Modulation of visual signals in macaque MT and MST neurons during pursuit eye movement

Abstract

Retinal image motion is produced with each eye movement, yet we usually do not perceive this self-produced "reafferent" motion, nor are motion judgments much impaired when the eyes move. To understand the neural mechanisms involved in processing reafferent motion and distinguishing it from the motion of objects in the world, we studied the visual responses of single cells in middle temporal (MT) and medial superior temporal (MST) areas during steady fixation and smooth-pursuit eye movements in awake, behaving macaques. We measured neuronal responses to random-dot patterns moving at different speeds in a stimulus window that moved with the pursuit target and the eyes. This allowed us to control retinal image motion at all eye velocities. We found the expected high proportion of cells selective for the direction of visual motion. Pursuit tracking changed both response amplitude and preferred retinal speed for some cells. The changes in preferred speed were on average weakly but systematically related to the speed of pursuit for area MST cells, as would be expected if the shifts in speed selectivity were compensating for reafferent input. In area MT, speed tuning did not change systematically during pursuit. Many cells in both areas also changed response amplitude during pursuit; the most common form of modulation was response suppression when pursuit was opposite in direction to the cell's preferred direction. These results suggest that some cells in area MST encode retinal image motion veridically during eye movements, whereas others in both MT and MST contribute to the suppression of visual responses to reafferent motion.

Fig. 1.

The course of a single pursuit trial with a moving stimulus. The pursuit target moved across the screen in a step-ramp fashion (red). The stimulus window (yellow dots) remained centered on the receptive field (blue dashed lines) as long as the monkey pursued accurately; stimuli usually moved within the window along the axis of the pursuit movement. Fixation trials, trials in 2 pursuit directions, and the speed and direction of stimulus motion within the moving window varied in a randomly interleaved manner from trial to trial.

Fig. 2.

Sample data from a neuron recorded in the medial superior temporal (MST) area. A: each of the 9 panels shows eye-velocity and spiking data from 5 trials, each represented by a different shade of gray. In each trial, saccadic eye-velocity excursions were detected and used to define exclusion windows, indicated by breaks in the lines under each raster line. Allowing for a 50-ms visual latency (Bair and O'Keefe 1998), spikes associated with those excursions (shown in blue) were identified and removed from the analysis. Spikes indicated in red were counted over the period of each trial when eye velocity was close to target velocity to compute a firing rate. The 3 columns represent trials of pursuit in the preferred stimulus direction (left), fixation (middle), and pursuit in the null direction (right). The rows show trials with retinal speeds of 2, 8, and 32°/s. B: averaged firing rates for all tested speeds in the 3 pursuit conditions for this cell. The speeds for which data are shown are marked with gray bands. The smooth curves show fits to the data of the probability density function of the gamma distribution, as described in the text.

Fig. 3.

Speed tuning under different pursuit and fixation conditions for 2 cells recorded from the middle temporal (MT) area (left) and 2 recorded from area MST (right). The plots represent speeds in the preferred and the null stimulus direction as positive and negative values, respectively. Three speed-tuning curves are shown in each plot: responses during pursuit in the preferred stimulus direction in red, during fixation in black, and during pursuit in the null stimulus direction in blue. Responses to fixation or pursuit with no receptive field stimuli are shown with dashed lines. The SEs for the 3 eye-movement conditions were similar, so we show SE bars only for the fixation curve to reduce clutter.

Fig. 4.

A comparison of the observed shift in preferred speed of neurons with the pursuit speed (i.e., the shift expected from the reafference of the pursuit movement) for cells from areas MT and MST. The negative diagonal indicates the prediction shift if velocity compensation were perfect. Cells for which the preferred speed in at least once condition was not well constrained by the data are omitted.

Fig. 5.

Partial correlation analysis of the speed tuning of cells recorded from MT (left) and MST (right) during pursuit and fixation. We computed the correlation of speed tuning during pursuit with the predictions of 2 models: 1) a retinal speed model (abscissa), in which reafferent motion and visual motion are processed together; and 2) a world speed model (ordinate), in which reafferent motion is subtracted from retinal motion to yield a tuning curve defined in world coordinates. The quadrants of each plot indicate whether correlations between speed-tuning curves measured during pursuit and fixation are well explained by the world speed model, the retinal speed model, neither model, or both. The white square in the middle indicates regions of the space in which neither correlation is significant at the level of P < 0.1; the light bands above, below, and to the sides of the square indicate regions in which one correlation was significant but not the other. See text for details.

Fig. 6.

Changes in response magnitude between pursuit and fixation conditions. A: changes in peak firing rate during pursuit for cells recorded in MT (top) and MST (bottom). Red points and marginal distributions are for pursuit in the cell's preferred direction; blue points and marginal distributions are for pursuit in the nonpreferred direction. The mean changes (means ± SE, in impulses/s) in evoked firing rate for preferred pursuit for MT were 0.99 ± 1.22 and for MST the changes were 1.74 ± 1.36 impulses/s; for the nonpreferred pursuit for MT the changes were −1.84 ± 1.36 and for MST the changes were −3.66 ± 1.22. B: changes in baseline firing rate during the same conditions shown in A. Baseline firing is taken as the response during pursuit or fixation in the absence of a visual stimulus to the receptive field. Conventions as in A. The mean changes (means ± SE, in impulses/s) in baseline firing rate for preferred pursuit for MT were 1.94 ± 1.49 and for MST the changes were 2.91 ± 1.10; for nonpreferred pursuit for MT the changes were 1.50 ± 1.27 and for MST the changes were −0.75 ± 0.93. The blue asterisk in A and the red asterisk in B indicate the 2 distributions whose means differ significantly from 0.