Contrasting roles for parvalbumin-expressing inhibitory neurons in two forms of adult visual cortical plasticity

The roles played by cortical inhibitory neurons in experience-dependent plasticity are not well understood. Here we evaluate the participation of parvalbumin-expressing (PV+) GABAergic neurons in two forms of experience-dependent modification of primary visual cortex (V1) in adult mice: ocular dominance (OD) plasticity resulting from monocular deprivation and stimulus-selective response potentiation (SRP) resulting from enriched visual experience. These two forms of plasticity are triggered by different events but lead to a similar increase in visual cortical response. Both also require the NMDA class of glutamate receptor (NMDAR). However, we find that PV+ inhibitory neurons in V1 play a critical role in the expression of SRP and its behavioral correlate of familiarity recognition, but not in the expression of OD plasticity. Furthermore, NMDARs expressed within PV+ cells, reversibly inhibited by the psychotomimetic drug ketamine, play a critical role in SRP, but not in the induction or expression of adult OD plasticity.

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Inhibition of Cdk5 in PV Neurons Reactivates Experience-Dependent Plasticity in Adult Visual Cortex

International Journal of Molecular Sciences ◽

10.3390/ijms23010186 ◽

2021 ◽

Vol 23 (1) ◽

pp. 186

Author(s):

Xinxin Zhang ◽

Huiping Tang ◽

Sitong Li ◽

Yueqin Liu ◽

Wei Wu ◽

...

Keyword(s):

Visual Cortex ◽

Cortical Plasticity ◽

Ocular Dominance ◽

Critical Role ◽

Threshold Current ◽

Inhibitory Neurons ◽

Resting Membrane Potential ◽

Intrinsic Signals ◽

Single Action ◽

Visual Cortical

Cyclin-dependent kinase 5 (Cdk5) has been shown to play a critical role in brain development, learning, memory and neural processing in general. Cdk5 is widely distributed in many neuron types in the central nervous system, while its cell-specific role is largely unknown. Our previous study showed that Cdk5 inhibition restored ocular dominance (OD) plasticity in adulthood. In this study, we specifically knocked down Cdk5 in different types of neurons in the visual cortex and examined OD plasticity by optical imaging of intrinsic signals. Downregulation of Cdk5 in parvalbumin-expressing (PV) inhibitory neurons, but not other neurons, reactivated adult mouse visual cortical plasticity. Cdk5 knockdown in PV neurons reduced the evoked firing rate, which was accompanied by an increment in the threshold current for the generation of a single action potential (AP) and hyperpolarization of the resting membrane potential. Moreover, chemogenetic activation of PV neurons in the visual cortex can attenuate the restoration of OD plasticity by Cdk5 inhibition. Taken together, our results suggest that Cdk5 in PV interneurons may play a role in modulating the excitation and inhibition balance to control the plasticity of the visual cortex.

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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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Pull-Push Neuromodulation of Cortical Plasticity Enables Rapid Bi-Directional Shifts in Ocular Dominance

10.1101/2019.12.13.875849 ◽

2019 ◽

Author(s):

Su Z. Hong ◽

Shiyong Huang ◽

Daniel Severin ◽

Alfredo Kirkwood

Keyword(s):

Cortical Plasticity ◽

Ocular Dominance ◽

Long Term Potentiation ◽

Monocular Deprivation ◽

Ocular Dominance Plasticity ◽

Hebbian Plasticity ◽

Term Potentiation ◽

Visual Cortical

SUMMARYNeuromodulatory systems are essential for remodeling glutamatergic connectivity during experience-dependent cortical plasticity. This permissive/enabling function of neuromodulators has been associated with their capacity to facilitate the induction of Hebbian forms of long-term potentiation (LTP) and depression (LTD) by affecting cellular and network excitability. In vitro studies indicate that neuromodulators can also affect the expression of Hebbian plasticity in a pull-push manner: receptors coupled to the G-protein Gs promote the expression of LTP at the expense of LTD, and Gq-coupled receptors promote LTD at the expense of LTD. Here we show that the pull-push mechanism can be recruited in vivo by pairing brief monocular stimulation with pharmacological or chemogenetical activation of Gs- or Gq-coupled receptors to respectively enhance or reduce visual cortical responses. These changes were stable, can be induced in adults after the termination of the critical period for juvenile ocular dominance plasticity, and can rescue deficits induced by prolonged monocular deprivation.

