Intrinsic reference frames of superior colliculus visuomotor receptive fields during head-unrestrained gaze shifts.

A sensorimotor neuron's receptive field and its frame of reference are easily conflated within the natural variability of spatial behavior. Here, we capitalized on such natural variations in 3-D eye and head positions during head-unrestrained gaze shifts to visual targets in two monkeys: to determine whether intermediate/deep layer superior colliculus (SC) receptive fields code visual targets or gaze kinematics, within four different frames of reference. Visuomotor receptive fields were either characterized during gaze shifts to visual targets from a central fixation position (32 U) or were partially characterized from each of three initial fixation points (31 U). Natural variations of initial 3-D gaze and head orientation (including torsion) provided spatial separation between four different coordinate frame models (space, head, eye, fixed-vector relative to fixation), whereas natural saccade errors provided spatial separation between target and gaze positions. Using a new statistical method based on predictive sum-of-squares, we found that in our population of 63 neurons (1) receptive field fits to target positions were significantly better than fits to actual gaze shift locations and (2) eye-centered models gave significantly better fits than the head or space frame. An intermediate frames analysis confirmed that individual neuron fits were distributed target-in-eye coordinates. Gaze position "gain" effects with the spatial tuning required for a 3-D reference frame transformation were significant in 23% (7/31) of neurons tested. We conclude that the SC primarily represents gaze targets relative to the eye but also carries early signatures of the 3-D sensorimotor transformation.