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The Journal of Neuroscience, March 31, 2004, 24(13):3199-3209; doi:10.1523/JNEUROSCI.4419-03.2004

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Behavioral/Systems/Cognitive
Common Sensory Inputs and Differential Excitability of Segmentally Homologous Reticulospinal Neurons in the Hindbrain

Hisako Nakayama¹ and Yoichi Oda^2,3

¹Division of Biophysical Engineering, Graduate School of Engineering Science, and ²Neuroscience Laboratories, Graduate School of Frontier Biosciences, Osaka University, and ³Precursory Research for Embryonic Science and Technology, Toyonaka, Osaka 560-8531, Japan

In the hindbrain of zebrafish and goldfish, reticulospinal (RS) neurons are arranged in seven segments, with segmental homologs in adjacent segments. The Mauthner cell (M-cell) in the fourth segment (r4) is known to trigger fast escape behavior. Its serial homologs, MiD2cm in r5 and MiD3cm in r6, are predicted to contribute to this behavior, which can be evoked by head-tap stimuli. However, little is known about their input–output properties. Therefore, we studied afferent projections from the auditory posterior eighth nerve (pVIIIn) and firing properties of MiD2cm and MiD3cm for comparison with the M-cell in adult goldfish. Labeling of RS neurons and the pVIIIn afferents with fluorescent tracers showed that the pVIIIn projected to r4–r6. Tone burst and electrical stimulation of the pVIIIn evoked EPSPs in the M-cell, MiD2cm, and MiD3cm. Stepwise depolarization typically elicited a single spike at the onset in the M-cell but repetitive spiking in MiD2cm and MiD3cm. This atypical property of the M-cell was mediated by dendrotoxin-I (DTX-I)-sensitive voltage-gated potassium channels together with recurrent inhibition, because combined application of DTX-I, strychnine, and bicuculline led to continuous repetitive firing in M-cells. The M-cell but not MiD2cm or MiD3cm expressed Kv1.2, a DTX-I-sensitive potassium channel subunit. Thus, the M-cell and its segmental homologs may sense common auditory information but send different outputs to the spinal circuits to control adaptive escape behavior.

Key words: Mauthner cell; reticulospinal neurons; segmental homologs; eighth nerve afferents; recurrent inhibition; dendrotoxin

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Received Sep 30, 2003; revised January 26, 2004; accepted January 26, 2004.

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