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Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada
Berman, Neil J., James Plant, Ray W. Turner, and Leonard Maler. Excitatory amino acid receptors at a feedback pathway in the electrosensory system: implications for the searchlight hypothesis. J. Neurophysiol. 78: 1869-1881, 1997. The electrosensory lateral line lobe (ELL) of the South American gymnotiform fish Apteronotus leptorhynchus has a laminar structure: electroreceptor afferents terminate ventrally whereas feedback input distributes to a superficial molecular layer containing the dendrites of the ELL principle (pyramidal) cells. There are two feedback pathways: a direct feedback projection that enters the ELL via a myelinated tract (stratum fibrosum, StF) and terminates in the ventral molecular layer (VML) and an indirect projection that enters as parallel fibers and terminates in the dorsal molecular layer. It has been proposed that the direct feedback pathway serves as a "searchlight" mechanism. This study characterizes StF synaptic transmission to determine whether the physiology of the direct feedback projection is consistent with this hypothesis. 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 two current sinks: an early sink within the StF and a later sink that corresponded to the anatomically defined VML. Field potential recordings from VML demonstrated that stimulation of the StF evoked an excitatory postsynaptic potential (EPSP) that peaked at a latency of 4-7 ms with a slow decay (~50 ms) to baseline. Intracellular recordings from pyramidal cells revealed that StF-evoked EPSPs consisted of at least two 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 (~50 ms). The amplitudes of the peak and decay phases of the chemical EPSP were increased by depolarizing current injection. Pharmacological studies demonstrated that the chemical EPSP was mainly due to ionotropic glutamate receptors with bothN-methyl-D-aspartate (NMDA) and non-NMDA components. NMDA receptors contributed substantially to both the early and late phase of the EPSP, whereas non-NMDA receptors contributed mainly to the early phase. 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. 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 electrodetectability of scanned objects.
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A.-M. M. Oswald, J. E. Lewis, and L. Maler Dynamically Interacting Processes Underlie Synaptic Plasticity in a Feedback Pathway J Neurophysiol, May 1, 2002; 87(5): 2450 - 2463. [Abstract] [Full Text] [PDF]
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B. Doiron, A. Longtin, R. W. Turner, and L. Maler Model of Gamma Frequency Burst Discharge Generated by Conditional Backpropagation J Neurophysiol, October 1, 2001; 86(4): 1523 - 1545. [Abstract] [Full Text] [PDF]
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J. Bastian and J. Nguyenkim Dendritic Modulation of Burst-Like Firing in Sensory Neurons J Neurophysiol, January 1, 2001; 85(1): 10 - 22. [Abstract] [Full Text] [PDF]
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E. S. Fortune and G. J. Rose Short-Term Synaptic Plasticity Contributes to the Temporal Filtering of Electrosensory Information J. Neurosci., September 15, 2000; 20(18): 7122 - 7130. [Abstract] [Full Text] [PDF]
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S. Curti, A. Falconi, F. R. Morales, and M. Borde Mauthner Cell-Initiated Electromotor Behavior Is Mediated via NMDA and Metabotropic Glutamatergic Receptors on Medullary Pacemaker Neurons in a Gymnotid Fish J. Neurosci., October 15, 1999; 19(20): 9133 - 9140. [Abstract] [Full Text] [PDF]
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G. Rose and E. Fortune Mechanisms for generating temporal filters in the electrosensory system J. Exp. Biol., January 5, 1999; 202(10): 1281 - 1289. [Abstract] [PDF]
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J Bastian Plasticity of feedback inputs in the apteronotid electrosensory system J. Exp. Biol., January 5, 1999; 202(10): 1327 - 1337. [Abstract] [PDF]
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N. J. Berman and L. Maler Inhibition Evoked From Primary Afferents in the Electrosensory Lateral Line Lobe of the Weakly Electric Fish (Apteronotus leptorhynchus) J Neurophysiol, December 1, 1998; 80(6): 3173 - 3196. [Abstract] [Full Text] [PDF]
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N. J. Berman and L. Maler Interaction of GABAB-Mediated Inhibition With Voltage-Gated Currents of Pyramidal Cells: Computational Mechanism of a Sensory Searchlight J Neurophysiol, December 1, 1998; 80(6): 3197 - 3213. [Abstract] [Full Text] [PDF]
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N. J. Berman and L. Maler Distal Versus Proximal Inhibitory Shaping of Feedback Excitation in the Electrosensory Lateral Line Lobe: Implications for Sensory Filtering J Neurophysiol, December 1, 1998; 80(6): 3214 - 3232. [Abstract] [Full Text] [PDF]
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K. Grant, Y. Sugawara, L. Gomez, V. Z. Han, and C. C. Bell The Mormyrid Electrosensory Lobe In Vitro: Physiology and Pharmacology of Cells and Circuits J. Neurosci., August 1, 1998; 18(15): 6009 - 6025. [Abstract] [Full Text] [PDF]
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D. Bottai, L. Maler, and R. J. Dunn Alternative RNA Splicing of the NMDA Receptor NR1 mRNA in the Neurons of the Teleost Electrosensory System J. Neurosci., July 15, 1998; 18(14): 5191 - 5202. [Abstract] [Full Text] [PDF]
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J. Bastian Plasticity in an Electrosensory System. III. Contrasting Properties of Spatially Segregated Dendritic Inputs J Neurophysiol, April 1, 1998; 79(4): 1839 - 1857. [Abstract] [Full Text] [PDF]
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W. Metzner, C. Koch, R. Wessel, and F. Gabbiani Feature Extraction by Burst-Like Spike Patterns in Multiple Sensory Maps J. Neurosci., March 15, 1998; 18(6): 2283 - 2300. [Abstract] [Full Text] [PDF]
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D. Wang and L. Maler In Vitro Plasticity of the Direct Feedback Pathway in the Electrosensory System of Apteronotus leptorhynchus J Neurophysiol, October 1, 1997; 78(4): 1882 - 1889. [Abstract] [Full Text] [PDF]
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