Excitatory–inhibitory balance and critical period plasticity in developing visual cortex

doi:10.1016/S0079-6123(04)47009-5

Progress in Brain Research

Volume 147, 2005, Pages 115-124

https://doi.org/10.1016/S0079-6123(04)47009-5 Get rights and content

Publisher Summary

This chapter focuses on a newfound perspective of excitatory inhibitory balance within cortical circuits that has granted this control. Neuronal circuits are shaped by their activity during critical or sensitive periods in development. Initially spontaneous, then early sensory-evoked patterns of action potentials are required to sculpt the remarkably complex connectivity found in the adult brain, which then loses this extraordinary level of plasticity. Whether it is the targeting of individual axons or the acquisition of language, there is no doubt that dramatic rewiring is most powerful early in postnatal life. The ability to freely switch on or off critical period mechanisms confirms the very existence of the special stages of heightened plasticity.

Introduction

Neuronal circuits are shaped by their activity during “critical” or “sensitive periods” in development. Initially spontaneous, then early sensory-evoked patterns of action potentials, are required to sculpt the remarkably complex connectivity found in the adult brain, which then loses this extraordinary level of plasticity. Whether it is the targeting of individual axons or the acquisition of language, there is no doubt that dramatic re-wiring is most powerful early in postnatal life. Despite decades of similar robust observations across a wide spectrum of brain functions, only recently have we begun to understand the cellular basis that may underlie this fundamental process. The ability to freely switch on or off critical period mechanisms confirms the very existence of such special stages of heightened plasticity. Here, we focus on a newfound perspective of excitatory-inhibitory balance within cortical circuits that has finally granted this control.

Section snippets

Visual cortex as a model system

The premier physiological model of critical period plasticity is the developing visual system. Over 40 years ago, Wiesel and Hubel (1963) first described the loss of responsiveness to an eye deprived of vision in the primary visual cortex of kittens. As a direct behavioral consequence, the deprived eye becomes amblyopic: its visual acuity is strongly reduced and its contrast sensitivity blunted (see Daw, 1995). Moreover, the rapid physiological effects of monocular deprivation (MD) are soon

Manipulating excitatory-inhibitory balance in vivo

Despite a wealth of phenomenology regarding the rules of experience-dependent development (see Daw, 1995), precious little is known about the underlying cellular mechanism. Over the years, a popular model of homosynaptic plasticity has emerged in parallel studies of learning and memory primarily in the hippocampus. While it is attractive to think of loss of deprived-eye input as a long-term depression (LTD) or gain of open-eye input as long-term potentiation (LTP), advancing knowledge of their

Excitatory-inhibitory balance drives ocular dominance plasticity

Extracellular single-unit recording from the binocular zone of visual cortex in GAD65 KO mice reveals an identical ocular dominance distribution to wild-type animals. The response to a 4-day period of monocular occlusion beginning between P25 and P27 is, however, strikingly different (Hensch et al., 1998). Mice lacking GAD65 show no shift in their responsiveness in favor of the open eye and cortical neurons continue to respond better to the contralateral eye input (Fig. 3).

In order to rescue

Mechanisms and future directions

Excitatory-inhibitory balance determines the neural coding of sensory input. Specific spike timing-dependent windows for synaptic plasticity have recently been elucidated in developing and neocortical structures (Bi and Poo, 2001). Unlike classical models of LTP induced by changes in mean firing rate that are strictly blocked by enhancing inhibition with benzodiazepines (del Cerro et al., 1992; Trepel and Racine, 2000), spike-timing forms of plasticity rely upon physiologically realistic,

Concluding remarks

We have demonstrated the direct control of a classical critical period plasticity in developing primary visual cortex by focusing anew on excitatory-inhibitory balance. How general this principle will be across brain systems remains to be seen. It is already noteworthy that in the primary motor nucleus of the zebrafinch (RA), GABA cell number peaks in striking correlation with the acquisition of song only in the male birds that sing (Sakaguchi, 1996). In contrast, regions exhibiting persistent

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Excitatory–inhibitory balance and critical period plasticity in developing visual cortex

Publisher Summary

Introduction

Section snippets

Visual cortex as a model system

Manipulating excitatory-inhibitory balance in vivo

Excitatory-inhibitory balance drives ocular dominance plasticity

Mechanisms and future directions

Concluding remarks

Biochem. Biophys. Res. Commun

Curr. Opin. Neurobiol

Trends Neurosci

Brain Res

J. Chem. Neuroanat

Neuroscience

Dev. Brain Res

Vision Res

Neuron

Neuron

Brain Res

Neurosci. Res

Cell

Neuron

Neuron

Dev. Brain Res

Trends Pharmacol. Sci

Trends Neurosci

Brain Res

Trends Pharmacol

Brain Res. Rev

Brain Res

Anatomical correlates of functional plasticity in mouse visual cortex

J Neurosci

Rapid remodeling of axonal arbors in the visual cortex

Science

Effect of sensory disuse on geniculate afferents to cat visual cortex

Vis. Neurosci

Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase

Proc. Natl. Acad. Sci. USA

Synaptic modification by correlated activity: Hebb’s postulate revisited

Annu. Rev. Neurosci

Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps

J. Comp. Neurol

Visual Development

Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling

Proc. Natl. Acad. Sci. USA