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The projection from auditory cortex to cochlear nucleus in guinea pigs: an in vivo anatomical and in vitro electrophysiological study

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Abstract

Previous anatomical experiments have demonstrated the existence of a direct, bilateral projection from the auditory cortex (AC) to the cochlear nucleus (CN). However, the precise relationship between the origin of the projection in the AC and the distribution of axon terminals in the CN is not known. Moreover, the influence of this projection on CN principal cells has not been studied before. The aim of the present study was two-fold. First, to extend the anatomical data by tracing anterogradely the distribution of cortical axons in the CN by means of restricted injections of biotinylated dextran amine (BDA) in physiologically characterized sites in the AC. Second, in an in vitro isolated whole brain preparation (IWB), to assess the effect of electrical stimulation of the AC on CN principal cells from which intracellular recordings were derived. BDA injections in the tonotopically organized primary auditory cortex and dorsocaudal auditory field at high and low best frequency (BF) sites resulted in a consistent axonal labeling in the ipsilateral CN of all injected animals. In addition, fewer labeled terminals were observed in the contralateral CN, but only in the animals subjected to injections in low BF region. The axon terminal fields consisting of boutons en passant or terminaux were found in the superficial granule cell layer and, to a smaller extent, in the three CN subdivisions. No axonal labeling was seen in the CN as result of BDA injection in the secondary auditory area (dorsocaudal belt). In the IWB, the effects of ipsilateral AC stimulation were tested in a population of 52 intracellulary recorded and stained CN principal neurons, distributed in the three CN subdivisions. Stimulation of the AC evoked slow late excitatory postsynaptic potentials (EPSPs) in only two cells located in the dorsal CN. The EPSPs were induced in a giant and a pyramidal cell at latencies of 20 ms and 33 ms, respectively, suggesting involvement of polysynaptic circuits. These findings are consistent with anatomical data showing sparse projections from the AC to the CN and indicate a limited modulatory action of the AC on CN principal cells.

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Acknowledgements

This work was supported by Swiss National Science Foundation grants No. 31-55836.98 and 31-66731.01, and the National Center of Competence in Research (NCCR) "Neural plasticity and repair".

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Authors and Affiliations

  1. Division of Physiology, Department of Medicine, University of Fribourg, Rue du Musée 5, 1700 Fribourg, Switzerland

    A.-V. Jacomme, A. Babalian & E. M. Rouiller

  2. University Laboratory of Physiology, University of Oxford, Oxford, UK

    F. R. Nodal & V. M. Bajo

  3. NAMC, UMR CNRS 8620, University Paris Sud, Orsay, France

    Y. Manunta & J.-M. Edeline

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  1. A.-V. Jacomme
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  2. F. R. Nodal
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  3. V. M. Bajo
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  4. Y. Manunta
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  5. J.-M. Edeline
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  6. A. Babalian
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  7. E. M. Rouiller
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Correspondence to E. M. Rouiller.

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Jacomme, AV., Nodal, F.R., Bajo, V.M. et al. The projection from auditory cortex to cochlear nucleus in guinea pigs: an in vivo anatomical and in vitro electrophysiological study. Exp Brain Res 153, 467–476 (2003). https://doi.org/10.1007/s00221-003-1606-2

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  • DOI: https://doi.org/10.1007/s00221-003-1606-2

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