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  • Review Article
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Plasticity and stability of visual field maps in adult primary visual cortex

Key Points

  • Reports over the past two decades suggest that adult primary visual cortex (V1), the dominant cortical relay station distributing visual sensory input to the rest of the neocortex, reorganizes substantially following sensory deprivation. This is an important claim because it suggests that the adult visual cortex retains significant potential for plasticity that might one day be harnessed to promote recovery after injury. It also means that the rest of the neocortex must be able to update its interpretation of V1 signals.

  • We review the literature and point out several dissenting reports which suggest that adult reorganization in V1 is limited. We also describe some significant differences among the reports that claim reorganization does take place. For example, there are disputes about whether monocular or only homonymous binocular retinal lesions induce reorganization; about the effect of such lesions on receptive field size; about the time course of reorganization in response to retinal lesions; and about the extent of sub-cortical reorganization and its potential role in shaping cortical responses. We stress the need to resolve these important inconsistencies.

  • An important deficiency in the literature is that measurements are often interpreted without the guidance of quantitative theory or closely coordinated behavioural measurements. No theory has emerged that integrates the measurements obtained using different modalities, from unit recording to neuroimaging to behaviour. Such a theory is needed, is possible and should be developed.

  • Clarifying the extent of adult cortical plasticity under normal conditions, and the extent to which the cortex can be made plastic in response to injury or sensory deprivation, has implications for clinical applications and policy development. We conclude that at present the data do not support a strong position in favour of dynamic, large-scale reorganization of V1 responses. Rather, we argue that it is time to address the problem using new experimental and theoretical tools that measure, in vivo, specific cortical circuits and to understand the conditions under which specific neuronal pathways are plastic or stable.

Abstract

It is important to understand the balance between cortical plasticity and stability in various systems and across spatial scales in the adult brain. Here we review studies of adult plasticity in primary visual cortex (V1), which has a key role in distributing visual information. There are claims of plasticity at multiple spatial scales in adult V1, but a number of inconsistencies in the supporting data raise questions about the extent and nature of such plasticity. Our understanding of the extent of plasticity in V1 is further limited by a lack of quantitative models to guide the interpretation of the data. These problems limit efforts to translate research findings about adult cortical plasticity into significant clinical, educational and policy applications.

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Figure 1: Ocular dominance columns and visual field map in primary visual cortex (V1).
Figure 2: Primary visual cortex (V1) neurons receive diverse inputs.
Figure 3: No reorganization of the primary visual cortex (V1) visual field map after eye rotation.
Figure 4: Primary visual cortex (V1) responses in humans with central retinal lesions.
Figure 5: The expected effect of retinal lesions on V1 responses.

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Acknowledgements

Supported by RO1 EY03164 and EY015000 (B.W.) and the Howard Hughes Medical Institute, the Dana Foundation, R01 EY019272, Department of Defense grant PT074693P19 and R21 NS059607 (S.M.). We thank J. Farrell, R. Freeman, H. Horiguchi, J. Horton, N. Levin, N. Logothetis, C. Shatz, M. Schmid, A. Morland, A. Tolias, X. Peng and J. Winawer for comments and help with figures.

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Comparing measurements from different modalities (PDF 1780 kb)

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Glossary

Cytochrome oxidase staining

A technique that visualizes metabolically active neurons. If one eye is surgically removed from an experimental animal, cytochrome oxidase staining will selectively stain V1 neurons that receive input from the intact eye.

V1 ocular dominance columns

Most V1 neurons respond preferentially to inputs from one eye or the other. Cells with common preference are organized into columns that alternate with columns of neurons with the opposite preference.

Amblyopia

A developmental disorder of the visual nervous system. The amblyopic eye has decreased visual acuity that is not explained by structural abnormalities of the lens or retina.

Critical period

A period after birth during which neural connections have a large capacity for plasticity compared with adulthood.

GAD65-knockout mice

Mice with knockout of the gene coding for GAD65 (one of the main two glutamic acid decarboxylase isoforms). They are used to study the effects of inhibition on visual system plasticity during the critical period for ocular dominance.

Receptive field

The region in the visual field in which presentation of a stimulus influences a neuron's activity.

Fovea

A small central depression (pit) in the primate retina that has very high photoreceptor density and is used for high-acuity vision.

Scotoma

A blind spot in the visual field.

Monocular crescent

A crescent-shaped region in primate primary visual cortex that receives input from only one eye (the contralateral eye).

Area centralis

A central retinal region with relatively higher photoreceptor density that serves high-acuity vision; it exists in many species lacking a retinal fovea (pit).

Y cells

Ganglion cells in the cat retina exhibiting nonlinear spatial summation. They may be homologous to the primate parasol cells.

Parasol cells

A class of primate retinal ganglion cells identified by their large dendritic arbors. These cells comprise 10% of the retinal ganglion cells and project to the magnocellular layers of the lateral geniculate nucleus.

Visual field map

The receptive field centres of nearby neurons in visual cortex generally represent nearby positions in the visual field, forming an orderly map of at least a portion of the visual field.

Macula

The central portion of the primate retina that is covered by a yellow pigment (macular pigment). It includes the fovea.

Binocular neurons

Neurons that respond to stimulation of either eye.

Stereo-blindness

The inability to combine information from the two eyes to perceive depth. Stereo-blindness is a typical result of strabismus (eye misalignment) that was not corrected in early childhood.

Macular degeneration

A loss of vision due to disease in the central (macular) portion of the retina.

Preferred retinal locus

(PRL). When the fovea is damaged people often place the region of interest on a location in the spared peripheral part of the retina, the PRL.

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Wandell, B., Smirnakis, S. Plasticity and stability of visual field maps in adult primary visual cortex. Nat Rev Neurosci 10, 873–884 (2009). https://doi.org/10.1038/nrn2741

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