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Multiparametric corticofugal modulation and plasticity in the auditory system

Nature Reviews Neuroscience volume 4, pages 783–794 (2003)Cite this article

Key Points

  • The auditory system has the potential for reorganization as a function of experience. In particular, corticofugal projections can affect the properties of subcortical neurons in response to sound.

  • Corticofugal modulation in awake animals has been found across the different domains that comprise an acoustic signal: frequency, amplitude, time and threshold. In general terms, two forms of reorganization have been documented — expanded and compressed reorganizations.

  • Expanded reorganization results from an increase in the number of neurons that respond with properties equal to that of the stimulated corticofugal neuron — a 'centripetal shift'. By contrast, compressed reorganization results from 'centrifugal shifts'; that is, shifts away from the properties of the cortical neuron. Whereas expanded reorganization has been found in several species, compressed reorganization has been found only in the auditory system of the moustached bat, which is specialized for echolocation.

  • Experimentally, corticofugal modulation is commonly elicited by electrical or pharmacological stimulation. However, there is evidence that similar changes occur in response to auditory stimuli. In particular, the study of auditory fear conditioning has disclosed subcortical reorganization in the bat. These studies have also identified a key role of the cholinergic forebrain system in subcortical reorganization.

Abstract

The auditory systems of adult animals can be reorganized by auditory experience. The auditory cortex, the corticofugal system and the cholinergic basal forebrain are crucial for this reorganization. The auditory system can undergo two different forms of reorganization — expansion and compression. Whereas expanded reorganization has been found in different species and different sensory systems, compressed reorganization has only been found in the auditory system of the moustached bat, which is highly specialized for echolocation. Here, we review recent progress in our understanding of the corticofugal system and the reorganization of the auditory system.

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Figure 1: Corticofugal modulation of the auditory responses, frequency-response curves of collicular neurons, and time courses of collicular and cortical best-frequency shifts.
Figure 2: Facilitation of matched neurons, and centripetal or centrifugal best-frequency shifts of unmatched neurons, evoked by electrical stimulation of cortical neurons.
Figure 3: Shifts in best frequency evoked by electrical stimulation of cortical auditory neurons.
Figure 4: Expanded and compressed reorganizations in the auditory cortices of three species of mammal.
Figure 5: Corticofugal modulation of duration-tuned collicular neurons evoked by electrical stimulation of cortical duration-tuned neurons.
Figure 6: Corticofugal modulation of best delays and minimum thresholds.
Figure 7: Working models for the changes in auditory processing during auditory fear conditioning (associative learning).

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Acknowledgements

Our work has been supported by a research grant from the National Institute on Deafness and Other Communication Disorders.

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  1. Department of Biology, Washington University, One Brookings Drive, St Louis, 63130, Missouri, USA

    Nobuo Suga & Xiaofeng Ma

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Correspondence to Nobuo Suga.

Glossary

FEAR CONDITIONING

A form of Pavlovian (classical) conditioning in which an animal learns that an innocuous stimulus (for example, an auditory tone — the conditioned stimulus, CS) comes to reliably predict the occurrence of a noxious stimulus (for example, foot shock — the unconditioned stimulus, US) following their repeated paired presentation. As a result of this procedure, presentation of the CS alone elicits conditioned fear responses previously associated with the US only.

DOPPLER SHIFT

The Austrian physicist C. J. Doppler discovered that a light or sound wave measured by a moving observer will be shifted as a direct function of the speed of the observer and as an inverse function of the speed of the wave. A prototypical example of the Doppler shift is the sound of a train's horn as we stand at a station; the sound is shifted to a higher pitch as the train approaches, and then abruptly to a lower pitch as it passes by.

MICROPHONIC RESPONSE

The summated auditory response of the cochlear hair cells.

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Suga, N., Ma, X. Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4, 783–794 (2003). https://doi.org/10.1038/nrn1222

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