Induced deficits in speed perception by transcranial magnetic stimulation of human cortical areas V5/MT+ and V3A

Abstract

In this report, we evaluate the role of visual areas responsive to motion in the human brain in the perception of stimulus speed. We first identified and localized V1, V3A, and V5/MT+ in individual participants on the basis of blood oxygenation level-dependent responses obtained in retinotopic mapping experiments and responses to moving gratings. Repetitive transcranial magnetic stimulation (rTMS) was then used to disrupt the normal functioning of the previously localized visual areas in each participant. During the rTMS application, participants were required to perform delayed discrimination of the speed of drifting or spatial frequency of static gratings. The application of rTMS to areas V5/MT and V3A induced a subjective slowing of visual stimuli and (often) caused increases in speed discrimination thresholds. Deficits in spatial frequency discrimination were not observed for applications of rTMS to V3A or V5/MT+. The induced deficits in speed perception were also specific to the cortical site of TMS delivery. The application of TMS to regions of the cortex adjacent to V5/MT and V3A, as well as to area V1, produced no deficits in speed perception. These results suggest that, in addition to area V5/MT+, V3A plays an important role in a cortical network that underpins the perception of stimulus speed in the human brain.

Figure 1.

Functional identification of cortical areas V5/MT+ and V3A. Regions of the brain that are most significantly activated by the passive viewing of moving gratings (see Materials and Methods for details) are shown. Areas of most significant activation (p _{(uncorrected)} < 0.0005) are shown for two representative observers (N.C., M.P.B.). There is bilateral activation of the lateral occipito-temporal cortex in a location that is consistent with that of area V5/MT+. In addition, bilateral activation in a region of the superior occipito-parietal cortex can also be observed, and this region lies in close proximity to an area that has been previously identified as V3A.

Figure 2.

Retinotopic validation of functionally defined area V3A. a, The top panel shows the BOLD response phase depicted in false color on the flattened representations of the right hemisphere occipital gray matter for two observers (N.C., M.P.B.). The broken lines indicate locations of visual area boundaries, which occur at reversals in the phase distributions. The inserted representation of the left hemifield allows a direct comparison between the BOLD phase and the region of the visual field stimulated. b, The bottom panel shows the areas identified as V3A on the flattened maps represented on the three-dimensional volume structural MRIs (shown in blue). If one compares these retinotopic localizations of area V3A, with those motion activations shown in Figure 1, it can be observed that the same cortical areas are being activated.

Figure 3.

Timeline of experimental paradigm. The temporal sequence of stimulus presentation used in the delayed speed discrimination paradigm. The moving reference and test stimuli (for full details, see Materials and Methods) were presented 15° to the left of the fixation point (note that for rTMS stimulation of V1, both the reference and test stimulus were placed at the fixation point) and were randomly jittered in terms of motion direction (leftward or rightward), spatial phase on a trial-by-trial basis. These stimuli were separated by an ISI of 1250 ms. In this example, the delivery of the rTMS pulses is coincident with the onset of the test stimulus but could be placed at any point along the timeline.

Figure 4.

Effect of rTMS on performance in speed discrimination task. a, Psychometric functions showing the performance of all five participants on the speed discrimination paradigm. The different curves indicate how performance is affected by the application of rTMS to areas V5/MT+, V3A, and V1 compared with performance when no TMS was delivered. The actual speed of the reference grating was 8°/s. TMS had little effect when applied to V1. When applied to V5/MT+ and V3A, the psychometric functions are shifted to the right, indicating perceived slowing of the test stimulus induced by TMS. The functions also exhibit decreases in slope, which signify an elevation in speed discrimination threshold. b, c, Group-averaged data (n = 5) showing the mean PSE values and speed discrimination thresholds (Δv/v) for the different experimental conditions. The asterisks indicate comparisons for which there are significant differences (p < 0.05) between the no-TMS and applied-TMS conditions. The error bars in this and all subsequent figures refer to ±1 SD of the mean.

Figure 5.

Task specificity control. a, Group-averaged psychometric functions showing how performance varied on a spatial frequency discrimination task while rTMS was delivered to areas V3A and V5/MT+. b, c, Performance is also shown for the no-TMS condition. The mean PSEs (b) and spatial frequency discrimination thresholds (Δf/f) (c) are also shown for the three experimental conditions, none of which exhibit any significant differences from one another.

Figure 6.

Cortical location specificity control. a, The location (red arrow) in a single observer (D.McK.) of a cortical area adjacent to V5/MT+ on the occipito-temporal surface located on a prominent gyrus posterior and medial to V5/MT (green arrow). This area was selected to examine the degree of cortical selectivity associated with disruption to performance by TMS while observers performed the speed discrimination task. b, Comparison of the psychometric functions generated when rTMS is applied in this observer to V5/MT+ (green circles/line), to the non-V5/MT location (red circles/line), and when no rTMS is applied (black circles/line). Functions fitted are represented by Equation 1. c, The location (red arrow) in a single observer (M.P.B.) of a cortical area ventral to V3A (green arrow) selected for rTMS application while the speed discrimination task was performed. d, Comparison of the psychometric functions generated when rTMS is applied in this observer to V3A (green triangles/line), to the non-V3A location (red triangles/line), and when no rTMS is applied (black circles/line).

Figure 7.

Effect of varying TMS strength. a, The magnitude of the decrease in perceived test stimulus speed plotted as a function of rTMS strength. Data are shown for application of rTMS to both V5/MT+ and V3A and are the average of three observers. The data have been fitted with linear regression lines with correlation coefficients (r ²) of 0.948 for the V3A data and 0.951 for the V5/MT+ data. b, Similar plots to a showing the increase in speed discrimination thresholds (Δv/v) with increasing TMS strength; the correlation coefficients (r ²) in this case are 0.952 for V3A and 0.761 for V5/MT+.

Figure 8.

TMS pulse timing. a, The variation in the speed of the test stimulus that was required to match an 8°/s reference when the onset of the rTMS was delivered at different times during the stimulus delivery cycle. The reference and test stimulus onset durations are indicated by the vertical shaded blocks. The variation of matched speed (i.e., PSE) is shown for V5/MT+ (black squares/line), V3A (gray triangles/line), and V1 stimulation (black circles/line). The mean matched speed when no TMS was delivered is shown by the horizontal dotted line banded by a gray area that represents ±1 SD of the mean. The results represent the average of five subjects. b, The variation in speed discrimination thresholds (Δv/v) for the same experiment as shown in a. The same conventions as above apply.