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.

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

2019 ◽  
Vol 116 (43) ◽  
pp. 21812-21820 ◽  
Author(s):  
Yujiao Jennifer Sun ◽  
J. Sebastian Espinosa ◽  
Mahmood S. Hoseini ◽  
Michael P. Stryker
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Critical Period ◽  
Molecular Mechanisms ◽  
Visual Experience ◽  
Structural Basis ◽  
Visual Responses ◽  
Functional Changes ◽  
Anatomical Changes ◽  
Layer 2

The 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 d. These findings reveal intracortical anatomical changes in cellular layers of the cortex that can account for rapid activity-dependent plasticity.

Functional postnatal development of the rat primary visual cortex and the role of visual experience: Dark rearing and monocular deprivation

1994 ◽  
Vol 34 (6) ◽  
pp. 709-720 ◽  
Author(s):  
Michela Fagiolini ◽  
Tommaso Pizzorusso ◽  
Nicoletta Berardi ◽  
Luciano Domenici ◽  
Lamberto Maffei
Keyword(s):  
Visual Cortex ◽  
Postnatal Development ◽  
Primary Visual Cortex ◽  
Visual Experience ◽  
Monocular Deprivation ◽  
Dark Rearing

scholarly journals Vision reconstructs the cellular composition of binocular circuitry during the critical period

2020 ◽  
Author(s):  
Liming Tan ◽  
Elaine Tring ◽  
Dario L. Ringach ◽  
S. Lawrence Zipursky ◽  
Joshua T. Trachtenberg
Keyword(s):  
Visual Cortex ◽  
Receptive Field ◽  
Primary Visual Cortex ◽  
Critical Period ◽  
Cellular Composition ◽  
Feature Detectors ◽  
Layer 2 ◽  
Layer 4 ◽  
High Acuity ◽  
Longitudinal Imaging

AbstractHigh acuity binocularity is established in primary visual cortex during an early postnatal critical period. In contrast to current models for the developmental of binocular neurons, we find that the binocular network present at the onset of the critical period is dismantled and remade. Using longitudinal imaging of receptive field tuning (e.g. orientation selectivity) of thousands of layer 2/3 neurons through development, we show most binocular neurons present at critical-period onset are poorly tuned and rendered monocular. These are replenished by newly formed binocular neurons that are established by a vision-dependent recruitment of well-tuned ipsilateral inputs to contralateral monocular neurons with matched tuning properties. The binocular network in layer 4 is equally unstable but does not improve. Thus, vision instructs a new and more sharply tuned binocular network in layer 2/3 by exchanging one population of neurons for another and not by refining an extant network.One Sentence SummaryUnstable binocular circuitry is transformed by vision into a network of highly tuned complex feature detectors in the cortex.

scholarly journals Closing the Critical Period Is Required for the Maturation of Binocular Integration in Mouse Primary Visual Cortex

2021 ◽  
Vol 15 ◽  
Author(s):  
Jiangping Chan ◽  
Xiangwen Hao ◽  
Qiong Liu ◽  
Jianhua Cang ◽  
Yu Gu
Keyword(s):  
Visual Cortex ◽  
Mouse Model ◽  
Primary Visual Cortex ◽  
Depth Perception ◽  
Critical Period ◽  
Visual Experience ◽  
Extracellular Recording ◽  
Molecular Assay ◽  
Binocular Matching

Binocular matching of orientation preference between the two eyes is a common form of binocular integration that is regarded as the basis for stereopsis. How critical period plasticity enables binocular matching under the guidance of normal visual experience has not been fully demonstrated. To investigate how critical period closure affects the binocular matching, a critical period prolonged mouse model was constructed through the administration of bumetanide, an NKCC1 transporter antagonist. Using acute in vivo extracellular recording and molecular assay, we revealed that binocular matching was transiently disrupted due to heightened plasticity after the normal critical period, together with an increase in the density of spines and synapses, and the upregulation of GluA1 expression. Diazepam (DZ)/[(R, S)-3-(2-carboxypiperazin-4-yl) propyl-1-phosphonic acid (CPP)] could reclose the extended critical period, and rescue the deficits in binocular matching. Furthermore, the extended critical period, alone, with normal visual experience is sufficient for the completion of binocular matching in amblyopic mice. Similarly, prolonging the critical period into adulthood by knocking out Nogo-66 receptor can prevent the normal maturation of binocular matching and depth perception. These results suggest that maintaining an optimal plasticity level during adolescence is most beneficial for the systemic maturation. Extending the critical period provides new clues for the maturation of binocular vision and may have critical implications for the treatment of amblyopia.

scholarly journals Activation of somatostatin interneurons by nicotinic modulator Lypd6 enhances plasticity and functional recovery in the adult mouse visual cortex

2017 ◽  
Author(s):  
Masato Sadahiro ◽  
Michael P. Demars ◽  
Poromendro Burman ◽  
Priscilla Yevoo ◽  
Andreas Zimmer ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Functional Recovery ◽  
Critical Period ◽  
Cortical Plasticity ◽  
Monocular Deprivation ◽  
Adult Brain ◽  
Clinical Issue ◽  
Dependent Plasticity ◽  
Excitatory Neurons ◽  
Interneuron Activity

