Tonotopic organization of the anteroventral cochlear nucleus of the cat

doi:10.1016/0378-5955(81)90008-3

Hearing Research

Volume 4, Issues 3–4, July 1981, Pages 215-241

https://doi.org/10.1016/0378-5955(81)90008-3 Get rights and content

Abstract

A quantitatively accuiate map of the tonotopic organization of the anteroventral cochlear nucleus (AVCN) was derived from single unit recordings. Histologically localized single unit recordings from many animals were mapped onto a computerized atlas of the cochlear nucleus, and surfaces of constant characteristic frequency (CF) estimated with the aid of computer graphics. In anterior AVCN the surfaces of constant CF were found to be parallel planes, whereas in posterior AVCN they progressively deviated from this simple description. A further complication was noted in the most posterior portion of the AVCN where units with very different CF were found in close proximity. Comparison of the tonotopic map with descriptions of cellular organization shows conclusively that different CF ranges are dominant in the various cytoarchitectonic regions of the AVCN.

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Left DCN was easily identified by its bulgy prominence on the surface of the brainstem and its surface tonotopic organization (Figure S1G, top panels) (Kaltenbach and Lazor, 1991; Young and Brownell, 1976). The anteroventral cochlear nucleus (AVCN) was determined by its relative rostraventral location to DCN and its CF gradients that demarcated the AVCN, as in bottom panels of Figure S1G; the posteroventral cochlear nucleus (PVCN) was identified by its deeper location than DCN and the discontinuity in CF gradients along dorsal-ventral axis when electrodes were moving into PVCN from DCN during penetration (Figure S1G, middle panels) (Bourk et al., 1981; Kopp-Scheinpflug et al., 2002; Young et al., 1988). A guided tube was lowered to penetrate through the right neocortex and positioned above midbrain; recording electrodes were cocentralized with the guiding tube during penetration (Figures S4A and S4B).
Both human speech and animal vocal signals contain frequency-modulated (FM) sounds. Although central auditory neurons that selectively respond to the direction of frequency modulation are known, the synaptic mechanisms underlying the generation of direction selectivity (DS) remain elusive. Here we show the emergence of DS neurons in the inferior colliculus by mapping the three major subcortical auditory nuclei. Cell-attached recordings reveal a highly reliable and precise firing of DS neurons to FM sweeps in a preferred direction. By using in vivo whole-cell current-clamp and voltage-clamp recordings, we found that the synaptic inputs to DS neurons are not direction selective, but temporally reversed excitatory and inhibitory synaptic inputs are evoked in response to opposing directions of FM sweeps. The construction of such temporal asymmetry, resulting DS, and its topography can be attributed to the spectral disparity of the excitatory and the inhibitory synaptic tonal receptive fields.
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Persons who lack an auditory nerve cannot benefit from cochlear implants, but a prosthesis utilizing an electrode array implanted on the surface of the cochlear nucleus can restore some hearing. Worldwide, more than 500 persons have received these “auditory brainstem implants,” most commonly after removal of the tumors that occur with Type 2 Neurofibromatosis (NF2). Typically, the ABIs provide these individuals with improved speech perception when combined with lip-reading and useful perception of environmental sounds, but little open-set speech recognition. The feasibility of supplementing the array of surface electrodes with penetrating microstimulating electrodes has been investigated in animal studies, and 10 persons with NF2 have received implants that include a surface array and an array of penetrating microelectrodes. Their speech perception is not significantly better than that of the NF2 patients who have only the surface arrays, but the findings do validate the concept of intranuclear stimulation and suggest how such prostheses might be improved by modifying the microstimulating array and also by optimizing the sound processing strategies. Recent publications have described ABI patients with deafness of etiologies other than NF2 who have achieved open-set speech recognition. This suggests that the cochlear nuclei of the NF2 patients are damaged by the disease process or during surgical removal of the tumor.
Projections of low spontaneous rate, high threshold auditory nerve fibers to the small cell cap of the cochlear nucleus in cats
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The drawn fiber segments were aligned across serial sections to produce a two-dimensional reconstruction of the entire fiber that was mapped onto the cochlear nucleus. Recovery and identification of the labeled fibers were guided by relative placement of the recording and injecting micropipette in the nerve, cochleotopic projections of auditory nerve fibers (Ryugo and May, 1993; Ryugo and Parks, 2003), and the tonotopic organization of the cochlear nucleus (Bourk et al., 1981). Special attention was given to those collaterals that arborized into the region of the SCC.
The marginal shell of the anteroventral cochlear nucleus houses small cells that are distinct from the overlying microneurons of the granule cell domain and the underlying projection neurons of the magnocellular core. This thin shell of small cells and associated neuropil receives auditory nerve input from only the low (<18 spikes/s) spontaneous rate (SR), high threshold auditory nerve fibers; high SR, low threshold fibers do not project there. It should be noted, that most of these auditory nerve terminations reside in the neuropil and intermix with dendrites that originate outside the shell. Consequently, electron microscopy is necessary to determine the synaptic targets. For this report, the terminations of intracellularly labeled low SR auditory nerve fibers in the small cell of cats cap were mapped through serial sections using a light microscope. The terminals were then examined with an electron microscope and found to form synapses with the somata and dendrites of small cells. Moreover, the small cell dendrites were identifiable by an abundance of microtubules and the presence of polyribosomes that were free or associated with membranous cisterns. These data contribute to the concept of a high threshold feedback circuit to the inner ear, and reveal translational machinery for local control of activity-dependent synaptic modification.
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Tonotopic organization of the anteroventral cochlear nucleus of the cat

Abstract

The cochlear nerve in the cat: topography, cochleotopy, and fiber spectrum

J. Comp. Neurol.

The staining of paraffin sections of nervous tissue with activated protargol, the role of fixatives

Anat. Rec.

Electrical responses of neural units in the anteroventral cochlear nucleus of the cat

The neuronal architecture of the cochlear nucleus of the cat

J. Comp. Neurol.

Axons from noncochlear sources in the anteroventral cochlear nucleus of the cat. A study with the rapid Golgi method

Neuroscience

Organization of the neurons in the anterior division of the anteroventral cochlear nucleus of the cat. Light-microscopic observations

Neuroscience

Tonotopic organization: review and analysis

Brain Res.

The responses of single neurons in the cochlear nucleus of the cat as a function of their location and the anaesthetic state

Exp. Brain Res.

The projection of the acoustic nerve to the ventral cochlear nucleus of the rat. A Golgi study

J. Comp. Neurol.

Spectral and temporal characteristics of activation and suppression of units in the cochlear nuclei of anaesthetized cat

Exp. Brain Res.

Single unit activity in the posteroventral cochlear nucleus of the cat

J. Comp. Neurol.

Single unit activity in the dorsal cochlear nucleus of the cat

J. Comp. Neurol.

Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study

J. Neurophysiol.

Discharge characteristics of neurons in anteroventral and dorsal cochlear nuclei of cat

Brain Res.

Single auditory units in the superior olivary complex II: Locations of unit categories and tonotopic organization

Int. J. Neurosci.

A study of the cochlear nucleus and ascending auditory pathways of the medulla

J. Comp. Neurol.

Stimulus coding in the auditory nerve and cochlear nucleus

Acta OtoLaryngol.

Discharge Patterns of Single Fibers in the Cat's Auditory Nerve

Stimulus coding in the cochlear nucleus

Ann. Otol. Rhinol. Laryngol.

Shapes of tuning curves for single auditory nerve fibers

J. Acoust. Soc. Am.

Auditory-nerve activity in cats with normal and abnormal cochleas