Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish.
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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Robert S. Dow Neurological Sciences Institute, Good Samaritan Hospital, Portland, Oregon 97210.
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D000200:Action Potentials; D000818:Animals; D004555:Electric Fish / Q000502:physiology*; D004557:Electric Organ / Q000166:cytology / Q000294:innervation / Q000502:physiology; D007425:Intracellular Membranes / Q000502:physiology; D009412:Nerve Fibers / Q000502:physiology; D009424:Nervous System Physiological Phenomena; D009433:Neural Inhibition; D009475:Neurons, Afferent / Q000166:cytology; D012677:Sensation / Q000502:physiology*; D013998:Time Perception / Q000502:physiology*