Re-examining overlap between tactile and visual motion responses within hMT+ and STS

Abstract

Here, we examine overlap between tactile and visual motion BOLD responses within the human MT+ complex. Although several studies have reported tactile responses overlapping with hMT+, many used group average analyses, leaving it unclear whether these responses were restricted to subregions of hMT+. Moreover, previous studies either employed a tactile task or passive stimulation, leaving it unclear whether or not tactile responses in hMT+ are simply the consequence of visual imagery. Here, we carried out a replication of one of the classic papers finding tactile responses in hMT+. We mapped MT and MST in individual subjects using visual field localizers. We then examined responses to tactile motion on the arm, either presented passively or in the presence of a visual task performed at fixation designed to minimize visualization of the concurrent tactile stimulation. To our surprise, without a visual task, we found only weak tactile motion responses in MT (6% of voxels showing tactile responses) and MST (2% of voxels). With an unrelated visual task designed to withdraw attention from the tactile modality, responses in MST were reduced to almost nothing (<1% regions). Consistent with previous results, we did observe tactile responses in STS regions superior and anterior to hMT+. Despite the lack of individual overlap, group-averaged responses produced strong spurious overlap between tactile and visual motion responses within hMT+ that resembled those observed in previous studies. The weak nature of tactile responses in hMT+ (and their abolition by withdrawal of attention) suggests that hMT+ may not serve as a supramodal motion processing module.

Keywords: Attention; Cross-modal; Multimodal; Multisensory; fMRI.

Figure 1

Schematic of the tactile and visual paradigm for the following conditions: (A) Tactile stimulation without a visual task. Left and right arms were stimulated on separate scans. (B) Tactile motion with a visual task, (C) hMT+ visual motion localizer, (D) Lateralized MT/MST visual motion localizer. Stimuli were presented to left and right visual field on separate scans. (E) Visual motion with and without a visual task.

Figure 2

Cortical surface maps for tactile responses for the no visual task and visual task conditions. Upper panels show responses from a single subject for left and right arm separately. Lower panels show responses in the remaining 4 subjects, with responses collapsed across left and right arms such that voxels were considered responsive to tactile stimulation if they responded to tactile stimulation of either the left or the right arm. Significant responses to tactile stimulation of either the left or right arm vs. rest (q(FDR) < 0.05) is shown in red, MT is shown in blue, MST is shown in green. Overlap between tactile responses and MT and MST are shown in purple and orange respectively.

Figure 3

Leftward panels show Beta weights for tactile responses within MT and MST. For comparison, responses to the contralateral visual motion stimulus are shown for each ROI (black bars). Responses in the absence of a distractor visual task are shown in red, and responses in the presence of a distractor visual task are shown with red hatched bars. Data are shown separately for left and right hemispheres, and left and right arms of stimulation. Each bar represents data averaged across subjects and single standard error bars are shown. Asterisks represent whether responses were significantly different from zero. * p<0.05, * p<0.01, * p<0.001. Rightward panels show the percentage of voxels within MT and MST that responded to tactile motion with and without a visual task. Again, voxels were considered to respond to tactile motion if they showed significant responses to tactile stimulation of either the left or the right arm vs. rest. The dotted line represents the number of voxels that might be expected to respond to tactile stimulation simply as a consequence of false positives.

Figure 4

fMRI time course in percent signal change within MT and MST for contralateral visual motion stimulus (A), tactile motion stimulus without a visual task (B: right arm; C: left arm), tactile motion stimulus with a visual task (D. right arm; E: left arm). Note that scale on the y-axis was changed for all tactile conditions. Leftward panels show time course data in right MT and MST, and rightward panels show time course data in left MT and MST. MT is shown in blue and MST is shown in green. Solid lines show contralateral stimulation, and dashed lines show ipsilateral stimulation. Shading represents the period of visual/tactile stimulation (10s block for visual stimulation, 24s block for tactile stimulation consisting of 4 5-s brushes).

Figure 5

The potential for spurious overlap between visual and tactile activation due to group averaging. Activation patterns are recolored so as to be consistent across all figures. Red shows tactile responses, green shows visual motion responses, and purple shows regions of overlap. (A, B) Group average tactile motion responses from the no visual task condition (C) and the visual task condition (D) reported in Figure 2, showing regions that responded to stimulation of either arm. Data are thresholded at q(FDR)<0.05. (C) Group average data reprinted from (Ricciardi et al. 2007). Tactile stimulation was via Braille-like dot patterns on a plastic surface undergoing translational and rotational tactile flow. Data are thresholded at z>+/- 3.5. (D) Group average data reprinted from (van Kemenade et al. 2014). Subjects performed a tactile motion direction discrimination task on moving Braille-like dot stimuli applied bilaterally to the fingertip. Data are thresholded at FWE p <0.05. The dotted line shows the estimated location of hMT+.