Abstract
Microsaccades are tiny saccades that take place during gaze fixation. Although long considered to occur randomly, recent evidence suggests that these movements are systematically biased by covert shifts of visual attention. Here, we show that superior colliculus (SC) activity is necessary for this influence of attention on microsaccades.
In 19 experiments, we reversibly inactivated SC neurons representing peripheral visual locations while two monkeys performed a demanding covert attention task. In this task, monkeys maintained fixation while four peripheral rings appeared in each visual quadrant. One of the rings was a different color from the others, serving as the attentional cue. Random dot motion patches (0% coherence) appeared inside each ring, and after some random delay, a brief coherent motion pulse occurred in the cued quadrant and in the diametrically opposite location (distractor). Monkeys had to report the direction of the cued pulse, irrespective of the distractor. We inactivated the SC with muscimol (see Lovejoy & Krauzlis, Nature Neuroscience, 2010) and compared microsaccade behavior before (baseline) and after inactivation.
When a cue guiding attention appeared in the peripheral visual region affected by SC inactivation, this cue's nominal influence in biasing microsaccade directions (confirmed from baseline data) disappeared. When the cue appeared in the region diametrically opposite from the affected area, its effectiveness in biasing microsaccade directions re-emerged. Importantly, these effects were not accompanied by a reduction in the overall microsaccade rate, suggesting that peripheral inactivation did not impair the motor control of microsaccades.
We conclude that SC activity is causally involved in the previously observed relationship between microsaccades and covert shifts of attention to peripheral locations. We hypothesize that biases in SC activity during attentional allocation normally alter the overall balance of SC activity representing the foveal fixated goal, in a manner sufficient to periodically trigger small saccades.