Recovery of Cortical Binocularity and Orientation Selectivity After the Critical Period for Ocular Dominance Plasticity

Cortical binocularity is abolished by monocular deprivation (MD) during a critical period of development lasting from approximately postnatal day (P) 35 to P70 in ferrets. Although this is one of the best-characterized models of neural plasticity and amblyopia, very few studies have examined the requirements for recovery of cortical binocularity and orientation selectivity of deprived eye responses. Recent studies indicating that different mechanisms regulate loss and recovery of binocularity raise the possibility that different sensitive periods characterize loss and recovery of deprived eye responses. In this report, we have examined whether the potential for recovery of binocularity and orientation selectivity is restricted to the critical period. Quantitative single unit recordings revealed recovery of cortical binocularity and full recovery of orientation selectivity of deprived eye responses following prolonged periods of MD (i.e., >3 wk) starting at P49, near the peak of plasticity. Surprisingly, recovery was present when binocular vision was restored after the end of the critical period for ocular dominance plasticity, as late as P83. In contrast, ferrets that had never received visual experience through the deprived eye failed to recover binocularity even though normal binocular vision was restored at P50, halfway through the critical period. Collectively, these results indicate that there is potential for recovery of cortical binocularity and deprived eye orientation selectivity after the end of the critical period for ocular dominance plasticity.

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Orientation Selectivity Is Reduced by Monocular Deprivation in Combination With PKA Inhibitors

Journal of Neurophysiology ◽

10.1152/jn.2002.88.4.1933 ◽

2002 ◽

Vol 88 (4) ◽

pp. 1933-1940 ◽

Cited By ~ 6

Author(s):

Chris J. Beaver ◽

Quentin S. Fischer ◽

Qinghua Ji ◽

Nigel W. Daw

Keyword(s):

Visual Cortex ◽

Protein Kinase ◽

Critical Period ◽

Ocular Dominance ◽

Receptive Fields ◽

Direction Selectivity ◽

Orientation Selectivity ◽

Monocular Deprivation ◽

Ocular Dominance Plasticity ◽

Kinase A

We have previously shown that the protein kinase A (PKA) inhibitor, 8-chloroadenosine-3′,5′–monophosphorothioate (Rp-8-Cl-cAMPS), abolishes ocular dominance plasticity in the cat visual cortex. Here we investigate the effect of this inhibitor on orientation selectivity. The inhibitor reduces orientation selectivity in monocularly deprived animals but not in normal animals. In other words, PKA inhibitors by themselves do not affect orientation selectivity, nor does monocular deprivation by itself, but monocular deprivation in combination with a PKA inhibitor does affect orientation selectivity. This result is found for the receptive fields in both deprived and nondeprived eyes. Although there is a tendency for the orientation selectivity in the nondeprived eye to be higher than the orientation selectivity in the deprived eye, the orientation selectivity in both eyes is considerably less than normal. The result is striking in animals at 4 wk of age. The effect of the monocular deprivation on orientation selectivity is reduced at 6 wk of age and absent at 9 wk of age, while the effect on ocular dominance shifts is less changed in agreement with previous results showing that the critical period for orientation/direction selectivity ends earlier than the critical period for ocular dominance. We conclude that closure of one eye in combination with inhibition of PKA reduces orientation selectivity during the period that orientation selectivity is still mutable and that the reduction in orientation selectivity is transferred to the nondeprived eye.

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Recovery from effects of brief monocular deprivation in the kitten

Journal of Neurophysiology ◽

10.1152/jn.1984.51.3.538 ◽

1984 ◽

Vol 51 (3) ◽

pp. 538-551 ◽

Cited By ~ 13

Author(s):

R. Malach ◽

R. Ebert ◽

R. C. Van Sluyters

Keyword(s):

