Excitatory Amino Acid Receptors at a Feedback Pathway in the Electrosensory
System: Implications for the Searchlight Hypothesis
Neil J. Berman, James Plant, Ray W. Turner and Leonard Maler
Department of Anatomy and Neurobiology, University of Ottawa, Ottawa,
Ontario K1H 8M5, Canada, Department of Psychology, University of Victoria, PO
Box 3050, Victoria, B.C., Dept. of Anatomy, University of Calgary, Calgary, Alberta
APStracts 4:112N, 1997.
ABSTRACT
1. The electrosensory lateral line lobe (ELL) of the South American
gymnotiform fish Apteronotus leptorhynchus has a laminar structure:
electroreceptor afferents terminate ventrally while feedback input distributes
to a superficial molecular layer containing the dendrites of the ELL principle
(pyramidal) cells. There are 2 feedback pathways: a direct feedback projection
which enters the ELL via a myelinated tract (stratum fibrosum, StF) and
terminates in the ventral molecular layer (VML), and an indirect projection
which enters as parallel fibers and terminates in the dorsal molecular layer
(DML). It has been proposed that the direct feedback pathway serves as a
ÒsearchlightÓ mechanism. This study characterizes StF synaptic transmission in
order to determine whether the physiology of the direct feedback projection is
consistent with this hypothesis.
2. We used field and intracellular recordings from the ELL to investigate
synaptic transmission of the StF in an in vitro slice preparation. Stimulation
of the StF produced field potentials with a maximal negativity confined to a
narrow band of tissue dorsal to the StF. Current source density analysis
revealed 2 current sinks: an early sink within the StF and a later sink that
corresponded to the anatomically defined VML.
3. Field potential recordings from VML demonstrated that stimulation of the
StF evoked an EPSP which peaked at a latency of 4-7 ms with a slow decay (ÿ7E50
ms) to baseline. Intracellular recordings from pyramidal cells revealed that
StF-evoked EPSPs consisted of at least 2 components: a fast gap junction
mediated EPSP (peak 1.2-1.8 ms) and a chemical synaptic potential (peak 4-7
ms) with a slow decay phase (ÿ7E50 ms). The amplitudes of the peak and decay
phases of the chemical EPSP were increased by depolarizing current injection.
4. Pharmacological studies demonstrated that the chemical EPSP was mainly due
to ionotropic glutamate receptors with both NMDA and non-NMDA components. NMDA
receptors contributed substantially to both the early and late phase of the
EPSP, while non-NMDA receptors contributed mainly to the early phase.
5. Stimulation of the StF at physiological rates (100-200 Hz, 100 ms) produced
an augmenting depolarization of the membrane potential of pyramidal cells.
Temporal summation and a voltage dependent enhancement of later EPSPs in the
stimulus train permitted the compound EPSP to reach spike threshold.
6. The nonlinear behavior of StF synaptic potentials is appropriate for the putative role of the direct feedback pathway as part of a searchlight
mechanism allowing these fish to increase the electro-detectability of scanned
objects.
Received 16 June 1997; accepted in final form 18 June 1997.
APS Manuscript Number J277-7.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 15 July 1997