SACCADES TO SOMATOSENSORY TARGETS .3. EYE-POSITION-DEPENDENT SOMATOSENSORY ACTIVITY IN PRIMATE SUPERIOR COLLICULUS

1. We recorded from cells with sensory responses to somatosensory stim uli in the superior colliculus (SC) of awake monkeys. Our goal was to determine the frame of reference of collicular somatosensory signals b y seeing whether the positions of the eyes influenced the responses of cells to a given tactile stimulus. Somatosensory targets consisted of vibrotactile stimuli delivered to the hands, which were held in fixed spatial positions. Monkeys performed a delayed saccade task from diff erent initial fixation positions to the locations of these tactile sti muli or to visual stimuli at approximately the same location. 2. The r esponses of a majority of somatosensory cells (25 of 34 or 74%) were s ignificantly affected by eye position. Nearly all somatosensory cells also responded to visual targets (28 of 30, 93%). Cells whose somatose nsory responses depended on eye position responded to visual and somat osensory tar ets located at approximately the same direction in space with respect to the eyes. 3. The activity of these cells exhibited bot h sensory and motor qualities. The discharge was more closely linked i n time to stimulus onset than to the movement. Sensory features of the stimulus were reflected in the responses: the discharge of a number o f cells was phase-locked to the pulses of vibration. The sensory respo nses occurred even if the animal's next saccade was not directed into the response field of the cell. However, two thirds of the cells also exhibited a burst of motor activity in conjunction with the saccade to the somatosensory target. Sensory and motor activity were not always spatially coextensive. When different, the tuning of motor activity wa s broader. 4. Cells with somatosensory responses to vibratory stimulat ion of the hands were found in a wide region of the SC, spanning a 40 degrees range of movement amplitudes. 5. These data show that somatose nsory signals in the SC are not purely somatotopic but are dependent o n eye position. For stimuli at a fixed location, this eye position dep endence allows somatosensory and visual signals to be in register and share a premotor circuitry for guiding saccadic eye movements. 6. The dependence of the somatosensory responses on eye position suggests tha t the somatosensory receptive fields may either shift on the body surf ace or they may be restricted to a limited region of the body surface but be gated by eye (and body) position. Future experiments varying bo dy position and the location of the stimulus on the body surface are n eeded to determine which of these alternatives is correct. Cells with either type of receptive field could provide an unambiguous signal of the location of somatosensory saccade targets with respect to the eyes . The transformation of somatosensory signals from a body-centered fra me of reference to a frame of reference that depends on the position o f the stimulus with respect to the eyes is necessary for the correct a ctivation of collicular neurons with motor activity, because this acti vity encodes saccades as desired changes in eye position.