Eye Position Effects in Monkey Cortex. I. Visual and Pursuit-Related Activity in Extrastriate Areas MT and MST

Abstract

We studied the effect of eye position on visual and pursuit-related activity in neurons in the superior temporal sulcus of the macaque monkey. Altogether, 109 neurons from the middle temporal area (area MT) and the medial superior temporal area (area MST) were tested for influence of eye position on their stimulus-driven response in a fixation paradigm. In this paradigm the monitored eye position signal was superimposed onto the stimulus control signal while the monkey fixated at different locations on a screen. This setup guaranteed that an optimized stimulus was moved across the receptive field at the same retinal location for all fixation locations. For 61% of the MT neurons and 82% of the MST neurons the stimulus-induced response was modulated by the position of the eyes in the orbit. Directional selectivity was not influenced by eye position. One hundred sixty-eight neurons exhibited direction-specific responses during smooth tracking eye movements and were tested in a pursuit paradigm. Here the monkey had to track a target that started to move in the preferred direction with constant speed from five different locations on the screen in random order. Pursuit-related activity was modulated by eye position in 78% of the MT neurons as well as in 80% of the MST neurons tested. Neuronal activity varied linearly as a function of both horizontal and vertical eye position for most of the neurons tested in both areas, i.e., two-dimensional regression planes could be approximated to the responses of most of the neurons. The directions of the gradients of these regression planes correlated neither with the preferred stimulus direction tested in the fixation paradigm nor with the preferred tracking direction in the pursuit paradigm. Eighty-six neurons were tested with both the fixation and the pursuit paradigms. The directions of the gradients of the regression planes fit to the responses in both paradigms tended to correlate with each other, i.e., for more than two thirds of the neurons the angular difference between both directions was less than +/-90 degrees. The modulatory effect of the position of the eyes in the orbit proved to balance out at the population level for neurons in areas MT and MST, tested with the fixation as well as the pursuit paradigm. Results are discussed in light of the hypothesis of an ongoing coordinate transformation of the incoming sensory signals into a nonretinocentric representation of the visual field.

Maps of Visual Space in Human Occipital Cortex Are Retinotopic, Not Spatiotopic

“…The most commonly reported effect of eye position is to change the overall gain of visual responses (Andersen et al, 1985b;Bremmer et al, 1997). Such gain fields scale the magnitude of retinotopic visual responses as a function of the position of the eye in the orbit.…”

Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area

“…originate in different spatial reference frames. Specifically, visual motion signals originate in retinal coordinates Maioli, 1996, 1997;Bremmer et al, 1997), whereas vestibular signals are head/body centered (Shaikh et al, 2004). It is often assumed that optic flow signals must first be converted into a headcentered reference frame, before being useful for heading perception (Royden, 1994;Royden et al, 1994;Banks et al, 1996).…”

Spatial Reference Frames of Visual, Vestibular, and Multimodal Heading Signals in the Dorsal Subdivision of the Medial Superior Temporal Area

“…Independent of such tuning shifts, another potentially important feature of many extrastriate and posterior parietal neurons is a modulation of response gain as a function of eye position, known as a "gain field" (Andersen et al, 1985(Andersen et al, , 1990Bremmer et al, 1997). For the present study, a gain field was defined as a significant Figure 7.…”

“…Three main factors may account for this difference. First, our experimental paradigm differed fundamentally from that of Bremmer et al (1997), who measured visual responses to planar motion stimuli that were always presented at the optimal speed, size, and retinal location for each neuron. We, however, measured heading tuning using a set of 3D optic flow stimuli that was identical for all neurons.…”