A disinhibitory microcircuit initiates critical period plasticity in visual cortex

By S. Kuhlman, Nicholas D. Olivas, Elaine Tring, T. Ikrar, Xiangmin Xu, J. Trachtenberg. 2013

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Early sensory experience instructs the maturation of neural circuitry in the cortex. This has been studied extensively in the primary visual cortex, in which loss of vision to one eye permanently degrades cortical responsiveness to that eye, a phenomenon known as ocular dominance plasticity (ODP). Cortical inhibition mediates this process, but the precise role of specific classes of inhibitory neurons in ODP is controversial. Here we report that evoked firing rates of binocular excitatory neurons in the primary visual cortex immediately drop by half when vision is restricted to one eye, but gradually return to normal over the following twenty-four hours, despite the fact that vision remains restricted to one eye. This restoration of binocular-like excitatory firing rates after monocular deprivation results from a rapid, although transient, reduction in the firing rates of fast-spiking, parvalbumin-positive (PV) interneurons, which in turn can be attributed to a decrease in local excitatory circuit input onto PV interneurons. This reduction in PV-cell-evoked responses after monocular lid suture is restricted to the critical period for ODP and appears to be necessary for subsequent shifts in excitatory ODP. Pharmacologically enhancing inhibition at the time of sight deprivation blocks ODP and, conversely, pharmacogenetic reduction of PV cell firing rates can extend the critical period for ODP. These findings define the microcircuit changes initiating competitive plasticity during critical periods of cortical development. Moreover, they show that the restoration of evoked firing rates of layer 2/3 pyramidal neurons by PV-specific disinhibition is a key step in the progression of ODP.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Molecular Biology

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Citations in the corpus

Plasticity of Cortical Excitatory-Inhibitory Balance (2015, background): “GABAergic inhibition keeps NMDA receptors nominally in check, and transient reduction of inhibition is an effective means for gating plasticity in response to electrical or sensory stimulation (Artola et al. 1990, Chun et al. 2013, Froemke et al. 2007, Kuhlman et al. 2013).”
A cortical circuit for gain control by behavioral state (2014, background): “…Stony Brook University, Stony Brook, NY 11790, USA 4Departments of Cellular and Molecular Pharmacology and Physiology, University of California, San Francisco, CA 94158, USA *Correspondence: yufu@phy.ucsf.edu (Y.F.), stryker@phy.ucsf.edu (M.P.S.) http://dx.doi.org/10.1016/j.cell.2014.01.050”
Fast-spiking, parvalbumin+ GABAergic interneurons: From cellular design to microcircuit function (2014, background): “PV interneurons in the visual cortex are transiently inhibited after monocular deprivation; this down-regulation appears to be necessary to enable ocular dominance plasticity in the critical period (103, 106).”
Modeling the dynamic interaction of Hebbian and homeostatic plasticity. (2014, neutral): “For example, here we did not model plasticity in synapses to or from inhibitory neurons (e.g., Gandhi et al., 2008; Kuhlman et al., 2013; Maffei et al., 2006) or in intrinsic intracortical synapses (e.g., Trachtenberg and Stryker, 2001).”
Rapid homeostasis by disinhibition during whisker map plasticity (2014, background): “Recent results in visual cortex show that eyelid closure rapidly weakens inhibitory circuits (within 1 d), and this process increases network excitability and, therefore, is an initial homeostatic response to deprivation (10, 16).”
Receptive field formation by interacting excitatory and inhibitory synaptic plasticity (2016, background): “…(Dorrn et al., 2010), with the hypothesis that the maturation of inhibition controls the duration of developmental critical periods (Hensch, 2005; Kuhlman et al., 2013) and with the apparent need for disinhibition for receptive field plasticity in mature animals (Froemke et al., 2007; Kuhlman et…”
Functional connectivity of visual cortex in the blind follows retinotopic organization principles (2015, methodology): “…in adulthood via molecular manipulations which reopen critical-period development opportunities based on the principles naturally occurring in critical periods and following brain injury (e.g. excitatoryinhibitory balance) (Bavelier et al., 2010; Kuhlman et al., 2013; Nahmani and Turrigiano, 2014).”