Temporally specific patterns of neural activity in interconnected corticolimbic structures during reward anticipation

Abstract

Functional neuroimaging studies indicate that interconnected parts of the subcallosal anterior cingulate cortex (ACC), striatum, and amygdala play a fundamental role in affect in health and disease. Yet, although the patterns of neural activity engaged in the striatum and amygdala during affective processing are well established, especially during reward anticipation, less is known about subcallosal ACC. Here, we recorded neural activity in non-human primate subcallosal ACC and compared this with interconnected parts of the basolateral amygdala and rostromedial striatum while macaque monkeys performed reward-based tasks. Applying multiple analysis approaches, we found that neurons in subcallosal ACC and rostromedial striatum preferentially signal anticipated reward using short bursts of activity that form temporally specific patterns. By contrast, the basolateral amygdala uses a mixture of both temporally specific and more sustained patterns of activity to signal anticipated reward. Thus, dynamic patterns of neural activity across populations of neurons are engaged in affect, especially in subcallosal ACC.