Auditory Plasticity

The perception of acoustic stimuli can be altered as a consequence of age, experience, and injury. A lasting change in either the perception of acoustic stimuli or in the responses of neurons to acoustic stimuli is known as auditory plasticity, a form of NEURAL PLASTICITY. This plasticity can be demonstrated at both the perceptual and neuronal levels through behavioral methods such as operant and classical CONDITIONING or by lesions of the auditory periphery both in the adult and during development. The plasticity of neuronal responses in the auditory system presumably reflects the ability of humans and animals to adjust their auditory perceptions to match the perceptual world around them as defined by the other sensory modalities, and to perceive the different acoustic-phonetic patterns of the native languages(s) learned during development (see Kuhl 1993).

There are several examples within the psychophysical literature where human subjects can improve their performance at making specific judgments of acoustic stimulus features over the course of several days to weeks, presumably due to changes in the cortical representation of the relevant stimulus parameters. For example, it has recently been shown that normal human subjects will improve their performance at a temporal processing task over the course of several days of training (Wright et al. 1997).

Training-induced changes in perceptual ability have recently been tested as a treatment strategy for children with language-based learning disabilities (cf. LANGUAGE IMPAIRMENT, DEVELOPMENTAL). It had been suggested that children with this type of learning disability are unable to determine the order of two rapidly presented sounds (Tallal and Piercy 1973). Recent studies have demonstrated that some children with this type of learning disability can make such discriminations following several weeks of practice (Merzenich et al. 1996), and these children also showed significant improvements in language comprehension (Tallal et al. 1996).

Several approaches in experimental animals have been employed to address the neuronal mechanisms that underlie auditory plasticity. Single auditory neurons have been shown to change their response properties following classical conditioning paradigms. As an example, single-neuron recording techniques define the response of a single neuron to a range of frequencies, and then a tone that was not optimal in exciting the neuron (the conditioned stimulus, CS) is paired with an unconditioned stimulus (US, e.g., a mild electrical shock). When the frequency response profile of the neuron is defined after conditioning, the response of the neuron to the conditioned tone can be much larger, in some cases to the point that the paired tone is now the best stimulus at exciting the neuron. These changes require a pairing of the CS and the US (Bakin and Weinberger 1990). This response plasticity has been demonstrated in both the auditory THALAMUS and auditory divisions of the CEREBRAL CORTEX (Ryugo and Weinberger 1978; Diamond and Weinberger 1986; Bakin and Weinberger 1990).

It has also been demonstrated that the modulatory neurotransmitter acetylcholine is an important contributor to this effect. If the acetylcholine receptor is blocked, there is no change in the response properties of the neurons (Mc- Kenna et al. 1989). Similarly, activation of the acetylcholine receptor produces a similar enhancement of the neuronal response to the conditioned stimulus (Metherate and Weinberger 1990).

A different experimental strategy is to observe the effects of the representation of frequencies across a wide region of the cerebral cortex. For example, if a limited region of the hair cells in the cochlea are destroyed, there is an expansion of the representation of the neighboring spared frequencies in the auditory cortex (Robertson and Irvine 1989; Rajan et al. 1993). These results indicate that the cerebral cortex is able to adjust the representation of different frequencies depending on the nature of the input. This same type of cortical reorganization probably occurs in normal humans during the progressive loss of high frequency hair cells in the cochlea with aging.

Cortical reorganization can also occur following a period of operant conditioning, where the perception of acoustic stimuli is improved over time, similar to the studies on human subjects described above. Monkeys trained at a frequency discrimination task show a continual improvement in performance during several weeks of daily training. After training, the area within the primary auditory cortex that is most sensitive to the trained frequencies is determined. This area of representation is the greatest in the monkeys trained to discriminate that frequency when compared to the representation of untrained monkeys. This occurs regardless of what particular frequency the monkey was trained to discriminate, but it occurs only at those trained frequencies, and no others. The cortical area of the representation of these trained and untrained frequencies is correlated with the behavioral ability (Recanzone, Schreiner, and Merzenich 1993). A further finding was that only animals that attended to and discriminated the acoustic stimuli showed any change in the cortical representations; monkeys stimulated in the same manner while engaged at an unrelated task had normal representations of the presented frequencies. Thus, stimulus relevance is important in both operant and classical conditioning paradigms.

