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J Physiol Volume 571, Number 3, 563-578, March 15, 2006 DOI: 10.1113/jphysiol.2005.098780
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Neuroscience

Topographic organization in the auditory brainstem of juvenile mice is disrupted in congenital deafness

Richardson N. Leao1, Hong Sun2, Katarina Svahn1, Amy Berntson1, Monique Youssoufian1, Antonio G. Paolini3, Robert E. W. Fyffe2 and Bruce Walmsley1

1 Synapse and Hearing Laboratory, The John Curtin School of Medical Research, The Australian National University, Canberra, ACT, Australia
2 Department of Neuroscience, Cell Biology and Physiology, Wright State University, Dayton, OH, USA
3 Latrobe University, Melbourne, VIC, Australia

There is an orderly topographic arrangement of neurones within auditory brainstem nuclei based on sound frequency. Previous immunolabelling studies in the medial nucleus of the trapezoid body (MNTB) have suggested that there may be gradients of voltage-gated currents underlying this tonotopic arrangement. Here, our electrophysiological and immunolabelling results demonstrate that underlying the tonotopic organization of the MNTB is a combination of medio-lateral gradients of low-and high-threshold potassium currents and hyperpolarization-activated cation currents. Our results also show that the intrinsic membrane properties of MNTB neurones produce a topographic gradient of time delays, which may be relevant to sound localization, following previous demonstrations of the importance of the timing of inhibitory input from the MNTB to the medial superior olive (MSO). Most importantly, we demonstrate that, in the MNTB of congenitally deaf mice, which exhibit no spontaneous auditory nerve activity, the normal tonotopic gradients of neuronal properties are absent. Our results suggest an underlying mechanism for the observed topographic gradient of neuronal firing properties in the MNTB, show that an intrinsic neuronal mechanism is responsible for generating a topographic gradient of time-delays, and provide direct evidence that these gradients rely on spontaneous auditory nerve activity during development.

(Received 14 September 2005; accepted after revision 12 December 2005; first published online 22 December 2005)
Corresponding author B. Walmsley: Synapse and Hearing Laboratory, Division of Neuroscience, John Curtin School of Medical Research, Australian National University, PO Box 334, Canberra, ACT 0200, Australia. Email: bruce.walmsley{at}anu.edu.au




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