Influence of gaze rotation on the visual response of primate MSTd neurons

Influence of gaze rotation on the visual response of primate MSTd neurons. J. Neurophysiol. 81: 2764-2786, 1999. When we move forward, the visual imag e on our retina expands. Humans rely on the focus, or center, of this expan sion to estimate their direction of bending and, as long as the eyes are st ill, the retinal focus corresponds to the heading. However, smooth rotation of the eyes adds nearly uniform visual motion to the expanding retinal ima ge and causes a displacement of the retinal focus. Ln spite of this, humans accurately judge their heading during pursuit eye movements and during act ive, smooth head rotations even though the retinal focus no longer correspo nds to the heading. Recent studies in macaque suggest that correction for p ursuit may occur in the dorsal aspect of the medial superior temporal area (MSTd) because these neurons are tuned to the retinal position of the focus and they modify their tuning during pursuit to compensate partially for th e focus shift. However, the question remains whether these neurons also shi ft focus tuning to compensate for smooth head rotations that commonly occur during gaze tracking. To investigate this question, we recorded from 80 MS Td neurons while monkeys tracked a visual target either by pursuing with th eir eyes or by vestibule-ocular reflex cancellation (VORC; whole-body rotat ion with eyes fixed in head and head fixed on body). VORC is a passive, smo oth head rotation condition that selectively activates the vestibular canal s. We found that neurons shift their focus tuning in a similar way whether focus displacement is caused by pursuit or by VORC. Across the population. compensation averaged 88 and 77% during pursuit and VORC, respectively (tun ing shift divided by the retinal focus to true heading difference). Moreove r the degree of compensation during pursuit and VORC was correlated in indi vidual cells (P < 0.001). Finally neurons that did not compensate appreciab ly tended to be gain-modulated during pursuit and VORC and may constitute a n intermediate stage in the compensation process. These results indicate th at many MSTd cells compensate for general gaze rotation, whether produced b y eye-in-head or head-in-world rotation, and further implicate MSTd as a cr itical stage in the computation of heading. Interestingly vestibular cues p resent during VORC allow many cells to compensate even though humans do not accurately judge their heading in this condition. This suggests that MSTd may use vestibular information to create a compensated heading representati on within at least a subpopulation of cells, which is accessed perceptually only when additional cues related to active head rotations are also presen t.