Dissecting the circuitry of the auditory system

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Abstract

The brainstem auditory system is a complex system composed of numerous parallel and serial pathways that converge on a common destination in the inferior colliculus (IC). The exact nature of the response transformations that occur in the IC have, however, been elusive – even though the IC has been the subject of numerous studies for more than 30 years. Recent studies have addressed this issue by recording from IC neurons before and during micro-iontophoresis of drugs that selectively block GABAA or glycine receptors (the dominant inhibitory receptors in the IC) or by reversibly inactivating a lower nucleus that provides inhibitory innervation to the IC. These studies have revealed some of the ways that signals, relayed via many different parallel routes, interact in the IC, and suggest some functional advantages that these interactions might have.

Section snippets

IC neurons and lower auditory nuclei often have similar response properties

Similar response properties in IC and lower nuclei are well illustrated by neurons that are excited by stimulation of one ear and inhibited by stimulation of the other ear (EI neurons). These neurons encode interaural intensity disparities (IIDs), the principal cues animals use to localize high frequency sounds [21]. EI properties are revealed by simply presenting a sound of fixed intensity to the excitatory ear and simultaneously presenting sounds of progressively increasing intensity to the

EI neurons are formed in multiple ways in the IC

Subjecting IC neurons to more challenging tests, however, reveals that the EI properties of many IC cells are not simply a reflection of LSO projections. The first question these tests were designed to answer is simple: does the actual inhibition evoked by stimulation of the inhibitory ear occur in the IC or does it occur in a lower nucleus, presumably the LSO? If the inhibition occurs in the LSO, then blocking inhibition at the IC cell should have no effect on ipsilaterally evoked inhibition;

Properties of DNLL neurons predict emergent properties of some EI neurons in the IC

The DNLL, like the IC, receives a large complement of inputs from lower nuclei 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45 and the neurons within it that are tuned to high frequencies are predominately, if not exclusively, EI 24, 26, 27, 46. Stimulation of the contralateral (excitatory) ear typically evokes a strong, sustained discharge train 13, 47, 48 (Fig. 4). The duration of the discharge train corresponds to the duration of the stimulus, and is never longer. By contrast,

Functional relevance of emergent properties resulting from DNLL innervation

The demonstration that an initial signal can change the responsiveness of IC cells to a trailing signal suggests that the DNLL circuitry could contribute to a precedence-like effect 12, 51. The precedence effect, or law of the first wavefront, was discovered in human psychophysical studies and is due to a mechanism that suppresses the directional information carried by echoes. It explains how, in a reverberant room, a listener can localize only the first sound and not the sequence of echoes

Concluding comments

The circuitry linking the LSO, DNLL and IC can serve as a model for a more general understanding of how the integration of incoming information creates complex, but biologically meaningful, properties within the IC. Although the variety of response transformations that occur in the IC is far larger than described here for EI cells 12, 20, 60, 61, 62, 63, 64, 65, we now have a better understanding of roles played by innervation from the DNLL for binaural processing. The significance of this is

Acknowledgements

We thank Eric Bauer for his helpful comments. Our work is supported by NIH grant DC 00268.

References (65)

  • D. Oertel

    The role of timing in the brain stem auditory nuclei of vertebrates

    Annu. Rev. Physiol.

    (1999)
  • L.S. Ross

    Origin of ascending projections to an isofrequency region of the mustache bat's inferior colliculus

    J. Comp. Neurol.

    (1988)
  • G.L. Roth

    Some features of the spatial organization of the central nucleus of the inferior colliculus of the cat

    J. Comp. Neurol.

    (1978)
  • D.L. Oliver

    Inferior and superior colliculi

  • M.B. Calford

    Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus

    J. Neurosci.

    (1983)
  • J.A. Winer

    Functional architecture of the medial geniculate body and primary auditory cortex

  • K.A. Davis

    Single-unit responses in the inferior colliculus of decerebrate cats. II. Sensitivity to interaural level differences

    J. Neurophysiol.

    (1999)
  • R. Ramachandran

    Single-unit responses in the inferior colliculus of decerebrate cats. I. Classification based on frequency response maps

    J. Neurophysiol.

    (1999)
  • K.A. Davis

    Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus

    J. Neurophysiol.

    (2002)
  • R.M. Burger

    Analysis of the role of inhibition in shaping responses to sinusoidally amplitude-modulated signals in the inferior colliculus

    J. Neurophysiol.

    (1998)
  • A. Klug

    Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat

    J. Neurophysiol.

    (1995)
  • R.M. Burger

    Reversible inactivation of the dorsal nucleus of the lateral lemniscus reveals its role in the processing of multiple sound sources in the inferior colliculus of bats

    J. Neurosci.

    (2001)
  • A. Klug

    Multiple components of ipsilaterally evoked inhibition in the inferior colliculus

    J. Neurophysiol.

    (1999)
  • L. Yang

    GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus

    J. Neurophysiol.

    (1992)
  • U. Koch

    GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat

    J. Neurophysiol.

    (1998)
  • T.J. Park

    A novel circuit in the bat's midbrain recruits neurons into sound localization processing

    Naturwissenschaften

    (1998)
  • D. McAlpine

    Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus

    J. Neurosci.

    (2002)
  • F.E. LeBeau

    Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig

    J. Neurosci.

    (2001)
  • S.D. Erulkar

    Comparative aspects of spatial localization of sounds

    Physiol. Rev.

    (1972)
  • J.C. Boudreau

    Binaural interaction in the cat superior olive S segment

    J. Neurophysiol.

    (1968)
  • M.J. Moore

    Strychnine blocks binaural inhibition in lateral superior olivary neurons

    J. Neurosci.

    (1983)
  • J.F. Brugge

    Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation

    J. Neurophysiol.

    (1970)
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