Harold Burton

Reading Braille activates visual cortex in blind people [Burton et al., J Neurophysiol 2002;87:589–611; Sadato et al., Nature 1996;380:526–528; Sadato et al., Brain 1998;121:1213–1229]. Because learning Braille requires extensive training, we had sighted and blind people read raised block capital letters to determine whether all groups engage visual cortex similarly when reading by touch. Letters were passively rubbed across the right index finger at 30 mm/s using an MR‐compatible drum stimulator. Age‐matched sighted, early blind (lost sight 0–5 years), and late blind (lost sight >5.5 years) volunteers performed three tasks: stating an identified letter, stating a verb containing an identified letter, and feeling a moving smooth surface. Responses were voiced immediately after the drum stopped moving across the fingertip. All groups showed increased activity in visual areas V1 and V2 during both letter identification tasks. Blind compared to sighted participants showed greater activation increases predominantly in the parafoveal‐peripheral portions of visuotopic areas and posterior parts of BA 20 and 37. Sighted participants showed suppressed activity in most of the same areas except for small positive responses bilaterally in V1, left V5/MT+, and bilaterally in BA 37/20. Blind individuals showed suppression of the language areas in the frontal cortex, while sighted individuals showed slight positive responses. Early blind showed a more extensive distribution of activity in superior temporal sulcal multisensory areas. These results show cross‐modal reorganization of visual cortex and altered response dynamics in nonvisual areas that plausibly reflect mechanisms for adaptive plasticity in blindness. Hum Brain Mapp, 2005.

We studied whether default functionality of the human brain, as revealed by task-independent decreases in activity occurring during goal-directed behaviors, is functionally reorganized by blindness. Three groups of otherwise normal adults were studied: early blind, adventitiously blind, and normally sighted. They were imaged by using functional MRI during performance of a word association task (verb generation to nouns) administered by using auditory stimuli in all groups and Braille reading in blind participants. In sighted people, this task normally produces robust task-independent decreases relative to a baseline of quiet wakefulness with eyes closed. Our functional MRI results indicate that task-independent decreases are qualitatively similar across all participant groups in medial and dorsal prefrontal, lateral parietal, anterior precuneus, and posterior cingulate cortices. Similarities in task-independent decreases are consistent with the hypothesis that functional reorganization resulting from the absence of a particular sensory modality does not qualitatively affect default functionality as revealed by task-independent decreases. More generally, these results support the notion that the brain largely operates intrinsically, with sensory information modulating rather than determining system operations.

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. Hum. Brain Mapp. 23:210–228, 2004.

Brain imaging studies describe visual cortex activity in blind people during nonvisual tasks such as Braille reading, hearing words, or sensory discriminations of tactile or auditory stimuli [for literature citations see Burton et al. ([2002a][1],[b][2]) and Sadato et al. ([2002][3])]. Simply stated

The functional organization of somatosensory and motor cortex was investigated in an individual with a high cervical spinal cord injury, a 5-year absence of nearly all sensory/motor function at and below the shoulders, and rare recovery of some function in years 6–8 after intense and sustained rehabilitation therapies. We used functional magnetic resonance imaging to study brain activity to vibratory stimulation and voluntary movements of body parts above and below the lesion. No response to vibratory stimulation of the hand was observed in the primary somatosensory cortex (SI) hand area, which was conversely recruited during tongue movements that normally evoke responses only in the more lateral face area. This result suggests SI reorganization analogous to previously reported neuroplasticity changes after peripheral lesions in animals and humans. In striking contradistinction, vibratory stimulation of the foot evoked topographically appropriate responses in SI and second somatosensory cortex (SII). Motor cortex responses, tied to a visuomotor tracking task, displayed a near-typical topography, although they were more widespread in premotor regions. These findings suggest possible preservation of motor and some somatosensory cortical representations in the absence of overt movements or conscious sensations for several years after spinal cord injury and have implications for future rehabilitation and neural-repair therapies.

Literacy for blind people requires learning Braille. Along with others, we have shown that reading Braille activates visual cortex. This includes striate cortex (V1), i.e., banks of calcarine sulcus, and several higher visual areas in lingual, fusiform, cuneus, lateral occipital, inferior temporal, and middle temporal gyri. The spatial extent and magnitude of magnetic resonance (MR) signals in visual cortex is greatest for those who became blind early in life. Individuals who lost sight as adults, and subsequently learned Braille, still exhibited activity in some of the same visual cortex regions, especially V1. These findings suggest these visual cortex regions become adapted to processing tactile information and that this cross-modal neural change might support Braille literacy. Here we tested the alternative hypothesis that these regions directly respond to linguistic aspects of a task. Accordingly, language task performance by blind persons should activate the same visual cortex regions regardless of input modality. Specifically, visual cortex activity in blind people ought to arise during a language task involving heard words. Eight early blind, six late blind, and eight sighted subjects were studied using functional magnetic resonance imaging (fMRI) during covert generation of verbs to heard nouns. The control task was passive listening to indecipherable sounds (reverse words) matched to the nouns in sound intensity, duration, and spectral content. Functional responses were analyzed at the level of individual subjects using methods based on the general linear model and at the group level, using voxel based ANOVA and t-test analyses. Blind and sighted subjects showed comparable activation of language areas in left inferior frontal, dorsolateral prefrontal, and left posterior superior temporal gyri. The main distinction was bilateral, left dominant activation of the same visual cortex regions previously noted with Braille reading in all blind subjects. The spatial extent and magnitude of responses was greatest on the left in early blind individuals. Responses in the late blind group mostly were confined to V1 and nearby portions of the lingual and fusiform gyri. These results confirm the presence of adaptations in visual cortex of blind people but argue against the notion that this activity during Braille reading represents somatosensory (haptic) processing. Rather, we suggest that these responses can be most parsimoniously explained in terms of linguistic operations. It remains possible that these responses represent adaptations which initially are for processing either sound or touch, but which are later generalized to the other modality during acquisition of Braille reading skills.

