ReviewMaturation of GABAergic transmission and the timing of plasticity in visual cortex
Introduction
Deprivation studies, conducted first in carnivores and primates and later in rodent, have shown that the maturation of visual cortex requires normal visual experience during a brief postnatal critical period of enhanced plasticity. At this stage, simple manipulations of sensory experience, like depriving one eye of vision for a few days (monocular deprivation, MD), can shift the cortical responses of binocular neurons toward the non-deprived eye (ocular dominance plasticity, ODP) [24], [34], [49]. Considerable progress has been made in identifying the mechanisms by which neural activity can alter cortical connectivity. It is now widely accepted that NMDA receptor dependent synaptic modifications, such as long-term depression (LTD) and long-term potentiation (LTP) are crucial for ocular dominance plasticity [17], [19], [47], [61], [80], [81]. Much less is known about the mechanisms that constrain synaptic modification to a short critical period [8], [45]. Recently, however, it has become apparent that GABAergic inhibitory circuits are central to determining the timing of the critical period for the modification of excitatory synapses [46], [48], [60].
GABAergic inhibitory circuits change during the critical period and can be altered by sensory deprivation [35], even in adults [44]. In virtually all species studied, the anatomical [9], [32], [36], [68], [70], [71] and physiological [6], [62], [64] evidence indicates that synaptic inhibition matures later than excitatory transmission in the neocortex. By controlling excitation, GABAergic circuits are ideally posed to control the engagement of activity dependent synaptic modification. Thus, the mismatch in the maturation of excitation and inhibition may define a window of opportunity, early in postnatal life, for activity dependent plasticity to occur [48], [60].
Section snippets
Involvement of GABAergic circuits in the timing of experience-dependent plasticity
It is well established from in vivo studies that pharmacological activation and blockade of cortical GABA receptors can alter dramatically the outcome of monocular deprivation [40], [78], [79]. However, a role of GABAergic inhibition in terminating the critical period was first suggested by in vitro analysis of developmentally regulated forms of NMDA receptor-dependent plasticity. These studies showed that GABAergic antagonists can restore the long-term potentiation (LTP) recorded in layer III
Postnatal maturation of GABAergic transmission
The protracted maturation of the cortical GABAergic system was initially inferred from anatomical [9] data and single unit recordings [6]. Later on, intracellular analysis in cortical slices confirmed in greater detail that cortical GABAergic circuits are highly immature at birth. Perinatal GABAergic responses are slow, depolarizing and sparse [1], [62]. However, not all postnatal changes in GABAergic transmission are likely to shape experience dependence plasticity. The shift in the reversal
Possible mechanisms of control
GABAergic neurons form a highly diverse group in terms of anatomy, connectivity and physiological properties, which is likely a reflection of the diversity of function [37], [55], [56]. For example, chandelier cells, which synapse onto the initial segment of the axon, can veto the initiation of the action potential. Basket cells targeting primarily the soma and proximal dendrites can influence the precise timing of the action potential, and bipolar cells contacting the dendrites can affect
Concluding remarks
It has been known for many years that the maturation of GABAergic circuits is protracted relative to the maturation of excitatory circuitry. Recent studies conducted in rodents using genetically altered mice underscore the importance of this slow maturation in the timing of cortical plasticity. On the other hand, in vitro studies have identified two mechanisms for the developmental strengthening of GABAergic transmission: a 3-fold increase in the number of GABA release sites, and a 2-fold
Acknowledgments
We thank Drs. H.K. Lee and E. Quinlan for critically reviewing the manuscript. Supported by grants from NEI to A.K. and FONDECYT 1030220 to B.M.
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