Sensory Deprivation Independently Regulates Neocortical Feedforward and Feedback Excitation-Inhibition Ratio

SUMMARYBrief (2-3d) monocular deprivation (MD) during the critical period induces a profound loss of responsiveness within layer 4 of primary visual cortex (V1). This has largely been ascribed to long-term depression (LTD) at thalamocortical synapses onto pyramidal neurons, while a contribution from intracortical inhibition has been controversial. Here we used optogenetics to probe feedforward thalamocortical and feedback intracortical excitation-inhibition (E-I) ratios following brief MD. While thalamocortical inputs onto pyramidal neurons were depressed, there was stronger depression onto PV+ interneurons, which shifted the thalamocortical-evoked E-I ratio toward excitation. In contrast, feedback intracortical E-I ratio was shifted toward inhibition, and a computational model of layer 4 demonstrated that these opposing shifts produced an overall suppression of layer 4 excitability. Thus, feedforward and feedback E-I ratios onto the same postsynaptic target can be independently regulated by visual experience, and enhanced feedback inhibition is the primary driving force behind loss of visual responsiveness.

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Sensory experience inversely regulates feedforward and feedback excitation-inhibition ratio in rodent visual cortex

eLife ◽

10.7554/elife.38846 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 20

Author(s):

Nathaniel J Miska ◽

Leonidas MA Richter ◽

Brian A Cary ◽

Julijana Gjorgjieva ◽

Gina G Turrigiano

Keyword(s):

Visual Cortex ◽

Driving Force ◽

Critical Period ◽

Visual Experience ◽

Feedback Inhibition ◽

Intracortical Inhibition ◽

Monocular Deprivation ◽

Long Term Depression ◽

Layer 4

Brief (2-3d) monocular deprivation (MD) during the critical period induces a profound loss of responsiveness within binocular (V1b) and monocular (V1m) regions of rodent primary visual cortex. This has largely been ascribed to long-term depression (LTD) at thalamocortical synapses, while a contribution from intracortical inhibition has been controversial. Here we used optogenetics to isolate and measure feedforward thalamocortical and feedback intracortical excitation-inhibition (E-I) ratios following brief MD. Despite depression at thalamocortical synapses, thalamocortical E-I ratio was unaffected in V1b and shifted toward excitation in V1m, indicating that thalamocortical excitation was not effectively reduced. In contrast, feedback intracortical E-I ratio was shifted toward inhibition in V1m, and a computational model demonstrated that these opposing shifts produced an overall suppression of layer 4 excitability. Thus, feedforward and feedback E-I ratios can be independently tuned by visual experience, and enhanced feedback inhibition is the primary driving force behind loss of visual responsiveness.

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Long-term Monocular Deprivation during Juvenile Critical Period Disrupts Binocular Integration in Mouse Visual Thalamus

Journal of Neuroscience ◽

10.1523/jneurosci.1626-19.2019 ◽

2019 ◽

Vol 40 (3) ◽

pp. 585-604 ◽

Cited By ~ 5

Author(s):

Carey Y.L. Huh ◽

Karim Abdelaal ◽

Kirstie J. Salinas ◽

Diyue Gu ◽

Jack Zeitoun ◽

...

Keyword(s):

Critical Period ◽

Monocular Deprivation ◽

Visual Thalamus

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Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1319571110 ◽

2013 ◽

Vol 110 (47) ◽

pp. E4540-E4547 ◽

Cited By ~ 19

Author(s):

S. Lefort ◽

A. C. Gray ◽

G. G. Turrigiano

Keyword(s):

Critical Period ◽

Cortical Layer ◽

Layer 4 ◽

Inhibitory Plasticity ◽

Visual Cortical

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Visual Experience Is Necessary for Maintenance But Not Development of Receptive Fields in Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.00166.2005 ◽

2005 ◽

Vol 94 (3) ◽

pp. 1962-1970 ◽

Cited By ~ 32

Author(s):

M. M. Carrasco ◽

K. A. Razak ◽

S. L. Pallas

Keyword(s):

Superior Colliculus ◽

Critical Period ◽

Visual Experience ◽

Sensory Deprivation ◽

Receptive Fields ◽

Visual Deprivation ◽

Visual Development ◽

Retinotopic Maps ◽

Nmda Receptor Blockade ◽

Dark Rearing

Sensory deprivation is thought to have an adverse effect on visual development and to prolong the critical period for plasticity. Once the animal reaches adulthood, however, synaptic connectivity is understood to be largely stable. We reported previously that N-methyl-d-aspartate (NMDA) receptor blockade in the superior colliculus of the Syrian hamster prevents refinement of receptive fields (RFs) in normal or compressed retinotopic projections, resulting in target neurons with enlarged RFs but normal stimulus tuning. Here we asked whether visually driven activity is necessary for refinement or maintenance of retinotopic maps or if spontaneous activity is sufficient. Animals were deprived of light either in adulthood only or from birth until the time of recording. We found that dark rearing from birth to 2 mo of age had no effect on the timing and extent of RF refinement as assessed with single unit extracellular recordings. Visual deprivation in adulthood also had no effect. Continuous dark rearing from birth into adulthood, however, resulted in a progressive loss of refinement, resulting in enlarged, asymmetric receptive fields and altered surround suppression in adulthood. Thus unlike in visual cortex, early visually driven activity is not necessary for refinement of receptive fields during development, but is required to maintain refined visual projections in adulthood. Because the map can refine normally in the dark, these results argue against a deprivation-induced delay in critical period closure, and suggest instead that early visual deprivation leaves target neurons more vulnerable to deprivation that continues after refinement.

