Excitatory Amino Acid Receptors at a Feedback Pathway in the Electrosensory System: Implications for the Searchlight Hypothesis

Abstract

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 ( approximately 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 ( approximately 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--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.

Excitatory Amino Acid Receptors of the Electrosensory System: The NR1/NR2BN-Methyl-d-Aspartate Receptor

“…The concentration of Mg 2ϩ in the plasma of freshwater fish is estimated to be between 0.8 and 1.7 mM (McDonald and Milligan 1992), only slightly lower than mammals. Thus the reduced Mg 2ϩ affinity may contribute to the previous observation that NMDA receptors at feedback synapses in the electrosensory lateral line lobe are active at hyperpolarized potentials approaching Ϫ70 mV (Berman et al 1997(Berman et al , 2001.…”

“…Glutamate-induced synaptic responses mediated by the NMDA class of glutamate receptors have been demonstrated in the nervous systems of a variety of vertebrate species, including teleost fish (Berman et al 1997;Curti et al 1999;Han et al 2000;Smeraski et al 1999;Spiro 1997;Wolszon et al 1997). To this date, the molecular analysis of the nonmammalian NMDA receptors has been limited to the NR1 subunit, with sequences reported for NR1 proteins from Xenopus (Soloviev et al 1996), duck (Kurosawa et al 1994), and apteronotid fish (Bottai et al 1998).…”

“…Critical sensory processes such as adaptation and attention are controlled from higher centers through feedback inputs to neurons in the ELL. Glutamate is the predominant excitatory neurotransmitter in the feedback and afferent projections to the ELL, with both N-methyl-D-aspartate (NMDA) and non-NMDA components to the synaptic responses (Bastian 1993;Berman et al 1997).…”

Parallel Processing of Sensory Input by Bursts and Isolated Spikes

“…Transverse brain slices from the ELL of A. leptorhynchus were prepared in accordance with animal care protocols of the University of Ottawa as described previously (Berman et al, 1997). The slices were maintained at room temperature (20 -22°C) in oxygenated artificial CSF (ACSF) for 1-2 hr before recording.…”

“…The pyramidal cell layer is located just below the stratum fibrosum (StF), an easily identifiable landmark in the ELL slice (Berman et al, 1997). Intracellular recordings from 37 ELL pyramidal cells from the entire pyramidal cell layer were made using 80 -120 M⍀ boroscillate glass electrodes, pulled by a Brown-Flaming P-87 puller (Sutter Instruments, Novato, CA), and filled with 2 M KAc.…”