Adult Visual Cortex—Adaptation and Reorganization

The adult visual cortex is capable of a remarkable degree of plasticity in the face of alterations of its normal pattern of input or in response to sensory adaptation or perceptual practice. This adult plasticity complements the use-dependent plasticity that plays an important role in the establishment of the normal organization during development.

Monocular Deprivation Plasticity in Adults

The shift in ocular dominance of cortical neurons as a consequence of monocular deprivation is one of the hallmarks of cortical plasticity during development. The potential for ocular dominance plasticity is greatest during a critical period of development, during which time thalamocortical axons segregate into ocular dominance columns. However, residual plasticity remains during later development even after this structural remodeling has occurred. However, later deprivation fails to induce plastic changes in ocular dominance to cortical neurons. Several lines of evidence suggest that ocular dominance plasticity can be restored to visual cortex through neuromodulators and growth factors. For example, modulation of cAMP activity through NA-beta adrenoreceptor activation, cholera A subunit, or forskolin produces a ocular dominance plasticity in adult cats that results in either a shift of ocular dominance or a reduction in binocularity. Cortical infusion of nerve growth factor, NGF, in adult cats, results in a paradoxical shift of ocular dominance toward the deprived eye.

Dark rearing tends to maintain the visual cortex in an immature, plastic state. This extended period of plasticity may be due to the prolonged expression of Cpg15, an activity-regulated gene that encodes a membrane-bound ligand that coordinates the growth of dendrites and axonal arbors and the maturation of their synapses. Normally, cpg15 levels decline during the critical period but dark-rearing results in the failure to down-regulate this gene and thus the cortex remains in a state of enhanced ability to form new synaptic connections.

Finally, the study of visual cortical development and plasticity has turned to mouse models, where despite the lack of ocular dominance segregation of thalamocortical afferents, knockouts of specific genes allows for the unprecedented ability to examine the role of receptors, ligands, and enzymes in the development and maintenance of visual cortical structure, function, and plasticity.

LTP and LTD in Visual Cortex

Adult visual cortex shows evidence for synaptic modifications in both in vitro and in vivo preparations. Tetanic stimulation of the LGN in adult rats leads to the induction of long-term potentiation (LTP) that is dependent on NMDA-receptor activation. The result is enhanced field potentials in layer 4 and deep layer 3 and increased visual evoked potentials to flash and grating stimulation. This LTP indication is paralleled by an increase in zif-268 expression in layers 2 and 3. In contrast, long-term depression, which has been hypothesized to underlie many plastic changes in development, has been inconsistently demonstrated in adult visual cortex. Consistent low-frequency stimulation (1 hertz) in cortical slices can induce LTD, but more physiologically based stimulation, based on a Poisson distribution of interpulse intervals, fails to produce LTD.

Plasticity Following Retinal and Cortical Lesions

Plastic changes in the topographic organization and receptive field properties have been reported in adult visual cortex following retinal and cortical lesions. Following binocular retinal lesions or monocular retinal lesions paired with enucleation of the other eye, researchers have observed a profound topographic reorganization of visual cortex. Immediately after the retinal lesion there is an unmasking of ectoptic receptive fields in the deafferented cortical zone. These large, unmasked receptive fields can be displaced up to fifteen degrees, reflecting the unmasking of intrinsic horizontal connections that extend up to 5 millimeters. Over the following weeks to months, the cortical scotoma becomes nearly completely driven by receptive fields arising from non-lesioned portions of the retina. This reorganization is described by a progressive shift in the topographic map into the deafferented zone. Neurons within the reorganized zone demonstrate nearly normal orientation, direction, and spatial frequency tuning. However, the contrast thresholds of cells are markedly elevated. This second phase of cortical reorganization appears due in part to the growth of new cortical connections into the deafferented zone.

Retinal lesions in adults lead to a wide range of biochemical changes in the deafferented cortex. The growth factors BDNF, NT-3, and NGF are elevated from three days to two years post-lesion. Neurotrophin receptors p75, TrkB, and TrkC increase. The expression of CREB, CaMKII, and MAP2 are also increased. In contrast, zif268 is decreased at twenty hours and recovered by thirteen months, while synaptophysin and GAP-43 increased at six months post-lesion. Neurotransmitters also show changes in the deafferented zone. GABA and glutamic acid decarboxylase levels decrease within the deafferented zone while glutamate levels increase initially along the edge of the deafferented zone and this peak progressively shifts into the deafferented zone.

Similar to the plasticity evoked by retinal lesions in adults, a temporary artificial scotoma produces rapid increases in receptive field sizes of neurons along the border of the scotoma. Receptive fields increase nearly twofold in width during the scotoma and rapidly return to normal following removal of the scotoma. Similar results have been observed in areas V2 and V3 of macaque monkeys and may be relatedto perceptual filling-in and color-constancy phenomena.

