Functional connectivity between somatosensory and visual cortex in early blind humans

Crossmodal plasticity occurs when loss of input in one sensory modality leads to reorganization in brain representations of other sensory modalities. In congenital blindness the visual cortex becomes responsive to somatosensory input such as occurs during Braille reading. The route by which somatosensory information reaches the visual cortex is not known. Here, we used repetitive transcranial magnetic stimulation (rTMS) to probe the connection between primary somatosensory cortex (S1) and early visual cortex (V1 and neighboring areas), combining rTMS with positron emission tomography (PET). We applied stimulation over S1 in sighted, early blind and late blind individuals. Baseline regional cerebral blood flow in occipital cortex was highest in early blind and lowest in late blind individuals. Only the early blind group showed significant activation of early visual areas when rTMS was delivered over S1. This activation was significantly higher in early than in late blind, but not relative to sighted controls. These results are consistent with the hypothesis that tactile information may reach early visual areas in early blind humans through cortico‐cortical pathways, possibly supporting enhanced tactile information processing.

[1]  M. Daube-Witherspoon,et al.  Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H2 15O positron emission tomography: i. effects of primary motor cortex rTMS , 2003, Biological Psychiatry.

[2]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.

[3]  Manabu Honda,et al.  Critical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study , 2002, NeuroImage.

[4]  Á. Pascual-Leone,et al.  Braille character discrimination in blindfolded human subjects , 2002, Neuroreport.

[5]  Sandra M. Sanabria-Bohórquez,et al.  Occipital Activation by Pattern Recognition in the Early Blind Using Auditory Substitution for Vision , 2001, NeuroImage.

[6]  T. Hendler,et al.  Visuo-haptic object-related activation in the ventral visual pathway , 2001, Nature Neuroscience.

[7]  J. Rauschecker,et al.  A Positron Emission Tomographic Study of Auditory Localization in the Congenitally Blind , 2000, The Journal of Neuroscience.

[8]  J. Downar,et al.  A multimodal cortical network for the detection of changes in the sensory environment , 2000, Nature Neuroscience.

[9]  Scott T. Grafton,et al.  Involvement of visual cortex in tactile discrimination of orientation , 1999, Nature.

[10]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[11]  M. Hallett,et al.  Period of susceptibility for cross‐modal plasticity in the blind , 1999, Annals of neurology.

[12]  Ziad Nahas,et al.  A combined TMS/fMRI study of intensity-dependent TMS over motor cortex , 1999, Biological Psychiatry.

[13]  M. Hallett,et al.  Neural networks for Braille reading by the blind. , 1998 .

[14]  M. Hallett Human Brain Function , 1998, Trends in Neurosciences.

[15]  H. Siebner,et al.  Imaging brain activation induced by long trains of repetitive transcranial magnetic stimulation , 1998, Neuroreport.

[16]  Alan C. Evans,et al.  Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. , 1998, Journal of neurophysiology.

[17]  Scott T. Grafton,et al.  Feeling with the mind's eye , 1997, Neuroreport.

[18]  C. Ploner,et al.  Repetitive transkranielle Magnetstimulation , 1997, Der Nervenarzt.

[19]  C. Ploner,et al.  [Repetitive transcranial magnetic stimulation. Possibilities, limits and safety aspects]. , 1997, Der Nervenarzt.

[20]  M. Hallett,et al.  Functional relevance of cross-modal plasticity in blind humans , 1997, Nature.

[21]  Peter T. Fox,et al.  Imaging human intra‐cerebral connectivity by PET during TMS , 1997, Neuroreport.

[22]  Alan C. Evans,et al.  Transcranial Magnetic Stimulation during Positron Emission Tomography: A New Method for Studying Connectivity of the Human Cerebral Cortex , 1997, The Journal of Neuroscience.

[23]  R J Ilmoniemi,et al.  Electrophysiological evidence for cross-modal plasticity in humans with early- and late-onset blindness. , 1997, Psychophysiology.

[24]  F. Rösler,et al.  Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. , 1996, Brain research. Cognitive brain research.

[25]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[26]  T. Pons Novel sensations in the congenitally blind. , 1996, Nature.

[27]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[28]  J. Rauschecker,et al.  Auditory compensation for early blindness in cat cerebral cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  J. Rauschecker,et al.  Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[30]  A. Volder,et al.  Glucose utilization in human visual cortex is abnormally elevated in blindness of early onset but decreased in blindness of late onset , 1990, Brain Research.

[31]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[32]  D A Rottenberg,et al.  Accuracy of PET RCBF measurements: effect of time shift between blood and brain radioactivity curves. , 1986, Physics in medicine and biology.

[33]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[34]  L. Hyvärinen,et al.  Modification of parietal association cortex and functional blindness after binocular deprivation in young monkeys , 2004, Experimental Brain Research.

[35]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[36]  Tim Rons Novel sensations in the congenitally blind , 1996, Nature.