Circuitry Underlying Experience-Dependent Plasticity in the Mouse Visual System

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2020 Apr 10

PMID 32272065

Citations 66

Authors

Bryan M Hooks

Chinfei Chen

Affiliations

Soon will be listed here.

Abstract

Since the discovery of ocular dominance plasticity, neuroscientists have understood that changes in visual experience during a discrete developmental time, the critical period, trigger robust changes in the visual cortex. State-of-the-art tools used to probe connectivity with cell-type-specific resolution have expanded the understanding of circuit changes underlying experience-dependent plasticity. Here, we review the visual circuitry of the mouse, describing projections from retina to thalamus, between thalamus and cortex, and within cortex. We discuss how visual circuit development leads to precise connectivity and identify synaptic loci, which can be altered by activity or experience. Plasticity extends to visual features beyond ocular dominance, involving subcortical and cortical regions, and connections between cortical inhibitory interneurons. Experience-dependent plasticity contributes to the alignment of networks spanning retina to thalamus to cortex. Disruption of this plasticity may underlie aberrant sensory processing in some neurodevelopmental disorders.

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References

Cynader M, Berman N, Hein A . Recovery of function in cat visual cortex following prolonged deprivation. Exp Brain Res. 1976; 25(2):139-56. DOI: 10.1007/BF00234899. View

Antonini A, Fagiolini M, Stryker M . Anatomical correlates of functional plasticity in mouse visual cortex. J Neurosci. 1999; 19(11):4388-406. PMC: 2452998. View

Gouwens N, Sorensen S, Berg J, Lee C, Jarsky T, Ting J . Classification of electrophysiological and morphological neuron types in the mouse visual cortex. Nat Neurosci. 2019; 22(7):1182-1195. PMC: 8078853. DOI: 10.1038/s41593-019-0417-0. View

Huang Z, Kirkwood A, Pizzorusso T, Porciatti V, Morales B, Bear M . BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 1999; 98(6):739-55. DOI: 10.1016/s0092-8674(00)81509-3. View

Wallace M, van Woerden G, Elgersma Y, Smith S, Philpot B . loss increases excitability and blunts orientation tuning in the visual cortex of Angelman syndrome model mice. J Neurophysiol. 2017; 118(1):634-646. PMC: 5511875. DOI: 10.1152/jn.00618.2016. View

Yaeger C, Ringach D, Trachtenberg J . Neuromodulatory control of localized dendritic spiking in critical period cortex. Nature. 2019; 567(7746):100-104. PMC: 6405296. DOI: 10.1038/s41586-019-0963-3. View

Yu J, Hu H, Agmon A, Svoboda K . Recruitment of GABAergic Interneurons in the Barrel Cortex during Active Tactile Behavior. Neuron. 2019; 104(2):412-427.e4. PMC: 6813892. DOI: 10.1016/j.neuron.2019.07.027. View

Hooks B, Hires S, Zhang Y, Huber D, Petreanu L, Svoboda K . Laminar analysis of excitatory local circuits in vibrissal motor and sensory cortical areas. PLoS Biol. 2011; 9(1):e1000572. PMC: 3014926. DOI: 10.1371/journal.pbio.1000572. View

Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L . Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 1994; 34(6):709-20. DOI: 10.1016/0042-6989(94)90210-0. View

10.

Sarnaik R, Wang B, Cang J . Experience-dependent and independent binocular correspondence of receptive field subregions in mouse visual cortex. Cereb Cortex. 2013; 24(6):1658-70. PMC: 4014185. DOI: 10.1093/cercor/bht027. View

11.

Ghosh A, Antonini A, McConnell S, Shatz C . Requirement for subplate neurons in the formation of thalamocortical connections. Nature. 1990; 347(6289):179-81. DOI: 10.1038/347179a0. View

12.

Stephany C, Ma X, Dorton H, Wu J, Solomon A, Frantz M . Distinct Circuits for Recovery of Eye Dominance and Acuity in Murine Amblyopia. Curr Biol. 2018; 28(12):1914-1923.e5. PMC: 6008222. DOI: 10.1016/j.cub.2018.04.055. View

13.

Sherman S, Spear P . Organization of visual pathways in normal and visually deprived cats. Physiol Rev. 1982; 62(2):738-855. DOI: 10.1152/physrev.1982.62.2.738. View

14.

Lefort S, Tomm C, Sarria J, Petersen C . The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron. 2009; 61(2):301-16. DOI: 10.1016/j.neuron.2008.12.020. View

15.

Xu X, Roby K, Callaway E . Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol. 2009; 518(3):389-404. PMC: 2804902. DOI: 10.1002/cne.22229. View

16.

Lee A, Hoy J, Bonci A, Wilbrecht L, Stryker M, Niell C . Identification of a brainstem circuit regulating visual cortical state in parallel with locomotion. Neuron. 2014; 83(2):455-466. PMC: 4151326. DOI: 10.1016/j.neuron.2014.06.031. View

17.

Hoseini M, Rakela B, Flores-Ramirez Q, Hasenstaub A, Alvarez-Buylla A, Stryker M . Transplanted Cells Are Essential for the Induction But Not the Expression of Cortical Plasticity. J Neurosci. 2019; 39(38):7529-7538. PMC: 6750933. DOI: 10.1523/JNEUROSCI.1430-19.2019. View

18.

Nelson S, Valakh V . Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders. Neuron. 2015; 87(4):684-98. PMC: 4567857. DOI: 10.1016/j.neuron.2015.07.033. View

19.

Kuhlman S, Olivas N, Tring E, Ikrar T, Xu X, Trachtenberg J . A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature. 2013; 501(7468):543-6. PMC: 3962838. DOI: 10.1038/nature12485. View

20.

Takesian A, Bogart L, Lichtman J, Hensch T . Inhibitory circuit gating of auditory critical-period plasticity. Nat Neurosci. 2018; 21(2):218-227. PMC: 5978727. DOI: 10.1038/s41593-017-0064-2. View