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Sleep Slow Oscillations and Spindles encode ocular dominance plasticity and promote its consolidation in adult humans

10.1101/2021.03.31.437408 ◽

2021 ◽

Author(s):

Danilo Menicucci ◽

Claudia Lunghi ◽

Andrea Zaccaro ◽

Maria Concetta Morrone ◽

Angelo Gemignani

Keyword(s):

Cortical Plasticity ◽

Ocular Dominance ◽

Monocular Deprivation ◽

Homeostatic Plasticity ◽

Ocular Dominance Plasticity ◽

Slow Oscillations ◽

Adult Humans ◽

The Individual ◽

Visual Cortical

Sleep and plasticity are highly interrelated, as sleep slow oscillations and sleep spindles are associated with consolidation of Hebbian-based processes. However, in adult humans, visual cortical plasticity is mainly sustained by homeostatic mechanisms, for which the role of sleep is still largely unknown. Here we demonstrate that non-REM sleep stabilizes homeostatic plasticity of ocular dominance in adult humans. We found that the effect of short-term monocular deprivation (boost of the deprived eye) was preserved at the morning awakening (>6 hours after deprivation). Subjects exhibiting stronger consolidation had increased sleep spindle density in frontopolar electrodes, suggesting distributed consolidation processes. Crucially, the individual susceptibility to visual homeostatic plasticity was encoded by changes in sleep slow oscillation rate and shape and spindle power in occipital sites, consistent with an early visual cortical site of ocular dominance homeostatic plasticity.

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Subanesthetic ketamine reactivates adult cortical plasticity to restore vision from amblyopia

10.1101/2020.03.16.994475 ◽

2020 ◽

Author(s):

Steven F. Grieco ◽

Xin Qiao ◽

Xiaoting Zheng ◽

Yongjun Liu ◽

Lujia Chen ◽

...

Keyword(s):

Functional Recovery ◽

Neural Plasticity ◽

Cortical Plasticity ◽

Brain Plasticity ◽

Excitatory Input ◽

Inhibitory Neurons ◽

List Type ◽

Visual Cortical

SummarySubanesthetic ketamine evokes rapid and long-lasting antidepressant effects in human patients. The mechanism for ketamine’s effects remains elusive, but ketamine may broadly modulate brain plasticity processes. We show that single-dose ketamine reactivates adult mouse visual cortical plasticity and promotes functional recovery of visual acuity defects from amblyopia. Ketamine specifically induces down-regulation of neuregulin-1 (NRG1) expression in parvalbumin-expressing (PV) inhibitory neurons in mouse visual cortex. NRG1 downregulation in PV neurons co-tracks both the fast onset and sustained decreases in synaptic inhibition to excitatory neurons, along with reduced synaptic excitation to PV neurons in vitro and in vivo following a single ketamine treatment. These effects are blocked by exogenous NRG1 as well as PV targeted receptor knockout. Thus ketamine reactivation of adult visual cortical plasticity is mediated through rapid and sustained cortical disinhibition via downregulation of PV-specific NRG1 signaling. Our findings reveal the neural plasticity-based mechanism for ketamine-mediated functional recovery from adult amblyopia.Highlights○ Disinhibition of excitatory cells by ketamine occurs in a fast and sustained manner○ Ketamine evokes NRG1 downregulation and excitatory input loss to PV cells○ Ketamine induced plasticity is blocked by exogenous NRG1 or its receptor knockout○ PV inhibitory cells are the initial functional locus underlying ketamine’s effects

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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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Early cross-modal interactions and adult human visual cortical plasticity revealed by binocular rivalry

10.36253/978-88-6655-687-9 ◽

2015 ◽

Author(s):

Claudia Lunghi

Keyword(s):

