Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts.
The supplementary eye fields (SEFs), located on the dorsomedial surface of the frontal cortex, are involved in high-level aspects of saccade generation. Some reports suggest that the same area could also be involved in the generation of motor commands for the head. If so, it is important to establish whether this structure encodes eye and head commands separately or gaze commands that give rise to coordinated eye-head movements. Here we systematically stimulated (50 microA, 300 Hz, 200 ms) the SEF of two head-free (head unrestrained) macaques while recording three-dimensional eye and head rotations. A total of 55 sites were found to consistently elicit saccade-like gaze movements, always in the contralateral direction with variable vertical components, and ranging in average amplitude from 5 to 60 degrees. These movements were always a combination of eye-in-head saccades and head-in-space movements. We then performed a comparison between these movements and natural gaze shifts. The kinematics of the elicited movements (i.e., their temporal structure, their velocity-amplitude relationships, and the relative contributions of the eye and the head as a function of movement amplitude) were indistinguishable from those of natural gaze shifts. Additionally, they obeyed the same three-dimensional constraints as natural gaze shifts (i.e., eye-in-head movements obeyed Listing's law, whereas head- and eye-in-space movements obeyed Donders' law). In summary, gaze movements evoked by stimulating the SEF were indistinguishable from natural coordinated eye-head gaze shifts. Based on this we conclude that the SEF explicitly encodes gaze and that the kinematics aspects of eye-head coordination are implicitly specified by mechanisms downstream from the SEF.
Martinez-Trujillo
Julio C
JC
Centre for Vision Research and Canadian Institute for Health Research, Group for Action and Perception, Department of Psychology, York University, Toronto, Ontario M3J 1P3, Canada. trujillo@yorku.ca
Wang
Hongying
H
Crawford
J Douglas
JD
D000818:Animals; D001696:Biomechanical Phenomena; D004558:Electric Stimulation; D005133:Eye Movements / Q000502:physiology*; D005625:Frontal Lobe / Q000502:physiology*; D019416:Head Movements / Q000502:physiology*; D008253:Macaca mulatta; D009949:Orientation; D011597:Psychomotor Performance / Q000502:physiology*; D012399:Rotation