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Journal of Neuroscience, Vol 9, 1029-1044, Copyright © 1989 by Society for Neuroscience
Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish
CC Bell and K Grant
Robert S. Dow Neurological Sciences Institute, Good Samaritan Hospital, Portland, Oregon 97210.
Knollenorgan electroreceptors in mormyrid fish are concerned with
electrocommunication, i.e., with detecting electric organ discharges (EODs)
of other electric fish. But knollenorgan electroreceptors are also
activated by the fish's own EOD. Potential interference by such
self-stimulation is blocked by an inhibitory corollary discharge in the
nucleus of the electrosensory lateral line lobe (NELL), the first central
relay of the knollenorgan pathway. This study used intracellular recording
and staining to examine the mechanism of the corollary inhibition and the
specializations in anatomy and physiology that permit the accurate relaying
of temporal information about the EODs of other fish. Several events are
recorded inside primary knollenorgan afferents in addition to a large
orthodromic action potential. The additional events include small
orthodromic electronic epsps, postsynaptic action potentials, and a
corollary discharge inhibitory postsynaptic potential (ipsp) associated
with the EOD motor command. These additional events are also recorded in
NELL cells and almost certainly originate there. Electrical coupling
between afferents and cells makes it possible to observe the events inside
primary afferents. The corollary discharge ipsp in the cell is associated
with a conductance increase and inverts rapidly when recorded with
chloride- containing electrodes, supporting a hypothesis of GABA mediation.
The ipsp lasts longer in cells than in afferents. Each electrotonic
excitatory postsynaptic potential (epsp) is probably caused by a single
primary afferent, and any one of several epsps in a given cell seems
capable of eliciting a postsynaptic spike in that cell. The epsps follow
stimulation rates as high as 500/sec with minimal variability. No lateral
inhibition is observed in NELL. These and other properties indicate that
the knollenorgan pathway is specialized for temporal information rather
than spatial or intensity information.
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