Binocular Vision ◽

Cortical Neurons ◽

Striate Cortex ◽

Ocular Dominance ◽

Recovery Process ◽

Complete Recovery ◽

Monocular Deprivation ◽

Cortical Input ◽

Binocular Function ◽

Normal Binocular Vision

The potential for recovery from the cortical effects of monocular deprivation (MD) was studied in kittens that were briefly deprived and then exposed to various periods of normal binocular vision. In eight kittens, recordings from the hemisphere ipsilateral to the deprived eye revealed that at 4 wk of age, exposure to 12 h of MD (six 2-h sessions spread over 2 days) was sufficient to cause a massive shift in the ocular dominance of striate cortex neurons in favor of the nondeprived eye. Six of these MD kittens were allowed 3 wk of normal binocular vision and then recorded from a second time to assess the extent to which their cortex could recover from the effects of this brief period of deprivation. Data from these animals indicated that now approximately equal numbers of cortical neurons were dominated by each eye and that, while the overall level of binocularity was somewhat lower than that found in normally reared animals, the majority of cells had regained functional binocular connections. The possibility that cortical binocularity could recover even further was explored by allowing four of these six MD kittens to experience an additional 4 wk of binocular vision and then recording from them a third time. These final recordings indicated that following a total of 7 wk of binocular vision, the level of cortical binocularity was no different from that found in normally reared animals. Having demonstrated that normal binocular function can be restored to a cortex in which it had been severely disrupted, we next attempted to characterize the earliest stages of this recovery process by examining the pattern of cortical binocularity in 10 MD kittens that were allowed to experience either 6 or 12 h of binocular vision (given over 1 or 2 days, respectively). Our results indicate that, during the initial day of binocular vision, recovery seems to involve a noncompetitive expansion of functional cortical input from the deprived eye, which joins with input from the nondeprived eye in driving cortical neurons. The level of cortical binocularity continues to increase during the next day of binocular vision, but now there is also a small increase in the proportion of cells driven exclusively by the initially deprived eye--suggesting that there may be an additional competitive component to the early stages of recovery. The results of this study complement our previous report of complete recovery of binocularity following exposure to a brief period of optically induced strabismus.(ABSTRACT TRUNCATED AT 400 WORDS)

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Axonal processes and neural plasticity. III. Competition for dendrites

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1997.0183 ◽

1997 ◽

Vol 352 (1364) ◽

pp. 1975-1983 ◽

Cited By ~ 2

Author(s):

T. Elliott ◽

C. I. Howarth ◽

N. R. Shadbolt

Keyword(s):

Neural Plasticity ◽

Critical Period ◽

Ocular Dominance ◽

Dendritic Morphology ◽

Monocular Deprivation ◽

Topographic Map ◽

Cortical Cells ◽

Optic Nerve Stimulation ◽

Axonal Process ◽

Dendritic Fields

In previous work we have developed a computational framework for topographic map formation and plasticity based on axonal process sprouting and retraction, in which sprouting and retraction are governed by competition for neurotrophic support. Here we show that such an approach can account for certain aspects of the dendritic morphology of cortical maps. In particular, we model the development of ocular dominance columns in the primary visual cortex and show that cortical cells near to column boundaries prefer to elaborate dendritic fields which avoid crossing the boundaries. This emerges as different functional inputs are spatially separated. We predict that afferent segregation occurs before or simultaneously with, but not after, the emergence of dendritic bias. We predict that animals reared with complete but asynchronous stimulation of the optic nerves do not develop a dendritic bias. We suggest that the emergence of a dendritic bias might provide a partial account for the critical period for a response to monocular deprivation. In particular, we predict that animals reared with asynchronous optic nerve stimulation might exhibit an extended critical period. Our results also indicate that the number of synapses supported by cortical cells depends on the intra–ocular image correlations used in our simulations. This suggests that inter–ocular image correlations, and thus strabismic rearing of kittens, may also affect the innervation density.

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Role of visual experience in activating critical period in cat visual cortex

Journal of Neurophysiology ◽

10.1152/jn.1985.53.2.572 ◽

1985 ◽

Vol 53 (2) ◽

pp. 572-589 ◽

Cited By ~ 33

Author(s):

G. D. Mower ◽

W. G. Christen

Keyword(s):

Visual Cortex ◽

Visual Experience ◽

Ocular Dominance ◽

Orientation Selectivity ◽

Monocular Deprivation ◽

Total Darkness ◽

Cortical Cells ◽

Visual Cortical ◽

Dark Rearing ◽

Made In

Cats were reared in total darkness from birth until 4-5 mo of age (DR cats, n = 7) or with very brief visual experience (1 or 2 days) during an otherwise similar period of dark rearing [DR(1) cats, n = 3; DR(2) cats, n = 7]. Single-cell recordings were made in area 17 of visual cortex at the end of this rearing period and/or after a subsequent prolonged period of monocular deprivation. Control observations were made in normal cats (n = 3), cats reared with monocular deprivation from birth (n = 4), and cats monocularly deprived after being reared normally until 4 mo of age (n = 2). After rearing cats in total darkness, the majority of visual cortical cells were binocularly driven and the overall distribution of ocular dominance was not different from that of normal cats. Orientation-selective cells were very rare in dark-reared cats. Monocular deprivation imposed after dark rearing resulted in selective development of connections from the open eye. Most cells were responsive only to the open eye and the majority of these were orientation selective. These results were similar to, though less severe than, those found in cats reared with monocular deprivation from birth. Monocular deprivation imposed after 4 mo of normal rearing did not produce selective development of connections from the open eye in terms of either ocular dominance or orientation selectivity. In DR(1) cats visual cortical physiology was degraded in comparison to dark-reared cats after the rearing period. Most cells were binocularly driven but there was a higher frequency of unresponsive cells and a reduced frequency of orientation-selective cells. Subsequent monocular deprivation resulted in a further decrease in the number of binocularly driven cells and an increase in unresponsive cells. However, it did not produce a bias in favor of the open eye in terms of either ocular dominance or orientation selectivity. In DR(2) cats there was a high incidence of unresponsive cells and a marked loss of binocularly driven cells after the rearing period. Subsequent monocular deprivation failed to produce any significant changes.(ABSTRACT TRUNCATED AT 400 WORDS)

