Title: Space and Value in the Primate Amygdala
Description: Planning behavioral actions requires the ability to form associations between stimuli and outcomes in order to appropriately attribute value and emotional significance to the stimuli. This ability to form associations between stimuli and outcomes is also dependent on being able to attend to the stimulus in question, which generally involves honing in on its spatial location. The amygdala is a brain area that has been investigated extensively in the context of forming associations between stimuli and outcomes; however, whether the amygdala may also be important in linking spatial representations of stimuli with their value is relatively unexplored. Recent work has demonstrated that individual primate amygdala neurons reflect both the value of stimulus-outcome associations and the degree to which spatial attention is directed towards valuable stimuli. While these experiments demonstrated that amygdala neurons are selective for value and spatial information in an attentionally-demanding environment, it is still unclear whether similarly coordinated spatial and value selectivity is present in less attentionally-demanding contexts.

To this end, we trained monkeys to perform trace-conditioning tasks similar to those known to induce robust value selectivity within the amygdala; our tasks differed in that we systematically manipulated the spatial location of stimuli in order to evaluate the degree of spatial selectivity in this relatively passive context. Additionally, we used two variants of the trace-conditioning task: a space-irrelevant task in which the relationship between stimuli and outcomes was not dependent on where the stimuli appeared, and a space-relevant task in which the outcome predicted by stimuli was dependent on their spatial location. We reasoned that spatial selectivity in the amygdala might be augmented when spatial variables were relevant to the task, particularly for guiding conditioned responses. This prediction was unsupported, however; amygdala neurons responded similarly in the space-irrelevant and space-relevant tasks. In each task, spatial selectivity was observed mainly around the time that that stimulus was present, and this spatial selectivity was essentially random with respect to neurons' value selectivity.

These results run counter to those observed in attentionally-demanding operant tasks, where spatial selectivity was sustained and coordinated with value selectivity, therefore suggesting that spatial coding in the amygdala is task-dependent. Given the weak and unpredictable spatial selectivity in these trace-conditioning tasks, we asked: Under what degree of attentional load are robust spatial signals apparent in the amygdala? To investigate this, we trained monkeys on an operant task where a single stimulus appeared at one of two locations; monkeys had to detect a second stimulus that appeared at the same location, but at an unpredictable time. Unlike in the trace-conditioning tasks, amygdala neurons exhibited sustained spatial selectivity that was well-coordinated with value selectivity on this task. Further suggesting an influential role on attention, the response of amygdala neurons predicted trial-to-trial fluctuations in monkeys' spatial attention. Together, these results show that the amygdala participates in more than just encoding of value-related or emotional stimuli, expanding its role to include encoding of spatial features and lending support to the notion that this brain area may be involved in emotional guidance of spatial attention in physiological and pathological states.