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

eLife ◽  
2018 ◽  
Vol 7 ◽  
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.

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

2018 ◽  
Author(s):  
Nathaniel J. Miska ◽  
Leonidas M.A. Richter ◽  
Brian A. Cary ◽  
Julijana Gjorgjieva ◽  
Gina G. Turrigiano
Keyword(s):  
Critical Period ◽  
Visual Experience ◽  
Pyramidal Neurons ◽  
Feedback Inhibition ◽  
Sensory Deprivation ◽  
Intracortical Inhibition ◽  
Monocular Deprivation ◽  
Layer 4 ◽  
Postsynaptic Target

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.

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

2009 ◽  
Vol 101 (1) ◽  
pp. 269-275 ◽  
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.

Monocular deprivation induces homosynaptic long-term depression in visual cortex

Nature ◽  
10.1038/16922 ◽  
1999 ◽  
Vol 397 (6717) ◽  
pp. 347-350 ◽  
Author(s):  
Cynthia D. Rittenhouse ◽  
Harel Z. Shouval ◽  
Michael A. Paradiso ◽  
Mark F. Bear
Keyword(s):  
Visual Cortex ◽  
Monocular Deprivation ◽  
Long Term Depression

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

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.

scholarly journals Adult visual experience promotes recovery of primary visual cortex from long-term monocular deprivation

2007 ◽  
Vol 14 (9) ◽  
pp. 573-580 ◽  
Author(s):  
Q. S. Fischer ◽  
S. Aleem ◽  
H. Zhou ◽  
T. A. Pham
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Experience ◽  
Monocular Deprivation

scholarly journals Experience-dependent development of NMDAR1 subunit expression in the lateral geniculate nucleus

1999 ◽  
Vol 16 (4) ◽  
pp. 781-789 ◽  
Author(s):  
MARK A. FAVA ◽  
KEVIN R. DUFFY ◽  
KATHRYN M. MURPHY
Keyword(s):  
Visual Cortex ◽  
Postnatal Development ◽  
Lateral Geniculate Nucleus ◽  
Critical Period ◽  
Visual Experience ◽  
Monocular Deprivation ◽  
Lateral Geniculate ◽  
Subunit Expression ◽  
Complete Reversal ◽  
Eye Opening

Monocular deprivation early in postnatal development leads to anatomical and physiological changes in the lateral geniculate nucleus (LGN) and visual cortex. Many of these changes are dependent upon activation of the NMDA receptor. We have examined the role of visual experience in modifying NMDAR1 subunit expression in the LGN of animals reared with various forms of visual deprivation. Following monocular deprivation initiated either at eye opening or at the peak of the critical period, there were approximately 20% fewer NMDAR1-immunopositive neurons in the deprived laminae of the LGN. The loss of NMDAR1-immunopositive neurons was found throughout both the binocular and monocular segments of the LGN and after monocular deprivation until just 3 weeks of age. These results indicate that the loss of NMDAR1 in the LGN following monocular deprivation does not simply reflect changes in the visual cortex. The loss of NMDAR1 expression was not necessarily permanent. Initiation of binocular vision at the peak of the critical period ameliorated the effect of monocular deprivation and the introduction of a period of reverse occlusion led to a complete reversal. Taken together, the results show that the expression of the NMDAR1 subunit in the LGN can be modified by the pattern of visual experience during postnatal development.

scholarly journals Experience-dependent structural plasticity at pre- and postsynaptic sites of layer 2/3 cells in developing visual cortex

2019 ◽  
Author(s):  
Yujiao Jennifer Sun ◽  
J. Sebastian Espinosa ◽  
Mahmood S. Hoseini ◽  
Michael P. Stryker
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Critical Period ◽  
Visual Experience ◽  
Visual Deprivation ◽  
Monocular Deprivation ◽  
Structural Basis ◽  
Dependent Plasticity ◽  
Anatomical Changes ◽  
Layer 2