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Recovery of glutamatergic and GABAergic protein expression in visual cortex after monocular deprivation

10.1101/684191 ◽

2019 ◽

Author(s):

Justin L. Balsor ◽

David G. Jones ◽

Kathryn M. Murphy

Keyword(s):

Visual Cortex ◽

Protein Expression ◽

Binocular Vision ◽

Critical Period ◽

Visual Experience ◽

Monocular Deprivation ◽

The Other ◽

Synaptic Proteins ◽

Normal Expression ◽

Binocular Deprivation

AbstractA collection of glutamatergic and GABAergic proteins participate in regulating experience-dependent plasticity in the visual cortex (V1). Many studies have characterized changes to those proteins caused by monocular deprivation (MD) during the critical period (CP), but less is known about changes that occur when MD stops. We measured the effects of 3 types of visual experience after MD (n=24, 10 male and 14 female); reverse occlusion (RO), binocular deprivation (BD), or binocular vision, on the expression of synaptic proteins in V1 including glutamatergic and GABAergic receptor subunits. Synapsin expression was increased by RO but not affected by the other treatments. BD shifted the balance between glutamatergic and GABAergic receptor subunits to favor GABAAα1. In contrast, BV shifted expression to favor the glutamatergic mechanisms by increasing NMDAR and decreasing GABAAα1 subunits. None of the conditions returned normal expression levels to all of the proteins, but BV was the closest.

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Layer differences in the effect of monocular vision in light- and dark-reared kittens

Visual Neuroscience ◽

10.1017/s0952523801185147 ◽

2001 ◽

Vol 18 (5) ◽

pp. 811-820 ◽

Cited By ~ 20

Author(s):

CHRISTOPHER J. BEAVER ◽

QINGHUA JI ◽

NIGEL W. DAW

Keyword(s):

Visual Cortex ◽

Critical Period ◽

Ocular Dominance ◽

Large Change ◽

Monocular Deprivation ◽

Monocular Vision ◽

Ocular Dominance Plasticity ◽

The Difference ◽

Dark Rearing

We compared the effect of 2 days of monocular vision on the ocular dominance of cells in the visual cortex of light-reared kittens with the effect in dark-reared kittens at 6, 9, and 14 weeks of age, and analyzed the results by layer. The size of the ocular-dominance shift declined with age in all layers in light-reared animals. There was not a large change in the ocular-dominance shift with age in dark-reared animals in any layer, suggesting that dark rearing largely keeps the cortex in the immature 6-week state until 14 weeks or longer, although there was a slight decrease in layers II, III, and IV, and a slight increase in layers V and VI. At 14 weeks, the difference between light- and dark-reared animals was smallest in layer IV, larger in layers II/III, and largest in layers V/VI, suggesting that dark rearing has a large effect on intracortical synapses and a small effect on geniculocortical synapses. There was a significant ocular-dominance shift in layer IV at 14 weeks of age in both light- animals and dark-reared animals, showing that the critical period for ocular-dominance plasticity is not ended at this age. While the ocular-dominance shift after 26 h of monocular deprivation in 6-week animals was similar in light- and dark-reared animals, after 14 h it was smaller in dark-reared animals, showing that ocular-dominance changes occur more slowly in dark-reared animals at this age, in agreement with Mower (1991). Increases in selectivity for axis of movement after 26 h of monocular vision were seen in dark-reared animals at 6 weeks of age, but not at 9 or 14 weeks of age, showing that the critical period for axial selectivity ends earlier than the critical period for ocular dominance in dark-reared animals, as it does in light-reared animals.

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Enhancement of visual cortex plasticity by dark exposure

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0159 ◽

2017 ◽

Vol 372 (1715) ◽

pp. 20160159 ◽

Cited By ~ 13

Author(s):

Irina Erchova ◽

Asta Vasalauskaite ◽

Valentina Longo ◽

Frank Sengpiel

Keyword(s):

