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Journal of Neuroscience, Vol 14, 6453-6471, Copyright © 1994 by Society for Neuroscience
TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron
RW Turner, L Maler, T Deerinck, SR Levinson and MH Ellisman
Department of Anatomy and Neurobiology, University of Ottawa, Ontario, Canada.
Immunocytochemical and electrophysiological techniques were used to
localize TTX-sensitive sodium channels (NaChs) over the soma-dendritic axis
of basilar and nonbasilar pyramidal cells of the electrosensory lateral
line lobe (ELL) of weakly electric fish (Apteronotus leptorhynchus). Dense
NaCh-like immunolabel was detected on the membranes of basilar and
nonbasilar pyramidal cell somata. Punctate regions of immunolabel
(approximately 15 microns) were separated by nonlabeled expanses of
membrane over the entire extent of basal dendrites. Similar punctate
immunolabel was observed over the apical dendrites, and frequently on
membranes of afferent parallel fiber boutons in the distal apical dendritic
region. Intracellular recordings from pyramidal cell somata or proximal
apical dendrites (75-200 microns) were obtained using an in vitro ELL slice
preparation. TTX- sensitive potentials were identified by focal pressure
ejection of TTX. Somatic recordings demonstrated both TTX-sensitive fast
spike discharge and a slow prepotential; similar but lower amplitude
potentials were recorded in apical dendrites. Dendritic spikes were
composed of at least two active components triggered by a fast prepotential
(FPP) generated by the somatic spike. TTX-sensitive spikes propagated in a
retrograde fashion over at least the proximal 200 microns of the apical
dendrites, as determined by the conduction of an antidromic population
spike and focal TTX ejections. Somatic spikes were followed by a
depolarizing afterpotential (DAP) that was similar in duration and
refractory period to that of proximal dendritic spikes. During repetitive
spike discharge, the DAP could increase in amplitude and attain somatic
spike threshold, generating a high-frequency spike doublet and a subsequent
hyperpolarization that terminated spike discharge. Repetition of this
process gave rise to an oscillatory burst discharge (2-6 spikes/burst) with
a frequency of 40-80 Hz. Both the DAP and oscillatory discharge were
selectively blocked by TTX ejections restricted to the proximal apical
dendritic region. The present study demonstrates an immunolocalization of
NaChs over somatic and dendritic membranes of a vertebrate sensory neuron
that correlates with the distribution of TTX-sensitive potentials. The
interaction of somatic and dendritic action potentials is further shown to
underlie an oscillatory discharge believed to be important in
electrosensory processing.
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