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Age-Dependent Decline in Supragranular Long-Term Synaptic Plasticity by Increased Inhibition During the Critical Period in the Rat Primary Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.90900.2008 ◽

2009 ◽

Vol 101 (1) ◽

pp. 269-275 ◽

Cited By ~ 19

Author(s):

Hyun-Jong Jang ◽

Kwang-Hyun Cho ◽

Hyun-Sok Kim ◽

Sang June Hahn ◽

Myung-Suk Kim ◽

...

Keyword(s):

Synaptic Plasticity ◽

Visual Cortex ◽

Primary Visual Cortex ◽

Critical Period ◽

Excitatory Postsynaptic Potential ◽

Age Dependent ◽

Layer 4 ◽

Old Rats ◽

Synaptic Model

Supragranular long-term potentiation (LTP) and depression (LTD) are continuously induced in the pathway from layer 4 during the critical period in the rodent primary visual cortex, which limits the use of supragranular long-term synaptic plasticity as a synaptic model for the mechanism of ocular dominance (OD) plasticity. The results of the present study demonstrate that the pulse duration of extracellular stimulation to evoke a field potential (FP) is critical to induction of LTP and LTD in this pathway. LTP and LTD were induced in the pathway from layer 4 to layer 2/3 in slices from 3-wk-old rats when FPs were evoked by 0.1- and 0.2-ms pulses. LTP and LTD were induced in slices from 5-wk-old rats when evoked by stimulation with a 0.2-ms pulse but not by stimulation with a 0.1-ms pulse. Both the inhibitory component of FP and the inhibitory/excitatory postsynaptic potential amplitude ratio evoked by stimulation with a 0.1-ms pulse were greater than the values elicited by a 0.2-ms pulse. Stimulation with a 0.1-ms pulse at various intensities that showed the similar inhibitory FP component with the 0.2-ms pulse induced both LTD and LTP in 5-wk-old rats. Thus extracellular stimulation with shorter-duration pulses at higher intensity resulted in greater inhibition than that observed with longer-duration pulses at low intensity. This increased inhibition might be involved in the age-dependent decline of synaptic plasticity during the critical period. These results provide an alternative synaptic model for the mechanism of OD plasticity.

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Effects of monocular deprivation on the development of visual inhibitory interactions in kittens

Visual Neuroscience ◽

10.1017/s095252380000482x ◽

1991 ◽

Vol 7 (4) ◽

pp. 335-343 ◽

Cited By ~ 5

Author(s):

Harriet D. Speed ◽

M. Concetta Morrone ◽

David C. Burr

Keyword(s):

Visual Evoked Potential ◽

Evoked Potential ◽

Visual Experience ◽

Monocular Deprivation ◽

Response Curves ◽

Short And Long Term ◽

The Right ◽

Contrast Response ◽

Inhibitory Interactions

AbstractA visual-evoked-potential (VEP) masking technique was used to assess the effects of short- and long-term monocular deprivation on the development of visual inhibitory interactions in kittens. VEP contrast-response curves were recorded in response to contrast-reversed sinusoidal gratings, both with and without superimposed high-contrast masks. The contrast-response curves measured from the nondeprived eye were similar to those of normal cats: with no mask VEP amplitudes increase with contrast up to saturation at about 10% contrast; parallel masks shift the curves to the right, decreasing thresholds; and orthogonal masks decrease the slope of the contrast-response curves without affecting thresholds. After monocular deprivation (either brief or extensive), the contrast-response curves without mask did not show the typical response saturation, and neither parallel nor orthogonal mask had any effect on the contrast-response curves. The masking effects did not return after 100 days of normal vision, although contrast sensitivity and acuity recovered to about half of the normal levels during that period. The results indicate that the inhibitory intracortical circuitry that mediates the orientation-dependent masking effects are highly vulnerable to visual experience.

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

Journal of Neurophysiology ◽

10.1152/jn.00266.2004 ◽

2004 ◽

Vol 92 (4) ◽

pp. 2113-2121 ◽

Cited By ~ 44

Author(s):

David S. Liao ◽

Thomas E. Krahe ◽

Glen T. Prusky ◽

Alexandre E. Medina ◽

Ary S. Ramoa

Keyword(s):

Binocular Vision ◽

Neural Plasticity ◽

Critical Period ◽

Visual Experience ◽

Ocular Dominance ◽

Orientation Selectivity ◽

Monocular Deprivation ◽

Ocular Dominance Plasticity ◽

Single Unit Recordings ◽

Normal Binocular Vision

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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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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