Sensory tuning in neuronal movement commands

Abstract

Movement control is critical for successful interaction with our environment. However, movement does not occur in complete isolation of sensation, and this is particularly true of eye movements. Here we show that the neuronal eye movement commands emitted by the superior colliculus, a structure classically associated with oculomotor control, encompass a robust visual sensory representation of eye movement targets. Thus, similar saccades towards different images are associated with different saccade-related 'motor' bursts. Such sensory tuning in superior colliculus saccade motor commands appeared for all image manipulations that we tested, from simple visual features to real-life object images, and it was also strongest in the most motor neurons in the deeper collicular layers. Visual-feature discrimination performance in the motor commands was also stronger than in visual responses. Comparing superior colliculus motor command feature discrimination performance to that in the primary visual cortex during steady gaze fixation revealed that collicular motor bursts possess a reliable peri-saccadic sensory representation of the peripheral saccade target's visual appearance, exactly when retinal input is most uncertain. Consistent with this, we found that peri-saccadic perception is altered as a function of saccade target visual features. Therefore, superior colliculus neuronal movement commands likely serve a fundamentally sensory function.

Sensory tuning in neuronal movement commands

“…The raw SC visual and motor burst data collected for the purposes of this study are publicly available at: https://osf.io/qpj7m/ ( 64 ).…”

Distinct context- and content-dependent population codes in superior colliculus during sensation and action

“…This accumulating activity can even be observed in early visual areas ( 52 ), which arguably serves to induce a different state in the sensorimotor circuitry by the time of target presentation and impacts the subsequent visual response in the gap task. For matched behavioral metrics and identical stimulus conditions, the saccade-related motor burst of SC neurons is thought to be task invariant as long as the target remains illuminated ( 12 , 17 ), although target modality and features are known to also modulate the burst ( 53 – 55 ). Thus, we were surprised by the separation of motor subspaces across the two tasks for the identical target ( Fig.…”

Pre-saccadic Preview Shapes Post-Saccadic Processing More Where Perception is Poor

“…This could explain the worse post-saccadic foveal discrimination in the postview task after upward saccades than saccades in other directions: Without attention shifting prospectively to the saccade target -easing trans-saccadic integration by rendering the peripheral visual input more fovea-like-visual sensitivity might recover more slowly after saccade offset. Similarly, in the integration task, because the target disappeared briefly after saccade offset (before vision could fully recover), participants needed to rely more on the peripheral preview (Baumann et al, 2023), leading to a larger preview effect at the UVM.…”

“…This could explain the worse post-saccadic foveal discrimination in the postview task after upward saccades than saccades in other directions: Without attention shifting prospectively to the saccade target –easing trans-saccadic integration by rendering the peripheral visual input more fovea-like– visual sensitivity might recover more slowly after saccade offset. Similarly, in the integration task, because the target disappeared briefly after saccade offset (before vision could fully recover), participants needed to rely more on the peripheral preview (Baumann et al, 2023), leading to a larger preview effect at the UVM. Regardless of the mechanism underlying the worsened post-saccadic sensitivity following upward saccades, the visual system might have given more decision weight to the peripheral preview when a less reliable post-saccadic percepts was expected, consistent with the optimal integration framework (Ganmor et al, 2015; Steward et al, 2020; Wolf & Schütz, 2015).…”