Express Visuomotor Responses Reflect Knowledge of Both Target Locations and Contextual Rules during Reaches of Different Amplitudes

Abstract

When humans reach to visual targets, extremely rapid (∼90 ms) target-directed responses can be observed in task-relevant proximal muscles. Such express visuomotor responses are inflexibly locked in time and space to the target and have been proposed to reflect rapid visuomotor transformations conveyed subcortically via the tecto-reticulo-spinal pathway. Previously, we showed that express visuomotor responses are sensitive to explicit cue-driven information about the target, suggesting that the express pathway can be modulated by cortical signals affording contextual prestimulus expectations. Here, we show that the express visuomotor system incorporates information about the physical hand-to-target distance and contextual rules during visuospatial tasks requiring different movement amplitudes. In one experiment, we recorded the activity from two shoulder muscles as 14 participants (6 females) reached toward targets that appeared at different distances from the reaching hand. Increasing the reaching distance facilitated the generation of frequent and large express visuomotor responses. This suggests that both the direction and amplitude of veridical hand-to-target reaches are encoded along the putative subcortical express pathway. In a second experiment, we modulated the movement amplitude by asking 12 participants (4 females) to deliberately undershoot, overshoot, or stop (control) at the target. The overshoot and undershoot tasks impaired the generation of large and frequent express visuomotor responses, consistent with the inability of the express pathway to generate responses directed toward nonveridical targets as in the anti-reach task. Our findings appear to reflect strategic, cortically driven modulation of the express visuomotor circuit to facilitate rapid and effective response initiation during target-directed actions.SIGNIFICANCE STATEMENTExpress (∼90 ms) arm muscle responses that are consistently tuned toward the location of visual stimuli suggest a subcortical contribution to target-directed visuomotor behavior in humans, potentially via the tecto-reticulo-spinal pathway. Here, we show that express muscle responses are modulated appropriately to reach targets at different distances, but generally suppressed when the task required nonveridical responses to overshoot/undershoot the real target. This suggests that the tecto-reticulo-spinal pathway can be exploited strategically by the cerebral cortex to facilitate rapid initiation of effective responses during a visuospatial task.