Braille reading depends on remarkable adaptations that connect the somatosensory system to language. We hypothesized that the pattern of cortical activations in blind individuals reading Braille would reflect these adaptations. Activations in visual (occipital-temporal), frontal-language, and somatosensory cortex in blind individuals reading Braille were examined for evidence of differences relative to previously reported studies of sighted subjects reading print or receiving tactile stimulation. Nine congenitally blind and seven late-onset blind subjects were studied with fMRI as they covertly performed verb generation in response to reading Braille embossed nouns. The control task was reading the nonlexical Braille string “######”. This study emphasized image analysis in individual subjects rather than pooled data. Group differences were examined by comparing magnitudes and spatial extent of activated regions first determined to be significant using the general linear model. The major adaptive change was robust activation of visual cortex despite the complete absence of vision in all subjects. This included foci in peri-calcarine, lingual, cuneus and fusiform cortex, and in the lateral and superior occipital gyri encompassing primary (V1), secondary (V2), and higher tier (VP, V4v, LO and possibly V3A) visual areas previously identified in sighted subjects. Subjects who never had vision differed from late blind subjects in showing even greater activity in occipital-temporal cortex, provisionally corresponding to V5/MT and V8. In addition, the early blind had stronger activation of occipital cortex located contralateral to the hand used for reading Braille. Responses in frontal and parietal cortex were nearly identical in both subject groups. There was no evidence of modifications in frontal cortex language areas (inferior frontal gyrus and dorsolateral prefrontal cortex). Surprisingly, there was also no evidence of an adaptive expansion of the somatosensory or primary motor cortex dedicated to the Braille reading finger(s). Lack of evidence for an expected enlargement of the somatosensory representation may have resulted from balanced tactile stimulation and gross motor demands during Braille reading of nouns and the control fields. Extensive engagement of visual cortex without vision is discussed in reference to the special demands of Braille reading. It is argued that these responses may represent critical language processing mechanisms normally present in visual cortex.

Clinical and neuroimaging observations of the cortical network implicated in tactile attention have identified foci in parietal somatosensory, posterior parietal, and superior frontal locations. Tasks involving intentional hand-arm movements activate similar or nearby parietal and frontal foci. Visual spatial attention tasks and deliberate visuomotor behavior also activate overlapping posterior parietal and frontal foci. Studies in the visual and somatosensory systems thus support a proposal that attention to the spatial location of an object engages cortical regions responsible for the same coordinate referents used for guiding purposeful motor behavior. Tactile attention also biases processing in the somatosensory cortex through amplification of responses to relevant features of selected stimuli. Psychophysical studies demonstrate retention gradients for tactile stimuli like those reported for visual and auditory stimuli, and suggest analogous neural mechanisms for working memory across modalities. Neuroimaging studies in humans using memory tasks, and anatomic studies in monkeys support the idea that tactile information relayed from the somatosensory cortex is directed ventrally through the insula to the frontal cortex for short-term retention and to structures of the medial temporal lobe for long-term encoding. At the level of single neurons, tactile (such as visual and auditory) short-term memory appears as a persistent response during delay intervals between sampled stimuli.

Neuronal responses in somatosensory cortical areas 3b and 1- 2 (S1) were recorded during an attention task involving cue directed selection of one of three simultaneous stimuli: dual sinewave shaped vibrotactile stimuli applied to mirror sites on both hands or a similarly timed auditory tone. The cued stimulus occurred with one of two equally probable patterns: a constant amplitude vibration or the latter with a superimposed brief sinewave amplitude pulse midway during stimulation. Uncued stimuli always contained amplitude pulses. Two monkeys signaled the absence or presence of an amplitude pulse by appropriately moving a foot pedal up or down. Cues initiated trials by marking the location where the monkey had to discriminate the stimulus pattern. Cue location and stimulus pattern varied randomly per trial. Approximately 50% of cells (44/77 in 3b and 39/77 in 1- 2) had significantly different firing rates to stimulation cued to the contralateral hand relative to spatially cuing the ipsilateral hand or cross-modally the auditory stimulus. Relatively suppressed firing rates during times prior to the epoch containing amplitude pulses improved signal-to-noise ratios for responses to amplitude pulses. Instances of significant enhanced activity during and after intervals with amplitude pulses were rare and relative to suppressed activity when cues directed attention to the ipsilateral hand or auditory stimulus. The present findings suggest that attention influences even the earliest stage somatosensory cortical processing. Findings were more modest in S1 than those previously seen in S2 (Burton et al. , Somatosens Mot Res 14 : 237-267, 1997), which supports the concept of multistage attention processes for touch.