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

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.

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

10.1101/743690 ◽

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.

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

10.1101/2020.05.31.126474 ◽

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.

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

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2021.749265 ◽

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.

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The role of early visual experience in the development of spatial‐frequency preference in the primary visual cortex

The Journal of Physiology ◽

10.1113/jp281463 ◽

2021 ◽

Author(s):

Nana Nishio ◽

Kenji Hayashi ◽

Ayako Wendy Ishikawa ◽

Yumiko Yoshimura

Keyword(s):

Visual Cortex ◽

Spatial Frequency ◽

Primary Visual Cortex ◽

Visual Experience

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A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex

Journal of Neuroscience ◽

10.1523/jneurosci.17-20-07926.1997 ◽

1997 ◽

Vol 17 (20) ◽

pp. 7926-7940 ◽

Cited By ~ 338

Author(s):

Juan A. Varela ◽

Kamal Sen ◽

Jay Gibson ◽

Joshua Fost ◽

L. F. Abbott ◽

...

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Quantitative Description ◽

Excitatory Synapses ◽

Short Term ◽

Short Term Plasticity ◽

Layer 2

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Critical periods in amblyopia

Visual Neuroscience ◽

10.1017/s0952523817000219 ◽

2018 ◽

Vol 35 ◽

Cited By ~ 47

Author(s):

TAKAO K. HENSCH ◽

ELIZABETH M. QUINLAN

Keyword(s):

Visual Cortex ◽

Critical Period ◽

Molecular Mechanisms ◽

Ocular Dominance ◽

Molecular Genetic ◽

Monocular Deprivation ◽

Critical Periods ◽

Developmental Constraints ◽

Early Postnatal Development ◽

Visual Cortical

AbstractThe shift in ocular dominance (OD) of binocular neurons induced by monocular deprivation is the canonical model of synaptic plasticity confined to a postnatal critical period. Developmental constraints on this plasticity not only lend stability to the mature visual cortical circuitry but also impede the ability to recover from amblyopia beyond an early window. Advances with mouse models utilizing the power of molecular, genetic, and imaging tools are beginning to unravel the circuit, cellular, and molecular mechanisms controlling the onset and closure of the critical periods of plasticity in the primary visual cortex (V1). Emerging evidence suggests that mechanisms enabling plasticity in juveniles are not simply lost with age but rather that plasticity is actively constrained by the developmental up-regulation of molecular ‘brakes’. Lifting these brakes enhances plasticity in the adult visual cortex, and can be harnessed to promote recovery from amblyopia. The reactivation of plasticity by experimental manipulations has revised the idea that robust OD plasticity is limited to early postnatal development. Here, we discuss recent insights into the neurobiology of the initiation and termination of critical periods and how our increasingly mechanistic understanding of these processes can be leveraged toward improved clinical treatment of adult amblyopia.

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Pure tones modulate the representation of orientation and direction in the primary visual cortex

Journal of Neurophysiology ◽

10.1152/jn.00069.2019 ◽

2019 ◽

Vol 121 (6) ◽

pp. 2202-2214 ◽

Cited By ~ 5

Author(s):

John P. McClure ◽

Pierre-Olivier Polack

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulus ◽

Visual Stimuli ◽

Direction Selectivity ◽

Multimodal Integration ◽

Visual Responses ◽

V1 Neurons ◽

Pure Tones ◽

The Impact

Multimodal sensory integration facilitates the generation of a unified and coherent perception of the environment. It is now well established that unimodal sensory perceptions, such as vision, are improved in multisensory contexts. Whereas multimodal integration is primarily performed by dedicated multisensory brain regions such as the association cortices or the superior colliculus, recent studies have shown that multisensory interactions also occur in primary sensory cortices. In particular, sounds were shown to modulate the responses of neurons located in layers 2/3 (L2/3) of the mouse primary visual cortex (V1). Yet, the net effect of sound modulation at the V1 population level remained unclear. In the present study, we performed two-photon calcium imaging in awake mice to compare the representation of the orientation and the direction of drifting gratings by V1 L2/3 neurons in unimodal (visual only) or multimodal (audiovisual) conditions. We found that sound modulation depended on the tuning properties (orientation and direction selectivity) and response amplitudes of V1 L2/3 neurons. Sounds potentiated the responses of neurons that were highly tuned to the cue’s orientation and direction but weakly active in the unimodal context, following the principle of inverse effectiveness of multimodal integration. Moreover, sound suppressed the responses of neurons untuned for the orientation and/or the direction of the visual cue. Altogether, sound modulation improved the representation of the orientation and direction of the visual stimulus in V1 L2/3. Namely, visual stimuli presented with auditory stimuli recruited a neuronal population better tuned to the visual stimulus orientation and direction than when presented alone. NEW & NOTEWORTHY The primary visual cortex (V1) receives direct inputs from the primary auditory cortex. Yet, the impact of sounds on visual processing in V1 remains controverted. We show that the modulation by pure tones of V1 visual responses depends on the orientation selectivity, direction selectivity, and response amplitudes of V1 neurons. Hence, audiovisual stimuli recruit a population of V1 neurons better tuned to the orientation and direction of the visual stimulus than unimodal visual stimuli.

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Visual Deprivation Decreases Somatic GAD65 Puncta Number on Layer 2/3 Pyramidal Neurons in Mouse Visual Cortex

Neural Plasticity ◽

10.1155/2009/415135 ◽

2009 ◽

Vol 2009 ◽

pp. 1-7 ◽

Cited By ~ 19

Author(s):

Alicja Kreczko ◽

Anubhuthi Goel ◽

Lihua Song ◽

Hey-Kyoung Lee

Keyword(s):

Visual Cortex ◽

Visual Experience ◽

Pyramidal Neurons ◽

Immunohistochemical Method ◽

Inhibitory Synapses ◽

Acid Decarboxylase ◽

3D Analysis ◽

Individual Layer ◽

Inhibitory Circuitry ◽

Layer 2

Proper functioning of the visual system depends on maturation of both excitatory and inhibitory synapses within the visual cortex. Considering that perisomatic inhibition is one of the key factors that control the critical period in visual cortex, it is pertinent to understand its regulation by visual experience. To do this, we developed an immunohistochemical method that allows three-dimensional (3D) analysis of the glutamic acid decarboxylase (GAD) 65-positive inhibitory terminals in the visual cortex. Using this method on transgenic mice expressing yellow fluorescence protein (YFP) in a subset of neurons, we found that the number of somatic GAD65-puncta on individual layer 2/3 pyramidal neurons is reduced when mice are dark-reared from birth and reverted to normal levels by re-exposure to light. There was no change in GAD65-puncta volume or intensity. These results support the reorganization of inhibitory circuitry within layer 2/3 of visual cortex in response to changes in visual experience.

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