Adaptive auditory plasticity in developing and adult animals

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Abstract

Enormous progress has been made in our understanding of adaptive plasticity in the central auditory system. Experiments on a range of species demonstrate that, in adults, the animal must attend to (i.e., respond to) a stimulus in order for plasticity to be induced, and the plasticity that is induced is specific for the acoustic feature to which the animal has attended. The requirement that an adult animal must attend to a stimulus in order for adaptive plasticity to occur suggests an essential role of neuromodulatory systems in gating plasticity in adults. Indeed, neuromodulators, particularly acetylcholine (ACh), that are associated with the processes of attention, have been shown to enable adaptive plasticity in adults. In juvenile animals, attention may facilitate plasticity, but it is not always required: during sensitive periods, mere exposure of an animal to an atypical auditory environment can result in large functional changes in certain auditory circuits. Thus, in both the developing and mature auditory systems substantial experience-dependent plasticity can occur, but the conditions under which it occurs are far more stringent in adults. We review experimental results that demonstrate experience-dependent plasticity in the central auditory representations of sound frequency, level and temporal sequence, as well as in the representations of binaural localization cues in both developing and adult animals.

Introduction

Experience-dependent plasticity is essential for shaping and modifying the functional properties of many circuits in the central auditory system. These circuits perform computations on aspects of the auditory world that cannot be known a priori and, therefore, must be learned from experience. For example, the circuits in humans that analyze and categorize phonemes cannot anticipate the languages that an individual will speak. For such circuits, the experience of the individual instructs the functional properties of the circuit, customizing these properties for the individual and its environment (Kuhl, 2004).

For many neural circuits, the shaping influence of experience is unusually strong during sensitive periods in their development (Knudsen, 2004). The exceptional capacity for plasticity during sensitive periods enables circuits to adapt their fundamental architecture and connectivity to the wide range of unknown conditions that can exist across individuals and across environments. In some cases, this early plasticity is guided by instructive signals, such as activity templates, error signals and/or reward signals, which shape the functional properties of a circuit so that it processes or represents information in a particular way (Knudsen, 1994).

Some auditory circuits retain the capacity for experience-dependent plasticity through adulthood (Buonomano and Merzenich, 1998, Suga and Ma, 2003, Weinberger, 2004). The capacity for adult plasticity in these circuits had been severely underestimated previously, because it had been shown that chronic exposure of animals to atypical auditory environments, a manipulation that drives plasticity effectively during sensitive periods, had no effect on the functional properties of these circuits in adult animals. Recent experiments have demonstrated, however, that to induce adaptive plasticity in the adult auditory system the stimulus must be behaviorally relevant. By employing various training paradigms, these studies have revealed an impressive capacity for adult auditory circuits to alter their representations of specific acoustic features.

In contrast to manipulations of the acoustic environment, partial lesions of the cochlea induce plasticity in adult animals that is independent of the behavioral relevance of the acoustic environment (Irvine et al., 2003, Rajan et al., 1993). However, there is no evidence that this kind of plasticity is adaptive. Lesions of the basal turns of the cochlea eliminate high frequency input from the lesioned ear to the central auditory system. Within 8 weeks, neurons in the ventral division of the medial geniculate nucleus (MGN) and the primary auditory cortex (A1), and to a much lesser extent the central nucleus of the inferior colliculus (ICC), that previously were tuned to the lesioned range of frequencies, become tuned to lower frequencies, frequencies represented near the edge of the lesion. The change in the frequency tuning of these neurons results in a large expansion in the representation of these lower frequencies. However, this expansion in the representation of lower frequencies may not be adaptive for the animal. Indeed, the altered frequency representation may cause animals to make errors when interpreting low frequency sounds. Moreover, the mechanisms that underlie lesion-induced plasticity appear to be different from those that underlie examples of plasticity that are more likely to be adaptive (Kamke et al., 2005), especially in adult animals. Therefore, lesion-induced plasticity will not be considered further in our discussion of adaptive plasticity.

This review summarizes the results from recent experiments that have explored the capacity for experience-dependent, adaptive plasticity in the central auditory system of developing and mature animals. Various methods are described that have proven successful in inducing adaptive plasticity, and the properties of sensitive period plasticity are compared with those of the continuing plasticity that exists in adult animals. We explore the importance of behavioral relevance and attention in generating adult plasticity. Finally, we discuss progress that has been made toward the identification of sites and mechanisms of adaptive plasticity.

Section snippets

Frequency tuning

The representation of sound frequency in the A1 of developing rats emerges during a sensitive period (Sally and Kelly, 1988, Zhang et al., 2001). During normal development, soon after the onset of hearing (around post-natal day 11; P11), neurons in A1 have relatively high thresholds and tonotopic organization is poorly defined. When rats are exposed to typical auditory environments over the subsequent 3 weeks, neuronal response thresholds in A1 decrease and a systematic tonotopic organization

Behavioral relevance and frequency tuning

To induce adaptive plasticity in the adult central auditory system, acoustic stimuli must be behaviorally relevant. Frequency tuning is the response property that has been used most often to document plasticity in adults. The plasticity of frequency tuning has been studied in a variety of species and with a variety of training paradigms. Most of these studies have focused on the auditory cortex, specifically the A1 (Bakin et al., 1996, Bakin and Weinberger, 1996, Bao et al., 2001, Bao et al.,

Sites and mechanisms of plasticity

The mechanisms that underlie experience-dependent plasticity in the auditory system are largely unknown. This is because, for the most part, sites of plasticity have yet to be determined. However, sites of plasticity have been identified in two cases: the representation of binaural localization cues in the midbrain of barn owls and the representation of frequency in the forebrain of bats and mice.

The ICX has been shown to be a major site of sensitive period plasticity in the barn owl sound

Comparison of sensitive period and adult plasticity

The expression of functional plasticity is similar in young and adult animals: in both cases, tuning curves for various acoustic parameters may shift, narrow and/or broaden, depending on the acoustic conditions that an animal experiences. However, the plasticity that occurs during sensitive periods is distinguished from the continuing plasticity in adulthood by its magnitude and the conditions under which it occurs. The magnitude and relative ease of inducing plasticity during sensitive periods

Conclusion

Our understanding of adaptive plasticity in the central auditory system has increased dramatically in recent years. As discussed in this review, extensive adaptive plasticity can be induced in juvenile animals by exposing them to atypical auditory environments during sensitive periods, and in adult animals by training them to respond to specific auditory stimuli. With this knowledge, future research will be able to explore more thoroughly the capacities and limitations of adaptive plasticity in

Acknowledgements

We thank J.F. Bergan, C.A. Goddard, S.P. Mysore, D. Winkowski, and I.B. Witten for helpful comments on this paper, and P. Knudsen for assistance with figures. This work has been supported by NIH grants to E.I.K. from the National Institute of Deafness and other Communication Disorders. A.S.K. is a recipient of the Natural Sciences and Engineering Research Council of Canada Postgraduate Scholarship.

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