Review
Critical periods during sensory development

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Abstract

Recent studies have made progress in characterizing the determinants of critical periods for experience-dependent plasticity. They highlight the role of neurotrophins, NMDA receptors and GABAergic inhibition. In particular, genetic manipulation of a single molecule, brain-derived neurotrophic factor (BDNF), has been shown to alter the timing of the critical period of plasticity in mouse visual cortex, establishing a causal relation between neurotrophin action, the development of visual function, and the duration of the critical period.

Introduction

Early in development, the existence, of critical periods for experience-dependent plasticity has been clearly demonstrated for the visual, auditory and somatosensory systems. Critical periods also exist for many other functions, including song in birds and language in humans — in this latter case, plasticity may even reach the extreme of allowing the interhemispheric transfer of language areas, as seen in the case of left hemisphere injury early in infancy 1, 2, 3. Critical periods have been found to exist in virtually all species, from humans to Drosophila [4]. Here, we shall restrict ourselves mainly to studies focusing on the development of visual and auditory systems in mammals and birds.

Classical studies have shown that the effects of sensory deprivation (such as monocular deprivation or monaural plugging) and the effects of alterations in sensory input (such as caused by strabismus, rearing in a restricted auditory environment, or misalignment of the auditory and visual space) are evident only when the manipulation of the sensory input is made during the critical period; similar deprivations and alterations in mature animals have no effect. The duration of these critical periods depends on the function tested and on the way plasticity is evaluated, as for instance, critical periods measured in terms of recovery from sensory deprivation are longer than critical periods measured in terms of the induction of sensory deprivation effects. In research on the visual system, the most extensively studied critical period is that for the effects of monocular deprivation (MD) on the ocular dominance of cortical neurons, which has been characterized in the monkey, cat, rat, mouse, ferret and human 5, 6, 7••, 8, 9, 10 (Figure 1). In the auditory system, the most extensively studied critical period is that for the calibration of the auditory space map by visual input 3, 11. Critical periods for sensory plasticity resulting from increased sensory experience have also occasionally been reported: in humans, musical training in infancy leads to an expanded auditory cortical representation [12••], but only if practising began before the age of 9 (Figure 2).

As shown in Figure 1, the critical period is a definite portion of an animal’s life devoted to the shaping of neural connections: the longer the life span, the longer the critical period. A relation also exists between the critical period and brain weight; if one assumes that brain weight is a rough measure of brain complexity, it follows that the more complex the brain, the longer the critical period. During the critical period, sensory functions reach maturity: for example, as shown in Figure 1b, the end of the critical period for MD roughly coincides with the completion of visual acuity development in a number of species. This indicates that experience-dependent plasticity during the critical period is closely interconnected with maturation of sensory functions.

It should be noted that some aspects of cortical organization are also modifiable, by experience, in the adult. This is the case for the frequency map in the auditory cortex [13] and the somatotopic map in the somatosensory cortex 1, 14. The search for the mechanisms determining the beginning and the end of critical periods has been progressing for some years. The possibility to exploit genetic manipulations in the mouse has given fresh impetus to the quest. In this review we shall highlight recent advances which have brought this quest to the cellular and molecular levels, calling into play neurotrophins, inhibitory circuitry and NMDA receptors.

Section snippets

Crossmodal plasticity following early sensory deprivation

Only during early development can total deprivation in one modality lead to compensatory changes in other modalities; namely, to ‘crossmodal’ plasticity. For example, it has recently been reported that early-blind human subjects localize sound sources better than sighted subjects [15], particularly for peripheral locations [16]. This ability might be subserved by the expansion of auditory inputs to ‘unused’ visual areas and the improvement of auditory neuron spatial tuning, as observed in

Experience-related control of critical periods

Experience is a strong determinant for the duration of critical periods: total lack of experience usually prolongs critical periods and delays development of sensory functions. The clearest examples of this come from studies using dark rearing (DR), but evidence is also available from studies in early-deaf children who have been fitted with cochlear implants 13, 20; in addition, a lack of appropriate tutorial experience seems to prolong the critical period for the development of birdsong [2].

Determinants of critical periods

We shall now examine some factors whose status as determinants of critical periods has recently been established, including NMDA receptors, neurotrophins, and inhibitory circuitry.

Conclusions

It is becoming increasingly clear that critical periods result from changes in the expression of molecules; however, the identity of these putative molecular determinants is far from being established. For most candidate molecules correlative — but not causal — connections between expression of that molecule and duration of the critical period have been obtained. The first conclusion to be drawn from this survey is that neurotrophins are the only factors for which a causal link between

Note added in proof

Two papers have been published very recently 62, 63. The first is concerned with the acute effects of neurotrophins. BDNF has been found to excite isolated cortical, hippocampal and cerebellar neurons in culture just as rapidly as the neurotransmitter glutamate. The second is concerned with the development of ocular dominance columns in ferrets. Surprisingly, total removal of retinal influence early in visual development did not prevent segregation of geniculocortical axons into alternating

Acknowledgements

This work was supported by Consiglio Nazionale della Ricerca targeted programs in Biotechnology; sub project 5 and Ministero delle Università e delle Ricerca Scientifica e Tecnologica, Cofinanziamento.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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