Temporally-specific patterns of neural activity across 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, while the patterns of neural activity engaged in striatum and amygdala during affective processing are well established, especially during reward anticipation, little is known about subcallosal ACC. Here we recorded neural activity in non-human primate subcallosal ACC and compared this to interconnected parts of 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, 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. HIGHLIGHTSO_LISustained changes in neural activity signal anticipated reward in basolateral amygdala C_LIO_LITemporally specific patterns signal anticipated reward in all areas recorded C_LIO_LINeurons exhibit more punctate encoding when tasks become more complex C_LIO_LITemporally specific patterns of neural activity signal different anticipated rewards in BLA C_LI