Critical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study

doi:10.1006/nimg.2002.1111

NeuroImage

Volume 16, Issue 2, June 2002, Pages 389-400

https://doi.org/10.1006/nimg.2002.1111 Get rights and content

Abstract

The primary visual cortex (V1) in congenitally blind humans has been shown to be involved in tactile discrimination tasks, indicating that there is a shift in function of this area of cortex, but the age dependency of the reorganization is not fully known. To investigate the reorganized network, we measured the change of regional cerebral blood flow using 3.0 Tesla functional MRI during passive tactile tasks performed by 15 blind and 8 sighted subjects. There was increased activity in the postcentral gyrus to posterior parietal cortex and decreased activity in the secondary somatosensory area in blind compared with sighted subjects during a tactile discrimination task. This suggests that there is a greater demand for shape discrimination processing in blind subjects. Blind subjects, irrespective of the age at onset of blindness, exhibited higher activity in the visual association cortex than did sighted subjects. V1 was activated in blind subjects who lost their sight before 16 years of age, whereas it was suppressed in blind subjects who lost their sight after 16 years of age during a tactile discrimination task. This suggests that the first 16 years of life represent a critical period for a functional shift of V1 from processing visual stimuli to processing tactile stimuli. Because of the age-dependency, V1 is unlikely to be the “entry node” of the cortex for the redirection of tactile signals into visual cortices after blinding. Instead, the visual association cortex may mediate the circuitry by which V1 is activated during tactile stimulation.

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Citation Excerpt :
Indeed, S has a full visual field with no evidence of a central scotoma despite the very low-resolution central vision (Cheung et al., 2009). It is possible that this preserved peripheral visual function or his age when he lost vision has prevented the foveal representation in visual cortex taking on a causal role in tactile discriminations as is clearly the case in congenitally and early-onset blind individuals (Cohen et al., 1997, 1999; Sadato et al., 2002). The finding that tactile responses in the foveal representation of S play little to no causal role in S's tactile performance on our Braille letter discrimination task offers the possibility that such cortical resources remain capable of high-resolution visual analysis even in the absence of such input from the retinogeniculate pathway (Cheung et al., 2009).
Braille reading and other tactile discrimination tasks recruit the visual cortex of both blind and normally sighted individuals undergoing short-term visual deprivation. Prior functional magnetic resonance imaging (fMRI) work in patient ‘S’, a visually impaired adult with the rare ability to read both highly magnified print visually and Braille by touch, found that foveal representations of S's visual cortex were recruited during tactile perception, whereas peripheral regions were recruited during visual perception. Here, we test the causal nature of tactile responses in the visual cortex of S by combining tactile and visual psychophysics with repetitive transcranial magnetic stimulation. First, we replicate the previous fMRI findings in S. Second, we demonstrate that transient disruption of S's foveal visual cortex has no measurable impact on S's tactile processing performance compared to that of healthy controls – a pattern not predicted by the fMRI results. Third, stimulation of foveal visual cortex maximally disrupted visual processing performance in both S and controls, suggesting the possibility of preserved visual processing within S's foveal representation. Finally, stimulation of somatosensory cortex induced the expected disruption to tactile processing performance in both S and controls. These data suggest that tactile responses in S's foveal representation reflect unmasking of latent connections between visual and somatosensory cortices and not behaviourally relevant cross-modal plasticity. Unlike studies in congenitally blind individuals, it is possible that the absence of complete visual loss in S has limited the degree of causally impactful cross-modal reorganisation.
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Regular ArticleCritical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study

Abstract

Brain Res.

Neuroimage

Neuroimage

Trends Neurosci.

Neurosci. Lett.

Neuropsychologia

Brain Res.

Brain Res.

Trend Neurosci.

Neuroimage

Brain Res.

Neurosci. Lett.

Visuo-haptic object-related activation in the ventral visual pathway

Nat. Neurosci.

Different activation patterns in the visual cortex of late and congenitally blind subjects

Brain

Multiple foci in parietal and frontal cortex activated by rubbing embossed grating patterns across fingerpads: A positron emission tomography study in humans

Cereb. Cortex

Functional relevance of cross-modal plasticity in blind humans

Nature

Period of susceptibility for cross-modal plasticity in the blind

Ann. Neurol.

Neural pathways in tactile object recognition

Neurology

An MRI-based probalistic atlas of neuroanatomy

Distributed hierarchical processing in the primate cerebral cortex

Cereb. Cortex

Testing for anatomically specified regional effects

Hum. Brain Mapp.

Assessing the significance of focal activations using their spatial extent

Hum. Brain Mapp.

Statistical parametric maps in functional imaging: A general linear approach

Hum. Brain Mapp.

Spatial registration and normalization of images

Hum. Brain Mapp.

Tactile perception in blind Braille readers: A psychophysical study of acuity and hyperacuity using gratings and dot patterns

Percept. Psychophys.

Regular Article
Critical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study