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Intact hemisphere and corpus callosum compensate for visuomotor functions after early visual cortex damage

  1. Marco Tamiettoa,b,d,1
  1. aDepartment of Psychology, University of Torino, 10123 Torino, Italy;
  2. bDepartment of Medical and Clinical Psychology, Tilburg University, 5000LE Tilburg, The Netherlands;
  3. cDepartment of Cognitive Neuroscience, Maastricht University, 6229ER Maastricht, The Netherlands;
  4. dDepartment of Experimental Psychology, University of Oxford, OX1 3UD Oxford, United Kingdom;
  5. eDepartment of Neuroscience, Biomedicine and Movement Sciences, University of Verona, 37134 Verona, Italy;
  6. fNational Institute of Neuroscience, 37134 Verona, Italy
  1. Contributed by Lawrence Weiskrantz, October 12, 2017 (sent for review August 21, 2017; reviewed by Melvyn A. Goodale and Juha Silvanto)

Significance

The brain is resilient to injury and the possibility to promote recovery rests with our ability to understand the nature of postlesional plasticity. After damage to the visual cortex some patients with clinical blindness still react to unseen stimuli with appropriate motor responses, a phenomenon known as “blindsight.” Our findings in one patient with early primary visual cortex damage suggest that this nonconscious visuomotor ability depends partly on the compensatory activity of the intact hemisphere, which can be dynamically recruited through the corpus callosum. Functional interactions between the damaged and intact hemisphere are subserved by changes in the underlying anatomical connections. These observations provide a framework for future investigations of functional recovery after brain damage and on mechanisms that mediate nonconscious abilities.

Abstract

Unilateral damage to the primary visual cortex (V1) leads to clinical blindness in the opposite visual hemifield, yet nonconscious ability to transform unseen visual input into motor output can be retained, a condition known as “blindsight.” Here we combined psychophysics, functional magnetic resonance imaging, and tractography to investigate the functional and structural properties that enable the developing brain to partly overcome the effects of early V1 lesion in one blindsight patient. Visual stimuli appeared in either the intact or blind hemifield and simple responses were given with either the left or right hand, thereby creating conditions where visual input and motor output involve the same or opposite hemisphere. When the V1-damaged hemisphere was challenged by incoming visual stimuli, or controlled manual responses to these unseen stimuli, the corpus callosum (CC) dynamically recruited areas in the visual dorsal stream and premotor cortex of the intact hemisphere to compensate for altered visuomotor functions. These compensatory changes in functional brain activity were paralleled by increased connections in posterior regions of the CC, where fibers connecting homologous areas of the parietal cortex course.

Footnotes

  • ?1To whom correspondence may be addressed. Email: larry.weiskrantz{at}psy.ox.ac.uk or marco.tamietto{at}unito.it.
  • Author contributions: A.C., C.A.M., and M.T. designed research; B.d.G., C.A.M., and M.T. performed research; A.C., M.D., and M.T. analyzed data; A.C., L.W., and M.T. wrote the paper; and A.C., L.W., C.A.M., and M.T. interpreted data.

  • Reviewers: M.A.G., University of Western Ontario; and J.S., University of Westminster.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.danielhellerman.com/lookup/suppl/doi:10.1073/pnas.1714801114/-/DCSupplemental.

Online Impact

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