V1 projection zone signals in human macular degeneration depend on task, not stimulus.

We used functional magnetic resonance imaging to assess abnormal cortical signals in humans with juvenile macular degeneration (JMD). These signals have been interpreted as indicating large-scale cortical reorganization. Subjects viewed a stimulus passively or performed a task; the task was either related or unrelated to the stimulus. During passive viewing, or while performing tasks unrelated to the stimulus, there were large unresponsive V1 regions. These regions included the foveal projection zone, and we refer to them as the lesion projection zone (LPZ). In 3 JMD subjects, we observed highly significant responses in the LPZ while they performed stimulus-related judgments. In control subjects, where we presented the stimulus only within the peripheral visual field, there was no V1 response in the foveal projection zone in any condition. The difference between JMD and control responses can be explained by hypotheses that have very different implications for V1 reorganization. In controls retinal afferents carry signals indicating the presence of a uniform (zero-contrast) region of the visual field. Deletion of retinal input may 1) spur the formation of new cortical pathways that carry task-dependent signals (reorganization), or 2) unmask preexisting task-dependent cortical signals that ordinarily are suppressed by the deleted signals (no reorganization).

[1]  S. Coren,et al.  The dominant eye. , 1976, Psychological bulletin.

[2]  E. G. Jones.  Cerebral Cortex , 1987, Cerebral Cortex.

[3]  S. Shipp,et al.  The functional logic of cortical connections , 1988, Nature.

[4]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[5]  J. Kaas,et al.  Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina , 1992, Vision Research.

[6]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[7]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

[8]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[9]  C. Gilbert,et al.  Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  C. Gilbert,et al.  Spatial integration and cortical dynamics. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[12]  Guillermo Sapiro,et al.  Creating connected representations of cortical gray matter for functional MRI visualization , 1997, IEEE Transactions on Medical Imaging.

[13]  H. Komatsu,et al.  Perceptual filling-in at the scotoma following a monocular retinal lesion in the monkey , 1997, Visual Neuroscience.

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

[15]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[16]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[17]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[18]  J. Horton,et al.  Monocular Core Zones and Binocular Border Strips in Primate Striate Cortex Revealed by the Contrasting Effects of Enucleation, Eyelid Suture, and Retinal Laser Lesions on Cytochrome Oxidase Activity , 1998, The Journal of Neuroscience.

[19]  C. Gilbert.  Adult cortical dynamics. , 1998, Physiological reviews.

[20]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

[21]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[22]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G H Glover,et al.  Simple analytic spiral K‐space algorithm , 1999, Magnetic resonance in medicine.

[24]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J B Poline,et al.  Transient Activity in the Human Calcarine Cortex During Visual-Mental Imagery: An Event-Related fMRI Study , 2000, Journal of Cognitive Neuroscience.

[26]  D. Heeger,et al.  Task-related modulation of visual cortex. , 2000, Journal of neurophysiology.

[27]  B. Wandell,et al.  Visualization and Measurement of the Cortical Surface , 2000, Journal of Cognitive Neuroscience.

[28]  D J Heeger,et al.  Robust multiresolution alignment of MRI brain volumes , 2000, Magnetic resonance in medicine.

[29]  B. Wandell,et al.  Abnormal retinotopic representations in human visual cortex revealed by fMRI. , 2001, Acta psychologica.

[30]  T. Dryja,et al.  Understanding the etiology of Stargardt's disease. , 2002, Ophthalmology clinics of North America.

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

[32]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[33]  J. Kaas.  Sensory loss and cortical reorganization in mature primates. , 2002, Progress in brain research.

[34]  Herbert Jägle,et al.  Reorganization of human cortical maps caused by inherited photoreceptor abnormalities , 2002, Nature Neuroscience.

[35]  L. Scullica,et al.  Diagnosis and classification of macular degenerations: an approach based on retinal function testing , 2001, Documenta Ophthalmologica.

[36]  Guillaume Flandin,et al.  Retinotopic organization of visual mental images as revealed by functional magnetic resonance imaging. , 2004, Brain research. Cognitive brain research.

[37]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[38]  Taosheng Liu,et al.  Retinotopic mapping of the visual cortex using functional magnetic resonance imaging in a patient with central scotomas from atrophic macular degeneration. , 2004, Ophthalmology.

[39]  N. Kanwisher,et al.  Reorganization of Visual Processing in Macular Degeneration , 2005, The Journal of Neuroscience.

[40]  S. Kosslyn,et al.  Visual mental imagery induces retinotopically organized activation of early visual areas. , 2005, Cerebral cortex.

[41]  N. Logothetis,et al.  Lack of long-term cortical reorganization after macaque retinal lesions , 2005, Nature.

[42]  B. Wandell,et al.  Specializations for Chromatic and Temporal Signals in Human Visual Cortex , 2005, Journal of Neuroscience.

[43]  U. Eysel,et al.  Dynamics and specificity of cortical map reorganization after retinal lesions. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[45]  Karl J. Friston,et al.  Extra-classical receptive field effects measured in striate cortex with fMRI , 2007, NeuroImage.

[46]  Brian N. Pasley,et al.  Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex , 2007, NeuroImage.

[47]  C. Hamel,et al.  Orphanet Journal of Rare Diseases BioMed Central Review , 2006 .