Motion opponency in visual cortex

Abstract

Perceptual studies suggest that visual motion perception is mediated by opponent mechanisms that correspond to mutually suppressive populations of neurons sensitive to motions in opposite directions. We tested for a neuronal correlate of motion opponency using functional magnetic resonance imaging (fMRI) to measure brain activity in human visual cortex. There was strong motion opponency in a secondary visual cortical area known as the human MT complex (MT+), but there was little evidence of motion opponency in primary visual cortex. To determine whether the level of opponency in human and monkey are comparable, a variant of these experiments was performed using multiunit electrophysiological recording in areas MT and MST of the macaque monkey brain. Although there was substantial variability in the degree of opponency between recording sites, the monkey and human data were qualitatively similar on average. These results provide further evidence that: (1) direction-selective signals underly human MT+ responses, (2) neuronal signals in human MT+ support visual motion perception, (3) human MT+ is homologous to macaque monkey MT and adjacent motion sensitive brain areas, and (4) that fMRI measurements are correlated with average spiking activity.

Fig. 1.

Statistical analysis of fMRI measurements.A, fMRI measurements of MT+ activity from 10 repeats (1 per scanning session) of the reference scan for subject djh. Response amplitude (percent MR signal modulation) indicated by radial distance from the origin and response temporal phase indicated by the angle from the horizontal axis. Circles, Responses from the 10 individual scans. Dashed line indicating the reference phase, passes through the vector mean of the 10 data points.B, MT+ responses in one of the experimental test conditions (high-density paired versus unpaired dots) for the same subject.Circles, Responses from the eight individual scans.Dashed line (copied from A) indicates the reference phase. C, Histogram of fMRI response amplitude components, produced from B by computing the orthogonal projection of each data point onto the dashed line.

Fig. 2.

Motion opponency in human MT+. fMRI responses to stimuli that alternated between counterphase and moving gratings. Response amplitude (percent MR signal modulation) indicated by radial distance from the origin, and response temporal phase indicated by the angle from the horizontal axis. Responses from V1 (open symbols) are near 0°, in phase with the presentation of counterphase gratings. Responses from MT+ (filled symbols) are near 180°, in phase with the presentation of moving gratings. Two panels correspond to the two subjects. Plot symbols represent the vector average of between four and six measurements that were repeated in separate scans. Large circles represent 95% confidence intervals on the bivariate distributions of response amplitudes and phases. Circles: sf = 0.8 cycle/°; tf = 4 Hz; mean luminance = 36 cd/m²; mean moving grating contrast = 45.75%; mean counterphase grating contrast = 91.5%; n = 5 for both subjects.Squares: sf = 0.4 cycle/°; tf = 8 Hz; mean luminance = 3 cd/m²; mean moving grating contrast = 44.25%; mean counterphase grating contrast = 88.5%; n = 5 for djh; n = 4 for gmb.Triangles: sf = 0.8 cycle/°; tf = 4 Hz; mean luminance = 36 cd/m²; mean moving grating contrast = 6.25%; mean counterphase grating contrast = 12.5%; n = 6 for djh; n = 5 for gmb.

Fig. 3.

fMRI response amplitudes in visual areas V1 and MT+ to stimuli that alternated between test gratings and a uniform gray field. White bars, Moving gratings (sf = 0.4 cycle/°; tf = 8 Hz; mean luminance = 3 cd/m²; mean contrast = 44.25%; n = 7 for djh;n = 8 for gmb). Gray bars, Counterphase gratings (same sf, tf, and mean luminance, mean contrast = 88.5%;n = 6 for djh; n = 8 for gmb). MT+ responses are greater to moving than to counterphase gratings. Bar height, Mean component response amplitudes (see Materials and Methods). Error bars indicate SEM.

Fig. 4.

Supersaturation control. fMRI responses (same format as Fig. 2) to moving grating stimuli that alternated between high (mean, 95%) and medium (mean, 47.75%) contrasts. sf = 0.8 cycle/°; tf = 4 Hz; mean luminance = 36 cd/m²; n = 6 for djh;n = 5 for gmb.

Fig. 5.

Motion opponency with random dot stimuli. fMRI responses (same format as Fig. 2) to paired versus unpaired dots.A, Low dot density (n = 8 for both subjects). Both V1 (open symbols) and MT+ (filled symbols) responses are near 180°, in phase with the presentation of unpaired dots. B, High dot density (n = 8 for both subjects). MT+ responses (filled symbols) are near 180°, in phase with the presentation of unpaired dots.

Fig. 6.

Multiunit responses in monkey MT to moving and counterphase grating stimuli shown as PSTH. A, Responses to high-contrast stimuli. B, Responses to low-contrast stimuli.Dark solid curves, Response to gratings moving first at 45° and than at 225°. Light solid curves, Response to gratings moving first at 225° and then at 45°. Dashed curves, Response to counterphase grating oriented at 135°. Responses are aligned to stimulus onset (time 0) and are binned in 100 msec time bins.

Fig. 7.

Polar plot depicting multiunit responses in monkey MT (same site as in Fig. 6) to moving and counterphase gratings.A, Responses to high-contrast stimuli. B, Responses to low-contrast stimuli. The angle of the polar plot indicates the direction of motion for the moving grating. For the counterphase gratings, each orientation is plotted twice at the two opposite directions from which the counterphase stimulus is composed (i.e., vertical counterphase stimulus generates two points at 0 and 180°). Radial distance from the origin indicates the magnitude of the response in events per second, scale given at the bottom left. The response to each stimulus condition was measured as the mean firing rate during the 500 msec starting 50 msec after stimulus onset. Solid curves, Responses to moving stimuli.Dashed curves, Responses to counterphase stimuli. Thegray polygon at the center indicates baseline activity estimated as the average firing rate during the 300 msec preceding stimulus onset.

Fig. 8.

Polar plot depicting multiunit responses (same format as Fig. 7) to high-contrast moving and counterphase gratings at a second site in monkey MT, which does not exhibit motion opponency.

Fig. 9.

Scatter plot of the normalized responses to moving and counterphase stimuli in all sites recorded from the two monkeys. The response for each single or mulitunit site to moving stimuli was computed as the mean firing rate during the entire 5.8 sec trial, averaged over all directions of motion. Similarly, the response to the counterphase stimuli was computed as the mean firing rate over all counterphase orientations. These responses were than normalized according to the baseline activity at that site (see Materials and Methods). A, Low-contrast stimuli in monkey S. B, High-contrast stimuli in monkey S. C, Low-contrast stimuli in monkey M. D, High-contrast in monkey M. The four points marked by + correspond to the four MST sites. E, Normalized responses of 12 single units in MT of monkey S to low-contrast stimuli. F, Same for high contrast.