AbstractThe limitation of plasticity in the adult brain impedes functional recovery later in life from brain injury or disease. This pressing clinical issue may be resolved by enhancing plasticity in the adult brain. One strategy for triggering robust plasticity in adulthood is to reproduce one of the hallmark physiological events of experience-dependent plasticity observed during the juvenile critical period – rapidly reduce the activity of parvalbumin (PV)-expressing interneurons and disinhibit local excitatory neurons. This may be achieved through enhancement of local inhibitory inputs, particularly those of somatostatin (SST)-expressing interneurons. However, to date the means for manipulating SST interneurons for enhancing cortical plasticity in the adult brain are not known. We show that SST interneuron-selective overexpression of Lypd6, an endogenous nicotinic signaling modulator, enhances ocular dominance plasticity in the adult primary visual cortex (V1). Lypd6 overexpression mediates a rapid experience-dependent increase in the visually evoked activity of SST interneurons as well as a simultaneous reduction in PV interneuron activity and disinhibition of excitatory neurons. Recapitulating this transient activation of SST interneurons using chemogenetics similarly enhanced V1 plasticity. Notably, we show that SST-selective Lypd6 overexpression restores visual acuity in amblyopic mice that underwent early long-term monocular deprivation. Our data in both male and female mice reveal selective modulation of SST interneurons and a putative downstream circuit mechanism as an effective method for enhancing experience-dependent cortical plasticity as well as functional recovery in adulthood.Significance StatementThe decline of cortical plasticity after closure of juvenile critical period consolidates neural circuits and behavior, but this limits functional recovery from brain diseases and dysfunctions in later life. Here we show that activation of cortical SST interneurons by Lypd6, an endogenous modulator of nicotinic acetylcholine receptors (nAChRs), enhances experience-dependent plasticity and recovery from amblyopia in adulthood. This manipulation triggers rapid reduction of PV interneuron activity and disinhibition of excitatory neurons, which are known hallmarks of cortical plasticity during juvenile critical periods. Our study demonstrates modulation of SST interneurons by Lypd6 to achieve robust levels of cortical plasticity in the adult brain and may provide promising targets for restoring brain function in the event of brain trauma or disease.

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 Synaptic Mechanisms of Activity-Dependent Remodeling in Visual Cortex during Monocular Deprivation

2009 ◽  
Vol 2 ◽  
pp. JEN.S2559 ◽  
Author(s):  
Cynthia D. Rittenhouse ◽  
Ania K Majewska
Keyword(s):  
Visual Cortex ◽  
Critical Period ◽  
Ocular Dominance ◽  
Monocular Deprivation ◽  
Neuronal Structure ◽  
Cortical Cells ◽  
Dependent Plasticity ◽  
Cortical Synapses ◽  
Activity Dependent ◽  
Synaptic Mechanisms

It has long been appreciated that in the visual cortex, particularly within a postnatal critical period for experience-dependent plasticity, the closure of one eye results in a shift in the responsiveness of cortical cells toward the experienced eye. While the functional aspects of this ocular dominance shift have been studied for many decades, their cortical substrates and synaptic mechanisms remain elusive. Nonetheless, it is becoming increasingly clear that ocular dominance plasticity is a complex phenomenon that appears to have an early and a late component. Early during monocular deprivation, deprived eye cortical synapses depress, while later during the deprivation open eye synapses potentiate. Here we review current literature on the cortical mechanisms of activity-dependent plasticity in the visual system during the critical period. These studies shed light on the role of activity in shaping neuronal structure and function in general and can lead to insights regarding how learning is acquired and maintained at the neuronal level during normal and pathological brain development.

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 Activation of NMDA Receptors Is Necessary for the Recovery of Cortical Binocularity

2010 ◽  
Vol 103 (5) ◽  
pp. 2700-2706 ◽  
Author(s):  
Thomas E. Krahe ◽  
Alexandre E. Medina
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Binocular Vision ◽  
Critical Period ◽  
Functional Change ◽  
Monocular Deprivation ◽  
Extracellular Recordings ◽  
Aspartate Receptor ◽  
Critical Period Of Development

Classic experiments have indicated that monocular deprivation (MD) for a few days during a critical period of development results in a decrease in the strength of connections mediating responses to the deprived eye, leading to a dramatic breakdown of cortical neuron binocularity. Despite the substantial functional change in the visual cortex, recovery from the effects of MD can be obtained if binocular vision is promptly restored. While great efforts have been made to elucidate the mechanisms regulating loss of deprived eye function, the mechanisms that underlie the recovery of cortical binocularity are poorly understood. Here, we examined whether activation of the N-methyl-d-aspartate receptor (NMDAR) is required for the recovery of cortical binocularity by pharmacologically blocking the NMDAR using d,l-2-amino-5-phosphonopentanoic (APV). Ferrets ( n = 10) were monocularly deprived for 6 days, and osmotic minipumps, filled with APV (5.6 mg/ml) or saline, were surgically implanted into the primary visual cortex. One day after surgery, the deprived eye was reopened, and the animals were allowed 24 h of binocular vision. Extracellular recordings showed that intracortical infusion of the NMDAR antagonist, APV, prevented recovery of cortical binocularity while preserving neuronal responsiveness. These findings provide an important new insight for a specific role of NMDARs in the recovery of cortical binocularity from the effects of MD.

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.

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