Elsevier

Neuroscience Research

Volume 47, Issue 1, September 2003, Pages 17-22
Neuroscience Research

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Controlling the critical period

https://doi.org/10.1016/S0168-0102(03)00164-0Get rights and content

Abstract

Neuronal circuits are shaped by experience during ‘critical periods’ of early postnatal life. The ability to control the timing, duration, and closure of these heightened levels of brain plasticity has recently become experimentally possible. Two seemingly opposed views of critical period mechanism have emerged: (1) plasticity may be functionally accessed throughout life by appropriately modified stimulation protocols, or (2) plasticity is rigidly limited to early postnatal life by structural modifications. This overview synthesizes both perspectives across a variety of brain regions and species. A deeper understanding of critical periods will form the basis for novel international efforts to “nurture the brain”.

Introduction

At no time in life is the brain so easily shaped by experience than in infancy and early childhood (Doupe and Kuhl, 1999, Daw, 1995). It is during these “critical periods” that neural circuits acquire language with native fluency, reproduce the courtship song of a parent bird, expand the representation of a stimulated whisker, or eliminate responsiveness to an occluded eye (ocular dominance, OD). Unraveling the mechanisms that limit such dramatic plasticity to early life would pave the way for novel paradigms or therapeutic agents for rehabilitation, recovery from injury, or improved learning in adulthood. Recent results primarily in the visual system indicate we are ever closer to reaching this elusive goal (Linkenhoker and Knudsen, 2002, Pizzorusso et al., 2002).

Essentially two lines of reasoning have been pursued (Fig. 1). In one view, the potential for plasticity is never lost, but merely tempered by an evolving dynamic of neural activation that can effectively tap into the process. One would thus need to identify the correct “training” regimen to coax these neural networks out of one stable state into another. It may simply be easier to do so in immature tissue, whose composition of receptors and downstream signaling machinery is actively changing. Alternatively, one may posit that amidst this molecular maelstrom appears a class of factors that are inhibitory to further plasticity, eventually preventing large-scale circuit reorganization and thereby structurally closing the critical period. Evidence has now been presented for both possibilities.

Section snippets

Stabilization of network dynamics

The most convincing demonstration that a “critical period” for plasticity exists would be the ability to directly manipulate timing of its expression. Remarkably, this has only recently been achieved in the classical model system of primary visual cortex. Converging inputs from the two eyes typically compete for connectivity (OD) with a peak sensitivity to monocular deprivation around 1 month after birth in cats and rodents (Hubel and Wiesel, 1970, Daw, 1995, Fagiolini and Hensch, 2000). Yet,

Relevance of synaptic plasticity rules

Taken together, these findings argue against a primary role for turning on and off excitatory synaptic plasticity rules to establish a critical period. Enhancing inhibition enables plasticity in visual cortex in vivo (Fagiolini and Hensch, 2000), but suppresses long-term potentiation (LTP) induced by high-frequency stimulation in vitro (Huang et al., 1999). Likewise, long-term depression (LTD) is reportedly most robust in young wild-type mice before the critical period, when OD plasticity is

Structural consolidation of circuits

A different view of critical period closure is an anatomical one (Fig. 1B). For instance, in barrel cortex the critical period refers to the capacity for anatomical expansion or contraction of individual whisker representations just after birth (Van der Loos and Woolsey, 1973, Lu et al., 2001, Datwani et al., 2002). If a row of whiskers is removed (cauterized) just after birth, barrels serving the deprived whiskers shrink while neighboring barrels from the intact whiskers expand. The degree of

Future directions

So, does the critical period permanently hard-wire our brains or can we enjoy massive plasticity throughout life by finding the right stimulation protocols? As is common in biology, both views are likely to be correct. Curiously, perineuronal nets mainly surround fast-spiking, parvalbumin-positive interneurons (Fig. 1B), whose function may be particularly sensitive to extracellular ionic balance (Hartig et al., 1999). This raises the possibility that Maffei and colleagues re-opened the critical

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