Elsevier

Brain Stimulation

Volume 8, Issue 2, March–April 2015, Pages 200-207
Brain Stimulation

Transcranial Magnetic Stimulation (TMS)
Original Article
The Role of Human Brain Area hMT+ in the Perception of Global Motion Investigated With Repetitive Transcranial Magnetic Stimulation (rTMS)

https://doi.org/10.1016/j.brs.2014.11.001Get rights and content

Highlights

  • rTMS with an off-line cTBS protocol of visual areas hMT+ and V1 in the human brain.

  • Deficits in chromatic and achromatic motion perception 11 min after rTMS of hMT+.

  • No deficits for stimulus detection after stimulation of either area.

  • hMT+ mediates the perception of motion of chromatic and achromatic stimuli but not color detection.

Abstract

Background

Psychophysical evidence suggests that the perception of the motion and color of moving stimuli are determined separately in the human brain. Here we aim to determine the role of visual cortical areas hMT+ and V1/V2 in each task by measuring the effect of rTMS of each area using an off-line continuous theta-burst stimulation (cTBS) protocol.

Methods

In the motion task, the direction of moving dots was identified using a global motion stimulus that avoids tracking, and in the detection task for the same stimulus, the presence of the dots was detected regardless of motion. Performance was measured using forced-choice methods in 8 subjects, both before and at 4 time-intervals in the 1-hour after brain stimulation. All experiments were done using achromatic and isoluminant, red-green chromatic stimuli.

Results

Performance on global motion for both achromatic and chromatic stimuli was significantly impaired following cTBS of visual area hMT+, with a maximum effect occurring 11 min after stimulation. In comparison, there was no effect of cTBS on the motion task for areas V1/V2 or the vertex (control). cTBS did not affect the detection task in either area.

Conclusions

Our experiments validate the use of cTBS as an advantageous off-line rTMS protocol for studying visual areas. The results indicate a causal link between neural activity in area hMT+ and perception of motion of isoluminant chromatic stimuli. We conclude that area hMT+ is part of a common pathway processing the global motion of chromatic and achromatic stimuli, but is not involved in their detection.

Introduction

Psychophysical evidence accumulated over several decades has shown that human color vision is poor in the perception of motion. This is thought to arise from the distinct specializations of the dorsal and ventral streams in primate vision for the attributes motion and color, respectively, with good processing of motion but poor sensitivity to color in the dorsal pathway and good processing of color but little sensitivity to motion in the ventral pathway. An overlap of function between the two streams appears to remain, however, allowing color vision to perform on motion tasks under a range of conditions. Such tasks include direction discrimination of isoluminant chromatic gratings at contrasts above threshold [1], [2], motion discrimination on global motion tasks at isoluminance [3], tasks using higher order motion stimuli [4], [5], [6] and the perception of motion after-effects generated by isoluminant chromatic stimuli [7], [8]. In color vision, a clear dissociation has been found between two different types of visual threshold: stimulus detection (color/form threshold) and the discrimination of its direction of motion (motion threshold) [3], [9]. This is based on the surprising observation that luminance noise masks the motion of chromatic stimuli but not their detection: as luminance noise contrast increases, chromatic stimuli show no change in detection threshold (visibility) but loose their perceived motion, eventually appearing static. This supports the idea that motion and detection thresholds are independently determined, with different physiological origins.

Here we aim to determine the physiological origins of chromatic global motion perception versus color detection. We aim to test two linked hypotheses, that hMT+ is involved in chromatic global motion thresholds but not chromatic detection thresholds, by selectively and temporarily impairing processing in two different areas of the human visual cortex using repetitive Transcranial Magnetic Stimulation (rTMS). We predict that stimulation of area hMT+ will selectively impair performance on discriminating the direction of motion of chromatic stimuli but will not affect performance on the detection of the stimulus. In addition, we measure the effect of rTMS applied to areas V1/V2 on motion and detection thresholds, with the aim of determining their comparative roles in these two tasks. As V1/V2 are not selective areas for global stimulus attributes, such as motion, we do not expect pronounced effects on motion discrimination, but might expect an effect on color detection [10].

On-line [11], [12], [13], [14], [15], [16], and off-line [17] TMS have previously been shown to be effective at reducing, or improving [18] motion sensitivity using a range of different stimuli and tasks, stimulation protocols, and brain areas targeted. Here we use a continuous theta-burst stimulation protocol (cTBS) [19], an off-line rTMS protocol, which is relatively novel to vision testing. As part of the study, we aimed to identify the time course for the effects of cTBS, which has not been well established yet for vision. We use global motion stimuli, as these are well suited to reveal the motion selective functions of area hMT+, and can also be used for color detection tasks. We also run all experiments on achromatic stimuli as a control and to verify the effectiveness of cTBS. This is the first attempt to determine the relative selectivity of dorsal area hMT+ (in relation to V1/V2) for color and global motion by direct stimulation of the human brain.

Section snippets

Participants

Eleven healthy participants (5 female, 6 male) took part in the experiments and all had normal or corrected to normal vision, and normal color vision assessed by the Farnsworth–Munsell 100-hue color test (Munsell Color Company Inc, 1957). Written consent was obtained from all participants and none reported any contraindications to rTMS. Experiments were approved locally by the Ethics Review Board of the Montreal Neurological Institute and were performed in accordance with the ethical standards

Experiment 1: effect of contrast on motion direction thresholds

Figure 2 shows thresholds for motion discrimination (percent coherence) as a function of contrast for both the achromatic (circles) and chromatic (triangles) stimuli for three subjects. Stimulus contrast was scaled in multiples of detection threshold in order to control for the effects of stimulus visibility. Thresholds for discriminating global motion direction follow a similar trend for both stimulus types with coherence thresholds asymptoting to stable levels as the contrast of the stimuli

Discussion

This study demonstrates that the use of cTBS significantly impairs the function of area hMT+ in a task-specific manner. Participants performed at significantly lower levels in the motion direction discrimination task after application of cTBS over hMT+ in comparison to stimulation of either the vertex or primary visual cortex. This was apparent for both the achromatic and chromatic global motion stimuli, with maximal effects observed 11 min after stimulation. Contrast detection of either

Conclusion

This study demonstrates that cTBS can disrupt normal cortical function when area hMT+ is targeted, selectively and reversibly impairing motion direction perception in a task-specific and location-specific manner, with the effect peaking 11 min after stimulation. The effect on isoluminant chromatic stimuli suggests some form of cross-talk between the dorsal and the ventral pathways with color providing some input to the dorsal pathway. Overall, the results indicate a causal link between neural

Acknowledgments

We thank Drs Simon Clavagnier, Robert Hess, William McIlhagga, Reza Farivar, and Dorita Chang for their helpful discussions and suggestions. We also thank our subjects for participating in this study.

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    Funding: Supported by the Natural Sciences and Engineering Research Council (grant RGPIN 183625-05) and the Canadian Institutes of Health Research (grant MOP-10891) to KTM and a McGill Faculty of Medicine Internal Studentship to SK.

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