positive affect by sustaining arousal in anticipation of positive emotional events. A failure to maintain positive affect for expected pleasurable events could provide insight into the pathophysiology of psychological disorders in which negative emotions dominate a patient's affective experience.
Proceedings of the National Academy of Sciences