Primate superior colliculus neurons activated by unexpected sensation.

Abstract

Midbrain superior colliculus (SC) contains a variety of neuronal types, influencing a rich spectrum of functions beyond gaze orienting. Here, we report on a novel class of SC neurons in the rhesus monkey (Macaca mulatta) that are activated by an unexpected perturbation in a goal-directed arm-movement task. One monkey subject reached for and pressed an illuminated target on a working panel upon a visual go-signal, while maintaining visual fixation elsewhere. On 50% of trials, a task perturbation occurred-the working panel abruptly and unexpectedly moved against the subject's hand after he pressed the target. During the performance, we recorded single SC neurons and found neurons activated exclusively for the task perturbation. These perturbation neurons were localized in the deep lateral zone of the SC, were silent during non-perturbed trials, did not appear to respond to task-irrelevant stimuli, and they had intriguingly long neuronal latencies. If the perturbation neurons' activity relates to the hand-target contact, it may reflect the saliency of an unexpected sensation, i.e. a sensation that is not self-induced and thus cannot be predicted on a basis of the monkey's motor program.