Visual Cortex ◽

Critical Period ◽

Time Course ◽

Ocular Dominance ◽

Monocular Deprivation ◽

Homeostatic Plasticity ◽

Ocular Dominance Plasticity ◽

Intrinsic Signals ◽

Significant Difference ◽

Dark Exposure

Dark rearing is known to delay the time course of the critical period for ocular dominance plasticity in the visual cortex. Recent evidence suggests that a period of dark exposure (DE) may enhance or reinstate plasticity even after closure of the critical period, mediated through modification of the excitatory–inhibitory balance and/or removal of structural brakes on plasticity. Here, we investigated the effects of a week of DE on the recovery from a month of monocular deprivation (MD) in the primary visual cortex (V1) of juvenile mice. Optical imaging of intrinsic signals revealed that ocular dominance in V1 of mice that had received DE recovered slightly more quickly than of mice that had not, but the level of recovery after three weeks was similar in both groups. Two-photon calcium imaging showed no significant difference in the recovery of orientation selectivity of excitatory neurons between the two groups. Parvalbumin-positive (PV+) interneurons exhibited a smaller ocular dominance shift during MD but again no differences in subsequent recovery. The percentage of PV+ cells surrounded by perineuronal nets, a structural brake on plasticity, was lower in mice with than those without DE. Overall, DE causes a modest enhancement of mouse visual cortex plasticity. This article is part of the themed issue ‘Integrating Hebbian and homeostatic plasticity’.

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Eye-specific voluntary attention can induce a shift of perceptual ocular dominance

10.1101/2020.08.03.233759 ◽

2020 ◽

Author(s):

Lili Lyu ◽

Qiu Han ◽

Xin He ◽

Min Bao

Keyword(s):

Neural Plasticity ◽

Ocular Dominance ◽

Recent Decade ◽

Visual Input ◽

Monocular Deprivation ◽

The Other ◽

Voluntary Attention ◽

Ocular Dominance Plasticity ◽

Visual Inputs ◽

Future Work

AbstractOcular dominance plasticity in adults has been extensively studied in the recent decade. An interocular imbalance of visual input, e.g. monocular deprivation, has been proved to markedly reshape ocular dominance. As visual attention can be eye-specific, dissimilar visual inputs from the two eyes during monocular deprivation inevitably lead attention to be more allocated to the monocular input that conveys relatively intact information. Does the imbalanced attention across the eyes also contribute to reshaping ocular dominance? Here, using a novel “backwards-movie” adaptation paradigm, we showed that prolonged attention to the input in one eye was sufficient to shift perceptual ocular dominance in favor of the unattended eye. Furthermore, the effect was stronger when eye-specific attention was directed to the dominant eye, possibly due to fewer disturbances from the other eye during the adaptation. Taken together, these findings suggest that top-down attention plays an important role in short-term ocular dominance plasticity.Statement of RelevanceAn important goal in neuroscience is to understand and take advantage of adaptive neural plasticity. Ocular dominance plasticity resulting from imbalanced visual input signals across the two eyes has been intensively investigated. By developing a novel “backwards-movie” paradigm in which movie images played normally were presented to one eye while movie images of the same episode but played backwards were presented to the other eye, the current study for the first time demonstrates the non-negligible contributions of selective attention in reshaping ocular dominance. These findings expand the homeostatic compensation theory of monocular deprivation by highlighting the contributions of feedback signals. Furthermore, our method could be applied in future work to explore new possibilities in treating adults with amblyopia.

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All-or-none disconnection of pyramidal inputs onto parvalbumin-positive interneurons gates ocular dominance plasticity

10.1101/2020.12.30.424871 ◽

2021 ◽

Author(s):

Daniel Severin ◽

Su Z. Hong ◽

Seung-Eon Roh ◽

Jiechao Zhou ◽

Michelle C. D. Bridi ◽

...

Keyword(s):

Critical Period ◽

Cortical Plasticity ◽

Classical Model ◽

Ocular Dominance ◽

Pyramidal Cells ◽

Initial Step ◽

Monocular Deprivation ◽

Ocular Dominance Plasticity ◽

Reversible Loss ◽

Underlying Mechanisms

ABSTRACTDisinhibition is an obligatory initial step in the remodeling of cortical circuits by sensory experience, yet the underlying mechanisms remain unclear. Our investigation of mechanisms for disinhibition in the classical model of ocular dominance plasticity (ODP) uncovered an unexpected novel form of experience-dependent circuit plasticity. In layer 2/3 of mouse visual cortex monocular deprivation triggers an “all-or-none” elimination of approximately half the connections from local pyramidal cells onto parvalbumin-positive interneurons (Pyr→PV), without affecting the strength of the remaining connections. This loss of Pyr→PV connections is transient, lasting one day only, has a critical period commensurate with the ODP critical period, and is contingent on a reduction of neuropentraxin2 (NPTX2), which normally stabilizes Pyr→PV connections. Bidirectional manipulations of NPTX2 functionality that prevent/promote the elimination Pyr→PV connections also promote/prevent ODP. We surmise, therefore, that this rapid and reversible loss of local Pyr→PV circuitry gates experience-dependent cortical plasticity.

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