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Lack of long-term cortical reorganization after macaque retinal lesions

Abstract

Several aspects of cortical organization are thought to remain plastic into adulthood, allowing cortical sensorimotor maps to be modified continuously by experience. This dynamic nature of cortical circuitry is important for learning, as well as for repair after injury to the nervous system. Electrophysiology studies suggest that adult macaque primary visual cortex (V1) undergoes large-scale reorganization within a few months after retinal lesioning, but this issue has not been conclusively settled. Here we applied the technique of functional magnetic resonance imaging (fMRI) to detect changes in the cortical topography of macaque area V1 after binocular retinal lesions. fMRI allows non-invasive, in vivo, long-term monitoring of cortical activity with a wide field of view, sampling signals from multiple neurons per unit cortical area. We show that, in contrast with previous studies, adult macaque V1 does not approach normal responsivity during 7.5 months of follow-up after retinal lesions, and its topography does not change. Electrophysiology experiments corroborated the fMRI results. This indicates that adult macaque V1 has limited potential for reorganization in the months following retinal injury.

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Figure 1: Homonymous retinal lesions.
Figure 2: BOLD signal inside the LPZ remains at noise level and LPZ size does not change as a function of time after lesioning.
Figure 3: The profile of BOLD coherence across the LPZ border does not change as a function of time after lesioning.
Figure 4: Receptive field maps cannot be obtained and steady-state neural responses remain abnormal inside the LPZ.
Figure 5: Examples of connectivity diagrams.

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Acknowledgements

We thank J. Horton and A. Wade for comments and suggestions, and C. Riedinger, R. Esaki, I. Kim, E. Lit, J. Pauls and J. Werner for technical help. We also thank L. Vaina, B. Rosen and the members of our laboratory for their advice and support. This work received support from a National Eye Institute (NEI) grant (S.M.S.), an NEI postdoctoral fellowship grant (A.S.T.), an NEI grant to B.A.W., a Howard Hughes Medical Institute Physician Postdoctoral Fellowship (S.M.S.), a National Institute of Neurological Disorders and Stroke grant (A.A.B.), a grant from the Max Planck Society and a Deutsche Forschungsgemeinschaft grant. S.M.S. is currently also affiliated with the Athinoula Martinos Center for Biomedical Imaging, Massachusetts General Hospital, CNY-Building 149, 13th Street, Charlestown, Massachusetts 02129-2000, USA.Author Contributions S.M.S. took primary responsibility for the design and execution of all experiments, as well as for performing the analysis and preparing the manuscript. A.A.B. and M.C.S. contributed equally to this work. M.C.S. helped perform MRI experiments and analysis. A.A.B. helped with the analysis and familiarized us with the mrVISTA software. A.S.T. was intimately involved with all aspects of the work. M.A. provided technical support with the MRI experiments. A.S. provided help with the histological preparations and W.I. helped with retinal lesioning. B.A.W. and N.K.L. provided resources and acted in supervisory roles.

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Correspondence to Stelios M. Smirnakis.

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Supplementary information

Supplementary Figure S1

The BOLD signal inside the V1 lesion projection zone (LPZ) remains at noise levels and the LPZ does not shrink as a function of time post-lesion. (PPT 692 kb)

Supplementary Figure S2

The profile of raw (not normalized) BOLD coherence across the lesion projection zone border does not shift or change slope as a function of time post lesion. (PPT 422 kb)

Supplementary Figure S3

Extraclassical multi-unit firing rate transients observed in animals without lesions. (PPT 604 kb)

Supplementary Figure S4

Comparison between pre-lesion and post-lesion coherence maps inside the V1 lesion projection zone. (PPT 580 kb)

Supplementary Figure S5

Comparison between pre-lesion and post-lesion visually driven BOLD modulation strength inside the lesion projection zone. (PPT 269 kb)

Supplementary Legends

Legends to accompany the above Supplementary Figures. (DOC 35 kb)

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Smirnakis, S., Brewer, A., Schmid, M. et al. Lack of long-term cortical reorganization after macaque retinal lesions. Nature 435, 300–307 (2005). https://doi.org/10.1038/nature03495

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