Visual Cortex ◽

Binocular Rivalry ◽

Visual Processing ◽

Cortical Plasticity ◽

Monocular Deprivation ◽

Homeostatic Plasticity ◽

Multisensory Perception ◽

Modal Interactions ◽

Early Visual Cortex ◽

Visual Cortical

In this research binocular rivalry is used as a tool to investigate different aspects of visual and multisensory perception. Several experiments presented here demonstrated that touch specifically interacts with vision during binocular rivalry and that the interaction likely occurs at early stages of visual processing, probably V1 or V2. Another line of research also presented here demonstrated that human adult visual cortex retains an unexpected high degree of experience-dependent plasticity by showing that a brief period of monocular deprivation produced important perceptual consequences on the dynamics of binocular rivalry, reflecting a homeostatic plasticity. In summary, this work shows that binocular rivalry is a powerful tool to investigate different aspects of visual perception and can be used to reveal unexpected properties of early visual cortex.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2105388118 ◽

2021 ◽

Vol 118 (37) ◽

pp. e2105388118

Author(s):

Daniel Severin ◽

Su Z. Hong ◽

Seung-Eon Roh ◽

Shiyong Huang ◽

Jiechao Zhou ◽

...

Keyword(s):

Cortical Plasticity ◽

Classical Model ◽

Ocular Dominance ◽

Pyramidal Cells ◽

Initial Step ◽

Monocular Deprivation ◽

Cortical Circuits ◽

Ocular Dominance Plasticity ◽

Layer 2 ◽

Mouse Visual Cortex

Disinhibition is an obligatory initial step in the remodeling of cortical circuits by sensory experience. Our investigation on disinhibitory mechanisms in the classical model of ocular dominance plasticity uncovered an unexpected form of experience-dependent circuit plasticity. In the layer 2/3 of mouse visual cortex, monocular deprivation triggers a complete, “all-or-none,” elimination of connections from pyramidal cells onto nearby parvalbumin-positive interneurons (Pyr→PV). This binary form of circuit plasticity is unique, as it is transient, local, and discrete. It lasts only 1 d, and it does not manifest as widespread changes in synaptic strength; rather, only about half of local connections are lost, and the remaining ones are not affected in strength. Mechanistically, the deprivation-induced loss of Pyr→PV is contingent on a reduction of the protein neuropentraxin2. Functionally, the loss of Pyr→PV is absolutely necessary for ocular dominance plasticity, a canonical model of deprivation-induced model of cortical remodeling. We surmise, therefore, that this all-or-none loss of local Pyr→PV circuitry gates experience-dependent cortical plasticity.

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Decision letter: Contrasting roles for parvalbumin-expressing inhibitory neurons in two forms of adult visual cortical plasticity

10.7554/elife.11450.025 ◽

2015 ◽

Keyword(s):

Cortical Plasticity ◽

Inhibitory Neurons ◽

Visual Cortical

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The gut microbiota of environmentally enriched mice regulates visual cortical plasticity

10.1101/2021.07.16.452307 ◽

2021 ◽

Author(s):

Leonardo Lupori ◽

Sara Cornuti ◽

Raffaele M Mazziotti ◽

Elisa Borghi ◽

Emerenziana Ottaviano ◽

...

Keyword(s):

Gut Microbiota ◽

Cortical Plasticity ◽

Brain Plasticity ◽

Ocular Dominance ◽

Standard Condition ◽

Intestinal Bacteria ◽

Short Chain Fatty Acids ◽

The Body ◽

Antibiotic Cocktail ◽

Visual Cortical

Exposing animals to an enriched environment (EE) has dramatic effects on brain structure, function and plasticity. The poorly known "EE derived signals" mediating the EE effects are thought to be generated within the central nervous system. Here, we shift the focus to the body periphery, revealing that gut microbiota signals are crucial for EE-driven plasticity. Developmental analysis of intestinal bacteria composition in EE mice revealed striking differences from standard condition (ST) animals and enhanced levels of short-chain fatty acids (SCFA). Depleting the EE mice gut microbiota with an antibiotic cocktail decreased SCFA and prevented EE induction of adult ocular dominance (OD) plasticity, spine dynamics and microglia rearrangement. SCFA treatment in ST mice mimicked the EE induction of adult OD plasticity and morphological microglial rearrangement. Remarkably, transferring the microbiota of EE mice to ST recipients activated adult OD plasticity. Thus, taken together our data suggest that experience-dependent changes in gut microbiota regulate brain plasticity.

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