Elsevier

Neuroscience

Volume 136, Issue 4, 2005, Pages 1159-1170
Neuroscience

Systems neuroscience
Spectral integration in the inferior colliculus of the CBA/CaJ mouse

https://doi.org/10.1016/j.neuroscience.2005.08.031Get rights and content

Abstract

The inferior colliculus receives a massive convergence of inputs and in the mustached bat, this convergence leads to the creation of neurons in the inferior colliculus that integrate information across multiple frequency bands. These neurons are tuned to multiple frequency bands or are combination-sensitive; responding best to the combination of two signals of different frequency composition. The importance of combination-sensitive neurons in processing echolocation signals is well described, and it has been thought that combination sensitivity is a neural specialization for echolocation behaviors. Combination sensitivity and other response properties indicative of spectral integration have not been thoroughly examined in the inferior colliculus of non-echolocating mammals. In this study we tested the hypothesis that integration across frequencies occurs in the inferior colliculus of mice. We tested excitatory frequency response areas in the inferior colliculus of unanesthetized mice by varying the frequency of a single tone between 6 and 100 kHz. We then tested combination-sensitive responses by holding one tone at the unit’s best frequency, and varying the frequency and intensity of a second tone. Thirty-two percent of the neurons were tuned to multiple frequency bands, 16% showed combination-sensitive facilitation and another 12% showed combination-sensitive inhibition. These findings suggests that the neural mechanisms underlying processing of complex sounds in the inferior colliculus share some common features among mammals as different as the bat and the mouse.

Section snippets

Experimental procedures

We recorded responses of single neurons in the IC of awake CBA/CaJ mice to single tones and combinations of tones. Animals used in the experiments were two to six months of age. As mice are nocturnal and we wanted their active period to be during the day, they were kept on a 12-h light/dark off/on schedule so that the lights were off during the day. Surgeries were performed early in the morning and electrophysiological recordings began around 10 a.m. of the same day. This increased the

Results

We obtained excitatory frequency tuning curves from 154 single units in the IC. Only responses localized to the central nucleus of the IC were included in the analyses. Characteristic frequencies ranged from 6 and 64 kHz, and there were two peaks in the CF distribution (Fig. 1A). One peak occurred at CFs around 20 kHz and the second peak occurred at CFs near 48 kHz. Of these 154 neurons, 49 (32%) were tuned to more than one frequency band and were classified as multiply tuned. Responses to

Discussion

Fig. 7 summarizes response properties recorded in the mouse IC. The 32% of multiply tuned neurons is similar to the percentage found in the mustached bat IC using a similar experimental paradigm and awake stereotaxic apparatus (Portfors and Wenstrup, 2002). This is higher than has been reported in other species (mouse: Egorova et al., 2001; guinea-pig: LeBeau et al., 2001). Egorova and colleagues found only 6.2% of neurons in the IC of mouse to be multiply tuned. In their study, the frequency

Acknowledgments

This work was supported by NIH/NIDCD grant 04733 to C.V.P. and an underrepresented minorities supplement to R.A.F. We thank Deborah Langley and Don Gans for technical assistance with this project.

References (59)

  • J.F. Willott et al.

    Response properties of inferior colliculus neurons in young and very old CBA/J mice

    Hear Res

    (1988)
  • J.A. Winer et al.

    Descending projections to the inferior colliculus from the posterior thalamus and the auditory cortex in rat, cat, and monkey

    Hear Res

    (2002)
  • A. Brand et al.

    Duration tuning in the mouse auditory midbrain

    J Neurophysiol

    (2000)
  • A.S. Bregman

    Auditory scene analysis

    The perceptual organization of sound

    (1990)
  • J.K. Brunso-Bechtold et al.

    HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus of cat

    J Comp Neurol

    (1981)
  • J.H. Casseday et al.

    Frequency tuning properties of neurons in the inferior colliculus of an FM bat

    J Comp Neurol

    (1992)
  • J.H. Casseday et al.

    The inferior colliculusA hub for the central auditory system

  • E. Covey et al.

    Whole-cell patch-clamp recording reveals subthreshold sound-evoked postsynaptic currents in the inferior colliculus of awake bats

    J Neurosci

    (1996)
  • S.P. Dear et al.

    Delay-tuned neurons in the midbrain of the big brown bat

    J Neurophysiol

    (1995)
  • M. Egorova et al.

    Frequency response areas of neurons in the mouse inferior colliculus. I. Threshold and tuning characteristics

    Exp Brain Res

    (2001)
  • G. Ehret et al.

    The central auditory system

    (1997)
  • K.H. Esser et al.

    Syntax processing by auditory cortical neurons in the FM-FM area of the mustached bat Pteronotus parnellii

    Proc Natl Acad Sci U S A

    (1997)
  • D.B. Geissler et al.

    Time-critical integration of formants for perception of communication calls in mice

    Proc Natl Acad Sci U S A

    (2002)
  • B. Haack et al.

    Sound communication between parents and offspring

  • M.D. Hauser

    The evolution of communication

    (1996)
  • S.C. Kadia et al.

    Spectral integration in A1 of awake primatesneurons with single- and multipeaked tuning characteristics

    J Neurophysiol

    (2003)
  • J.S. Kanwal et al.

    Analysis of acoustic elements and syntax in communication sounds emitted by mustached bats

    J Acoust Soc Am

    (1994)
  • J.S. Kanwal

    Processing species-specific calls by combination-sensitive neurons in an echolocating bat

  • J.S. Kanwal et al.

    Facilitatory and inhibitory frequency tuning of combination-sensitive neurons in the primary auditory cortex of mustached bats

    J Neurophysiol

    (1999)
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