Connections and frequency representation in the auditory brainstem of the mustache bat, Pteronotus parnellii

Authors

  • John M. Zook,

    Corresponding author
    1. Department of Zoological and Biomedical Sciences and Dept of Basic Sciences, COM, Ohio University, Athens, Ohio 45701 and Department of Zoology, University of Texas, Austin, Texas 78712
    • Dept. of Zoological & Biomedical Sciences, Ohio University, Athens, OH 45701
    Search for more papers by this author
  • Patricia A. Leake

    1. Department of Otolaryngology, University of California, San Francisco, California 94143
    Search for more papers by this author

Abstract

The goals of this study were to describe the cochlear frequency map of the mustache bat, Pteronotus parnellii, and to relate the organization of cochlear primary afferents to that of the second-order projections from the cochlear nucleus to the superior olivary complex. Small deposits of horseradish peroxidase (HRP) were placed in the cochlear nucleus at sites that were physiologically characterized with respect to unit-best frequency. From the deposits, labeled fibers were traced in the retrograde direction to the cochlea and in the anterograde direction to the superior olive.

Cochleas from both experimental and control animals were examined with light and electron microscopy. The peripheral axons of spiral ganglion neurons were counted in order to quantify the unusual variation in the innervation density along the cochlear spiral of the mustache bat. Regions of increased innervation density were found at the beginning and end of the basal turn of the cochlea. The highest cochlear innervation density consistently occurred in the upper basal turn. In horseradish peroxidase tracing experiments, this region contained labeled fibers only when HRP deposits were made at sites within the cochlear nucleus with unit-best frequencies around 60 kHz. These findings support the suggestion (Kössl and Vater, '85) that the cochlear sites of increased innervation density are related to the neural and behavioral emphasis that this echolocating bat places upon the analysis of the 60 kHz frequency band.

The general arrangement of tonotopic maps within the cochlea, cochlear nucleus, and superior olive was consistent with previous observations in this bat and other mammalian species. At all three levels, there was evidence of a disproportionately large representation of frequencies around 60 kHz, similar to the enlarged representation reported within the inferior colliculus and auditory cortex of the mustache bat. In all cases there was a consistent relation between the size of the HRP deposit and the number and distribution of retrogradely labeled neurons in the cochlea. For most cases there was a similar relation between the size of the deposit and the terminal arborization field of anterogradely labeled fibers in the superior olive. However, in cases with deposits associated with the 60 kHz frequency band, the size of the labeled arborization field was more than twice as large as expected from the size of the deposits and from the extent of labeling in the cochlea. These cases suggest that the representation of frequencies around 60 kHz, already overrepresented in both the cochlea and cochlear nucleus, may be further expanded at the level of the superior olivary complex.

Ancillary