AbstractThe developing brain can respond quickly to altered sensory experience by circuit reorganization. During a critical period in early life, neurons in the primary visual cortex rapidly lose responsiveness to an occluded eye and come to respond better to the open eye. While physiological and some of the molecular mechanisms of this process have been characterized, its structural basis, except for the well-known changes in the thalamocortical projection, remains obscure. To elucidate the relationship between synaptic remodeling and functional changes during this experience-dependent process, we used 2-photon microscopy to image synaptic structures of sparsely labeled layer 2/3 neurons in the binocular zone of mouse primary visual cortex. Anatomical changes at presynaptic and postsynaptic sites in mice undergoing monocular visual deprivation (MD) were compared to those in control mice with normal visual experience. We found that postsynaptic spines remodeled quickly in response to MD, with neurons more strongly dominated by the deprived eye losing more spines. These postsynaptic changes parallel changes in visual responses during MD and their recovery after restoration of binocular vision. In control animals with normal visual experience, the formation of presynaptic boutons increased during the critical period and then declined. MD affected bouton formation, but with a delay, blocking it after 3 days. These findings reveal intracortical anatomical changes in cellular layers of the cortex that can account for rapid activity-dependent plasticity.Significance statementThe operation of the cortex depends on the connections among its neurons. Taking advantage of molecular and genetic tools to label major proteins of the presynaptic and postsynaptic densities, we studied how connections of layer 2/3 excitatory neurons in mouse visual cortex were changed by monocular visual deprivation during the critical period, which causes amblyopia. The deprivation induced rapid remodeling of postsynaptic spines and impaired bouton formation. Structural measurement followed by calcium imaging demonstrated a strong correlation between changes in postsynaptic structures and functional responses in individual neurons after monocular deprivation. These findings suggest that anatomical changes at postsynaptic sites serve as a substrate for experience-dependent plasticity in the developing visual cortex.

Critical period for monocular deprivation in the cat visual cortex

1992 ◽  
Vol 67 (1) ◽  
pp. 197-202 ◽  
Author(s):  
N. W. Daw ◽  
K. Fox ◽  
H. Sato ◽  
D. Czepita
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Single Cells ◽  
Ocular Dominance ◽  
Monocular Deprivation ◽  
Significant Shift ◽  
Cat Visual Cortex

1. Cats were monocularly deprived for 3 mo starting at 8-9 mo, 12 mo, 15 mo, and several years of age. Single cells were recorded in both visual cortexes of each cat, and the ocular dominance and layer determined for each cell. Ocular dominance histograms were then constructed for layers II/III, IV, and V/VI for each group of animals. 2. There was a statistically significant shift in the ocular dominance for cells in layers II/III and V/VI for the animals deprived between 8-9 and 11-12 mo of age. There was a small but not statistically significant shift for cells in layer IV from the animals deprived between 8-9 and 11-12 mo of age, and for cells in layers V/VI from the animals deprived between 15 and 18 mo of age. There was no noticeable shift in ocular dominance for any other layers in any other group of animals. 3. We conclude that the critical period for monocular deprivation is finally over at approximately 1 yr of age for extragranular layers (layers II, III, V, and VI) in visual cortex of the cat.

Oscillations and Long-Lasting Correlations in a Model of the Lateral Geniculate Nucleus and Visual Cortex

2000 ◽  
Vol 84 (4) ◽  
pp. 1863-1868 ◽  
Author(s):  
Kyle L. Kirkland ◽  
Adam M. Sillito ◽  
Helen E. Jones ◽  
David C. West ◽  
George L. Gerstein
Keyword(s):  
Experimental Data ◽  
Visual Cortex ◽  
Cell Membrane ◽  
Lateral Geniculate Nucleus ◽  
Feedback Inhibition ◽  
Frequency Range ◽  
Lateral Geniculate ◽  
Low Threshold ◽  
Thalamocortical System

We have previously developed a model of the corticogeniculate system to explore cortically induced synchronization of lateral geniculate nucleus (LGN) neurons. Our model was based on the experiments of Sillito et al. Recently Brody discovered that the LGN events found by Sillito et al. correlate over a much longer period of time than expected from the stimulus-driven responses and proposed a cortically induced slow covariation in LGN cell membrane potentials to account for this phenomenon. We have examined the data from our model, and we found, to our surprise, that the model shows the same long-term correlation. The model's behavior was the result of a previously unsuspected oscillatory effect, not a slow covariation. The oscillations were in the same frequency range as the well-known spindle oscillations of the thalamocortical system. In the model, the strength of feedback inhibition from the cortex and the presence of low-threshold calcium channels in LGN cells were important. We also found that by making the oscillations more pronounced, we could get a better fit to the experimental data.

Sign in / Sign up

Export Citation Format

Share Document