Auditory plasticity also occurs during development, which has been investigated by taking advantage of the natural orienting behavior of barn owls. These birds can locate the source of a sound extremely accurately. Rearing young owls with optically displacing prisms results in a shift in the owl's perception of the source of an acoustic stimulus (Knudsen and Knudsen 1989). This shift can also be demonstrated electrophysiologically as an alignment of the visual and displaced auditory receptive fields of neurons in the optic tectum (Knudsen and Brainard 1991).

The converging neuronal data from experimental animals suggest that similar changes in response properties of cortical and subcortical neurons also occur in humans. The improvements in performance of human subjects in auditory discrimination tasks, the normal high frequency hearing loss during aging, the change from "language-general" to "language-specific" processing of phonetic information during language acquisition, and injuries to the cochlea or central auditory structures, are presumably resulting in changes in single neuron responses and in cortical and sub-cortical representations. It is quite likely that neuronal plasticity across other sensory modalities and other cognitive functions, particularly in the cerebral cortex, underlies the ability of humans and other mammals to adapt to a changing environment and acquire new skills and behaviors throughout life.

-- Gregg Recanzone

References

Bakin, J. S., and N. M. Weinberger. (1990). Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 536:271-286.

Diamond, D. M., and N. M. Weinberger. (1986). Classical conditioning rapidly induces specific changes in frequency receptive fields of single neurons in secondary and ventral ectosylvian auditory cortical fields. Brain Res. 372:357-360.

Knudsen, E. I., and M. S. Brainard. (1991). Visual instruction of the neural map of auditory space in the developing optic tectum. Science 253:85-87.

Knudsen, E. I., and P. F. Knudsen. (1989). Vision calibrates sound localization in developing barn owls. J. Neurosci. 9:3306-3313.

Kuhl, P. K. (1993). Developmental speech perception: implications for models of language impairment. Annal New York Acad. Sci. 682:248-263.

McKenna, T. M., J. H. Ashe, and N. M. Weinberger. (1989). Cholinergic modulation of frequency receptive fields in auditory cortex: 1. Frequency-specific effects of muscarinic agonists. Synapse 4:30-43.

Merzenich, M. M., W. M. Jenkins, P. Johnston, C. Schreiner, S. L. Miller, and P. Tallal. (1996). Temporal processing deficits of language-learning impaired children ameliorated by training. Science 271:77-81.

Metherate, R., and N. M. Weinberger. (1990). Cholinergic modulation of responses to single tones produces tone-specific receptive field alterations in cat auditory cortex. Synapse 6:133-145.

Rajan, R., D. R. Irvine, L. Z. Wise, and P. Heil. (1993). Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. J. Comp. Neurol. 338:17-49.

Recanzone, G. H., C. E. Schreiner, and M. M. Merzenich. (1993). Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. Journal of Neuroscience 13:87-103.

Robertson, D., and D. R. Irvine. (1989). Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol. 282:456-471.

Ryugo, D. K., and N. M. Weinberger. (1978). Differential plasticity of morphologically distinct neuron populations in the medical geniculate body of the cat during classical conditioning. Behav. Biol. 22:275-301.

Tallal, P., S. L. Miller, G. Bedi, G. Byma, X. Wang, S. S. Nagarajan, C. Schreiner, W. M. Jenkins, and M. M. Merzenich. (1996). Language comprehension in language-learning impaired children improved with acoustically modified speech. Science 271:81-84.

Tallal, P., and M. Piercy. (1973). Defects of non-verbal auditory perception in children with developmental aphasia. Nature 241:468-469.

Wright, B. A., D. V. Buonomano, H. W. Mahncke, and M. M. Merzenich. (1997). Learning and generalization of auditory temporal-interval discrimination in humans. J. Neurosci. 17:3956-3963.

Auditory Plasticity

References

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