Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons

doi:10.1016/S0306-4522(03)00207-0

Neuroscience

Volume 119, Issue 4, 16 July 2003, Pages 1085-1101

https://doi.org/10.1016/S0306-4522(03)00207-0 Get rights and content

Abstract

The trigeminal ganglion sends a projection to the granule and magnocellular regions of the ventral cochlear nucleus (VCN; [J Comp Neurol 419 (2000) 271]), as well as to the cochlea ([Neuroscience 79 (1997) 605; Neuroscience 84 (1998a) 559]). We investigated the effects of electrically stimulating the trigeminal ganglion on unit responses in the guinea-pig VCN. Responses consisted of one, two or more phases of excitation, sometimes followed by a longer inhibitory phase. The latencies to the first excitation peak ranged between 5 and 17 ms from the onset of stimulation. These responses were preceded by a slow wave potential evoked by the stimulation. Applying kainic acid, which eliminates VIIIth nerve responses, diminished the firing rates of VCN units to trigeminal stimulation, and increased their first spike latencies. Cochlear destruction had a similar effect. The responses in VCN evoked by trigeminal ganglion stimulation therefore appear to result from direct stimulation of the trigeminal ganglion—cochlear nucleus pathway, as well as modulation by the trigeminal ganglion—cochlear pathway. Alternatively, a reduction in spontaneous rate of VCN neurons by removal of VIIIth nerve input could explain the decreased response to trigeminal stimulation after cochlear manipulations. The modulation of firing rate in second order auditory neurons by first order somatosensory neurons could influence central auditory targets and may be involved in generating or modulating perceptions of phantom sounds which can be modified by manipulations of somatic regions of the head and neck (“somatic tinnitus”).

Section snippets

Experimental procedures

Experiments were performed on 40 healthy female, adult pigmented guinea-pigs (National Institutes of Health outbred strain) with normal Preyer's reflexes, weighing 250–350 g. All procedures were performed in accordance with the NIH guidelines for the care and use of laboratory animals (NIH publication no. 80-23), and guidelines provided by the University of Michigan. These guidelines minimise the number of animals used and their suffering.

Vcn unit responses to trigeminal ganglion stimulation

Results are based on responses from 410 units. All the responses were sorted using principal component analysis to remove the artifact (Fig. 3A). Of the sorted responses approximately 2/3 were considered multi-unit. The remaining 1/3 were considered single unit responses. For these units, trigeminal ganglion stimulation elicited primarily excitatory responses from VCN neurons. Scatter plots of unit response rates as a function of location in the VCN are shown for one level of current applied to

Activation of VCN neurons by trigeminal ganglion stimulation

Electrical stimulation of the trigeminal ganglion resulted primarily in excitation, sometimes followed by inhibition, of VCN neurons, demonstrating a functional connection between the trigeminal nerve and the VCN. Previous studies have demonstrated that electrical stimulation of second-order somatosensory nuclei, the dorsal column and trigeminal nuclei, inhibited cells in the superficial and deep layers of DCN and excited cells in the VCN Saade et al., 1989, Young et al., 1995, Davis et al.,

Acknowledgements

We are grateful to Mazy Bissinger for excellent histological reconstructions and to Chris Ellinger for invaluable electronic assistance. The center for neural communication technology (CNCT) in the Department of Engineering supplied the multichannel electrodes, and Sandy Bledsoe contributed valuable comments on the manuscript. This work was supported by grants from the American Tinnitus Association and NIH grant 5 R01 DC004825-03 awarded to S. Shore.

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Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons

Abstract

Section snippets

Experimental procedures

Vcn unit responses to trigeminal ganglion stimulation

Activation of VCN neurons by trigeminal ganglion stimulation

Acknowledgements

Hear Res

Brain Res

Brain Res

Response initiation sites and temporal fine structure. Hear Res

Neurosci Res

Hear Res

Hear Res

Brain Res

Hear Res

Hear Res

Hear Res

Hear Res

Single fiber recordings. Hear Res

Hear Res

Neuroscience

Neuroscience

Exp Neurol

Neuroscience

Neuroscience

Synaptic input to cochlear nucleus dendrites that receive medial olivocochlear synapses

J Comp Neurol

Fiber pathways and branching patterns of biocytin-labeled olivocochlear neurons in the mouse brainstem

J Comp Neurol

Transneuronal labeling of cochlear nucleus neurons by HRP-labeled auditory nerve fibers and olivocochlear branches in mice

J Comp Neurol