Spatial relationships of visuomotor transformations in the superior colliculus map.

The oculomotor system is well understood compared with other motor systems; however, we do not yet know the spatial details of sensory to motor transformations. This study addresses this issue by quantifying the spatial relationships between visual and motor responses in the superior colliculus (SC), a midbrain structure involved in the transformation of visual information into saccadic motor command signals. We collected extracellular single-unit recordings from 150 visual-motor (VM) and 28 motor (M) neurons in two monkeys trained to perform a nonpredictive visually guided saccade task to 110 possible target locations. Motor related discharge was greater than visual related discharge in 94% (141/150) of the VM neurons. Across the population of VM neurons, the mean locations of the peak visual and motor responses were spatially aligned. The visual response fields (RFs) were significantly smaller than and usually contained within the motor RFs. Converting RFs into the SC coordinate system significantly reduced any misalignment between peak visual and motor locations. RF size increased with increasing eccentricity in visual space but remained invariant on the SC map beyond 1 mm of the rostral pole. RF shape was significantly more symmetric in SC map coordinates compared with visual space coordinates. These results demonstrate that VM neurons specify the same location of a target stimulus in the visual field as the intended location of an upcoming saccade with minimal misalignment to downstream structures. The computational consequences of spatially transforming visual field coordinates to the SC map resulted in increased alignment and spatial symmetry during visual-sensory to saccadic-motor transformations.

Discharge properties of monkey tectoreticular neurons.

The intermediate layers of the superior colliculus (SC) contain neurons that clearly play a major role in regulating the production of saccadic eye movements: a burst of activity from saccade neurons (SNs) is thought to provide a drive signal to set the eyes in motion, whereas the tonic activity of fixation neurons (FNs) is thought to suppress saccades during fixation. The exact contribution of these neurons to saccade control is, however, unclear because the nature of the signals sent by the SC to the brain stem saccade generation circuit has not been studied in detail. Here we tested the hypothesis that the SC output signal is sufficient to control saccades by examining whether antidromically identified tectoreticular neurons (TRNs: 33 SNs and 13 FNs) determine the end of saccades. First, TRNs had discharge properties similar to those of nonidentified SC neurons and a proportion of output SNs had visually evoked responses, which signify that the saccade generator must receive and process visual information. Second, only a minority of TRNs possessed the temporal patterns of activity sufficient to terminate saccades: Output SNs did not cease discharging at the time of saccade end, possibly continuing to drive the brain stem during postsaccadic fixations, and output FNs did not resume their activity before saccade end. These results argue against a role for SC in regulating the timing of saccade termination by a temporal code and suggest that other saccade centers act to thwart the extraneous SC drive signal, unless it controls saccade termination by a spatial code.