Task-Dependent Spatial Selectivity in the Primate Amygdala

Humans and other animals routinely encounter visual stimuli that indicate whether future reward delivery depends upon the identity or location of a stimulus, or the performance of a particular action. These reinforcement contingencies can influence how much attention is directed toward a stimulus. Neurons in the primate amygdala encode information about the association between visual stimuli and reinforcement as well as about the location of reward-predictive stimuli. Amygdala neural activity also predicts variability in spatial attention. In principle, the spatial properties of amygdala neurons may be present independent of spatial attention allocation. Alternatively, the encoding of spatial information may require attention. We trained monkeys to perform tasks that engaged spatial attention to varying degrees to understand the genesis of spatial processing in the amygdala. During classical conditioning tasks, conditioned stimuli appeared at different locations; amygdala neurons responded selectively to the location of stimuli. These spatial signals diminished rapidly upon stimulus disappearance and were unrelated to selectivity for expected reward. In contrast, spatial selectivity was sustained in time when monkeys performed a delayed saccade task that required sustained spatial attention. This temporally extended spatial signal was correlated with signals encoding reward expectation. Furthermore, variability in firing rates was correlated with variability in spatial attention, as measured by reaction time. These results reveal two types of spatial signals in the amygdala: one that is tied to initial visual responses and a second that reflects coordination between spatial and reinforcement information and that relates to the engagement of spatial attention.