There is evidence for functional reorganization after cortical lesions. In patients suffering from visual field defects due to cortical lesions, intensive visual training can lead to shrinkage of the scotoma. This phenomenon suggests that cortical tissue adjacent to the zone of destruction can recover functions in a use-dependent manner. Such an interpretation is supported by studies of cortical lesions in adult cats. Restricted lesions of visual cortex lead to plastic changes in visual field topography. Immediately after a cortical lesion, there is little if any change in visual topography, but there is some change in spontaneous activity and excitability of cells surrounding the lesion. Within two to three months, cells within this border region develop significantly larger receptive fields that result in a partial filling in of the cortical scotoma. This increase in RF size is limited to three to four degrees, which is approximately the same dimension reported for shifts in human cortical scotomas following extensive computer-based visual field training. In addition, there is functional MRI evidence for topographic reorganization extrastriate cortical areas following restricted lesions of primary visual cortex in adult humans.

Adaptation and Perceptual Learning

The perceptual phenomenon of adaptation aftereffects suggests the possibility of use-dependent and long-lasting (minutes to hours) modifications of responsiveness of feature-specific neurons in the visual cortex. Prolonged exposure to patterned stimuli leads to a feature-specific elevation of perceptual thresholds that lasts several minutes. Such adaptation has been shown for the movement and the orientation of contours, for the spatial frequency of gratings, and for color contrast. A related and very long-lasting (up to twenty-four hours) adaptation phenomenon is the McCulloch effect. After exposure to colored gratings of different orientation, black and white gratings appear to a subject to be tinted in complementary colors that remain associated with the respective orientations of the gratings. All these adaptation aftereffects show interocular transfer, indicating that adaptation has occurred at the cortical level. Recordings from single cells support the idea that adaptation occurs in visual cortex. Optical and single cell recordings in cat visual cortex demonstrate that adaptation to a given orientation produces a repulsive shift in the orientation tuning of single cells. This phenomenon is most pronounced at orientation singularities in visual cortex where the representations of the full range of orientations are brought into close physical proximity.

Perceptual learning refers to the increase in performance in discrimination tasks that results from practice. In general, this enhanced performance shows interocular transfer and is specific for the topographic location and specific stimulus features of the practiced task. These results have been interpreted as enhanced performance by task-specific cortical modules that receive retintopic input and learn to solve a task after a short training phase.

In conclusion, behavioral, electrophysiological, and morphological evidence confirms the persistence of use-dependent plasticity in the striate cortex of adult mammals and humans. Furthermore, twenty-first century research has begun to uncover the biochemical mechanisms that support this cortical plasticity. This evidence supports the notion that adaptivity is a constituent property of cortical networks.

See also:GLUTAMATE RECEPTORS AND THEIR CHARACTERIZATION; GUIDE TO THE ANATOMY OF THE BRAIN: CEREBRAL CORTEX; LONG-TERM DEPRESSION IN THE CEREBELLUM, HIPPOCAMPUS, AND NEOCORTEX;LONG-TERM POTENTIATION; SECOND MESSENGER SYSTEMS

Bibliography

Chino, Y., Smith, E. L., Whang, B., Matsuura, K., Mori, T., and Kaas, J. H. (2001). Recovery of binocular responses by cortical neurons after early monocular lesions. Nature Neuroscience 4, 689-690.

Crist, R. E., Li, W., and Gilbert, C. D. (2001). Learning to see: Experience and attention in primary visual cortex. Nature Neuroscience 4, 519-525.

Galuske, R. A., Kim, D-S., Castren, E., and Singer, W. (2000). Differential effects of neurotrophins on ocular dominance plasticity in developing and adult cat visual cortex. European Journal of Neuroscience 12, 3,315-3,330.

Gilbert, C. D. (1998). Adult cortical dynamics. Physiological Reviews 78, 467-485.

Heynen, A. J., and Bear, M. F. (2001). Long-term potentiation of thalamocortical transmission in adult visual cortex in vivo. Journal of Neuroscience 21, 9,801-9,813.

Imamura, K., Kasamatsu, T., Shirokawa, T., and Ohashi, T. (1999). Restoration of ocular dominance plasticity mediated by adenosine 3',5'-monophosphate in adult visual cortex. Proceedings of the Royal Society of London 266, 1,507-1,516.

Kirkwood, A., Lee, H-K., and Bear, M. (1995). Co-regulation of long-term potentiation and experience-dependent plasticity in visual cortex by age and experience. Nature 375, 328-331.

Nedivi, E., and Lee, W-C. A. (2002). Extended plasticity of visual cortex in dark-reared animals may result from prolonged expression of cpg15-like genes. Journal of Neuroscience 22, 1,807-1,815.

Obata, S., Obata, J., Das, A., and Gilbert, C. D. (1999). Molecular correlates of topographic reorganization in primary visual cortex following retinal lesions. Cerebral Cortex 9, 238-248.

Daniel J.Felleman