Optogenetic Manipulation of Covert Attention in the Nonhuman Primate

Optogenetics affords new opportunities to interrogate neuronal circuits that control behavior. In primates, the usefulness of optogenetics in studying cognitive functions remains a challenge. The technique has been successfully wielded, but behavioral effects have been demonstrated primarily for sensorimotor processes. Here, we tested whether brief optogenetic suppression of primate superior colliculus can change performance in a covert attention task, in addition to previously reported optogenetic effects on saccadic eye movements. We used an attention task that required the monkey to detect and report a stimulus change at a cued location via joystick release, while ignoring changes at an uncued location. When the cued location was positioned in the response fields of transduced neurons in the superior colliculus, transient light delivery coincident with the stimulus change disrupted the monkey's detection performance, significantly lowering hit rates. When the cued location was elsewhere, hit rates were unaltered, indicating that the effect was spatially specific and not a motor deficit. Hit rates for trials with only one stimulus were also unaltered, indicating that the effect depended on selection among distractors rather than a low-level visual impairment. Psychophysical analysis revealed that optogenetic suppression increased perceptual threshold, but only for locations matching the transduced site. These data show that optogenetic manipulations can cause brief and spatially specific deficits in covert attention, independent of sensorimotor functions. This dissociation of effect, and the temporal precision provided by the technique, demonstrates the utility of optogenetics in interrogating neuronal circuits that mediate cognitive functions in the primate.