UCI P 140C - Cortical plasticity associated with Braille learning

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In 1688, the Irish philosopher William Molyneux posed aquestion in a letter to John Locke that would capture the at-tention of cognitive psychologists and philosophers of mindfor more than three centuries. Probably motivated to somedegree by the fact that his own wife was blind, he asked hisEnglish contemporary to imagine that a congenitally blindperson had learned to distinguish between and name asphere and a cube by touch alone, and then to imagine thatthis person had suddenly recovered the faculty of sight.Would this individual, Molyneux wondered, be able to dis-tinguish both objects by sight and to say which is the sphereand which is the cube1?Molyneux’s question served as the touchstone for 300years of debate over the role of experience in the develop-ment of perception and the existence of innate or acquiredcross-modal relationships between the senses. William James2argued that perceptions of space across different modalitieshave intrinsically different properties that make it imposs-ible for cross-modal information to be relayed between sightand touch without experience. He noted, for example, thatvisual space is projective and non-Euclidean, whereas tactilespace is Euclidean. More contemporary, experimental ap-proaches to Molyneux’s problem have included observationof surgically treated cataract patients3,4, visual deprivation inanimals5and the use of ‘sensory substitution systems’ thatrepresent visual scenes and objects tactually6; all have failedto provide unequivocal evidence with which to answerMolyneux’s 300-year-old conundrum. This review furtherexamines the relationship between visual and tactile infor-mation processing in the context of plastic cortical changesthat seem to occur in blind Braille readers.Because the processing of visual information encom-passes a significant portion of the brain, peripheral blind-ness represents a deafferentation of input to large areas ofthe cortex. Such deafferentation imposes great demands on other sensory systems to make compensatory adjust-ments in the absence of sight, particularly in the context ofour vision-dependent society. Blind individuals must de-velop the ability to extract crucial spatial information fromthe modalities of touch and hearing. One particularly complicated compensatory tactile ability acquired by manyblind individuals is Braille reading.The acquisition of Braille-reading skill also poses an interesting problem of neural logistics, because it imposes amarked increase in afferent and efferent demands onto a restricted body space (the pads of Braille-reading fingers).Blind Braille readers must discriminate, with exquisite sensi-tivity and accuracy, subtle patterns of raised and depresseddots with the pads of their fingers and translate this spatialcode into meaningful information. Faced with the complexcognitive demands of Braille reading, it appears that strikingadaptive changes occur in the human brain (Fig. 1).Enlarged somatosensory representation of braille-readingfingersEvidence from both animal and human models suggests thatsomatosensory representation of a body part can be selectivelyremodeled by new tactile experiences, and that repeated use168Cortical plasticityassociated with BraillelearningRoy H. Hamilton and Alvaro Pascual-LeoneBlind subjects who learn to read Braille must acquire the ability to extract spatialinformation from subtle tactile stimuli. In order to accomplish this, neuroplastic changesappear to take place. During Braille learning, the sensorimotor cortical area devoted to therepresentation of the reading finger enlarges. This enlargement follows a two-step processthat can be demonstrated with transcranial magnetic stimulation mapping and suggestsinitial unmasking of existing connections and eventual establishment of more stablestructural changes. In addition, Braille learning appears to be associated with therecruitment of parts of the occipital, formerly ‘visual’, cortex (V1 and V2) for tactileinformation processing. In blind, proficient Braille readers, the occipital cortex can be shownnot only to be associated with tactile Braille reading but also to be critical for readingaccuracy. Recent studies suggest the possibility of applying non-invasive neurophysiologicaltechniques to guide and improve functional outcomes of these plastic changes. Suchinterventions might provide a means of accelerating functional adjustment to blindness.R.H. Hamilton andA. Pascual-Leone areat the Laboratory forMagnetic BrainStimulation,Department ofNeurology, Beth IsraelDeaconess MedicalCenter and HarvardMedical School,Boston, MA 02215,USA.A. Pascual-Leone isalso at the Unidad deNeurobiologia,DepartimentoFisiologia,Universidad deValencia and theInstituto Cajal,Consejo Superior deInvestigacionesCientificas, Spain.tel: +1 617 667 0203fax: +1 617 975 5322e-mail: [email protected]@bidmc.harvard.eduReviewHamilton and Pascual-Leone – Cortical plasticityCopyright © 1998, Elsevier Science Ltd. All rights reserved. 1364-6613/98/$19.00 PII: S1364-6613(98)01172-3Trends in Cognitive Sciences – Vol. 2, No. 5, May 1998or stimulation of that portion of the bodycan lead to an enlarged cortical represen-tation. The work of Merzenich and col-leagues7–11using animal models suggeststhat these changes in cortical representationmight underlie changes in perception.Recanzone et al.12found that the topo-graphical and temporal response propertiesof cortical neurons of adult owl monkeyscan be altered by training them behav-iorally to discriminate the temporal fea-tures of a tactile stimulus. This findingstrongly suggests that the changes in theactivity of cortical neurons, including en-largement of cortical representation, aredirectly correlated with perceptual ability.Recording somatosensory evokedpotentials (SEPs) from the tips of thereading and non-reading index fingers ofblind Braille readers, Pascual-Leone andTorres13demonstrated that sensory rep-resentation of the reading finger is en-larged when compared with the sensoryrepresentation of the homologous fingerof their other hand, or with that of thefinger of sighted and blind non-Braille-reading controls.These results are consistent with data demonstrating en-largement of the somatosensory barrel cortex of binocularlydeprived mice14. The use of transcranial magnetic stimu-lation (TMS) to map the motor cortical areas representingthe reading fingers of blind Braille readers reveals similar enlargement15. This finding is


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