Cortical activity to vibrotactile stimulation: an fMRI study in blind and sighted individuals

Abstract

Blind individuals show visual cortex activity during Braille reading. We examined whether such cross-modal activations reflect processing somatosensory stimuli independent of language by identifying cortical activity during a one-back vibrotactile matching task. Three groups (sighted, early-onset, and late-onset [>12 years] blind) detected whether paired vibrations (25 and 100 Hz), delivered to the right index finger, differed in frequency. Three successive paired vibrations, followed by a no-stimulation interval, were presented in a long event-related design. A fixed effects average z-score analysis showed increased activity throughout the visuotopic visual cortex, where it was mostly restricted to foveal and parafoveal eccentricities. Early blind showed the most extensive distribution of activity. Late blind exhibited activity mostly in similar regions but with declining response magnitudes with age of blindness onset. Three sighted individuals had suprathreshold activity in V1 but negative responses elsewhere in visual cortex. Mixed effects ANOVA confirmed group distinctions in defined regions (V1, V3, V4v, V7, LOC, and MT). These results suggest cross-modal adaptation to tactile stimulation in visual cortex independent of language processes. All groups showed increased activity in left primary (S1) and bilateral second somatosensory areas, but without response magnitude differences between groups throughout sensorimotor cortex. Early blind showed the greatest spatial extent of S1 activity. Blind participants had more extensive bilateral activity in anterior intraparietal sulcus and supramarginal gyrus. Extensive usage of touch in Braille reading may underlie observed S1 expansions in the reading finger representation. In addition, learned attentiveness to touch may explain similar expansion of parietal tactile attention regions.

Figure 1

Task paradigm and records of tactile vibration stimuli. A: Single analysis epochs consisted of three successive pairs of tactile vibrations between 0 and 8.52 s (frames 1–3) followed by ∼14 s (8.52 to 22.72 s or frames 4–8) with no stimulation. Each vibration lasted 750 ms and the interval between pairs was 300 ms. This was followed by 1.5 s for participant responses. Each vibration pair occurred within, but was not synchronized with, the beginning of an image frame. B: Paired vibrations were matched (25–25 Hz or 100–100 Hz) or unmatched frequencies (25 and 100 Hz). Matched pairs were non‐targets and required no overt responses; unmatched pairs were targets that participants noted by briefly elevating their left index finger. The illustrated epoch shows two target trials followed by one non‐target trial and was analyzed as a target epoch. C,D: Expanded views of displacement signals for 25‐ and 100‐Hz vibrations recorded during a scan session. Amplitudes of the two frequencies were adjusted to create equal subjective intensities.

Figure 4

Individual participant z‐score maps showing activity in posterior occipital cortex. Coronal sections (in Talairach atlas space) [Talairach and Tournoux,1988] for each participant were selected to show the maximum activity in or near V1. Participant labels cross‐reference to demographic characteristics listed in Table I (early blind, EB; late blind, LB; sighted, NS).

Figure 2

Average z‐score maps for positive BOLD responses by group (early blind, EB; late blind, LB; sighted, NS) for non‐target epochs are shown overlying inflated canonical hemispheres and flat maps of visual cortex (description and methods for creating flat maps can be found in Drury et al. [1996], Van Essen et al. [1998,2001], and Van Essen [2004]. Borders and labeling of visual areas are from prior identifications in sighted people [Hadjikhani et al.,1998; Tootell et al.,1996,1997,1998; Van Essen,2002a,2004]. LOC: lateral occipital complex; MT: medial temporal area; OP/SMGi: parietal operculum/ inferior supramarginal gyrus; S1: primary somatosensory area; SMGs: superior supramarginal gyrus; V1d, V1v: dorsal and ventral primary visual areas; V2d, V2v: dorsal and ventral second visual areas; V3, V3A: third visual areas; V4v: ventral fourth visual area; VP: ventral posterior visual area; V7: seventh visual area; V8: eighth visual area.

Figure 5

Selected coronal sections (in Talairach atlas space) [Talairach and Tournoux,1988] and flat maps through visual cortex regions identified from the effects of time (top) and time‐by‐group (bottom) factors in a voxel‐based ANOVA. See Figure 2 for abbreviations and citations that explain flat maps. LH, left hemisphere; RH, right hemisphere.

Figure 8

Selected sagittal sections (in Talairach atlas space) [Talairach and Tournoux,1988] and flat maps through sensorimotor cortex regions identified from the effect of the time‐by‐epoch‐type factor in a voxel based ANOVA. Brodmann area (BA) borders for BA 4, 3, 1, 2, 5, and 7 taken from a canonical brain [Van Essen et al.,1998; Van Essen,2002a,b]. Regional time courses extracted for each epoch type are plotted for regions where cross‐correlation response magnitudes differed significantly between target and non‐target epochs. Plots from the left hemisphere (LH) regions are shown on the left and those from the right hemisphere (RH) regions are shown on the right in the vertical order that the regions are labeled on the brain images. OP: parietal operculum;SMGi, SMGs: inferior and superior parts of supramarginal gyrus.

Figure 6

Regional time courses extracted for each epoch type and group are plotted for regions of interest identified from the effects of the time (A) or time‐by‐group (B–H) in a voxel based ANOVA. Data at each time point show group mean and S.E.M. (early blind, EB; late blind, LB; sighted, NS). Plots from left hemisphere regions are shown in the left two columns and those from right hemisphere regions are shown in the right two columns. Each region is identified by its cortical location, visual area, and atlas coordinate location for the regional center of mass. The plots are arranged to follow the top‐to‐bottom and left‐right order of regions shown on the coronal sections in Figure 5. Cun: cuneus gyrus; FG: fusiform g; IOG: inferior occipital g; LG: lingual g; MOG: middle occipital g; SOG: superior occipital g.

Figure 3

BOLD responses during non‐target epochs in somatosensory cortex. A: Locations of analyzed S1 and OP regions in the left hemisphere are illustrated on a partially inflated canonical brain. B: Response time courses for each group (early blind, EB; late blind, LB; and sighted, NS) in S1 and bilaterally in OP. Talairach coordinates of the regional centers‐of‐mass are listed in parentheses. C: Left and right hemisphere time course cross‐correlation. Each point is one of the measurements in the time course. The axes are in average % MR signal change per voxel. D: Response magnitudes in somatosensory regions at different ages of blindness onset. Linear regression lines were fit to data from blind participants only. Results from NS are shown on the extreme right of each graph.

Figure 7

Magnitude of BOLD responses as a function of age of blindness onset in defined regions. Title for each graph identifies the anatomical location, visual area, and atlas coordinates for the centers of mass from the ANOVA effects (see Table II). Each point shows single participant mean and S.E.M. for target and non‐target epoch types.