The Journal of Neurophysiology Vol. 81 No. 1 January 1999, pp. 15-28
Copyright ©1999 The American Physiological Society

Current-Source Density Analysis in the Rat Olfactory Bulb: Laminar Distribution of Kainate/AMPA- and NMDA-Receptor-Mediated Currents

Vassiliki Aroniadou-Anderjaska, Matthew Ennis, and Michael T. Shipley

Department of Anatomy and Neurobiology and Program in Neuroscience, University of Maryland School of Medicine, Baltimore, Maryland 21201

Aroniadou-Anderjaska, Vassiliki, Matthew Ennis, and Michael T. Shipley. Current-source density analysis in the rat olfactory bulb: laminar distribution of kainate/AMPA- and NMDA-receptor-mediated currents. J. Neurophysiol. 81: 15-28, 1999. The one-dimensional current-source density method was used to analyze laminar field potential profiles evoked in rat olfactory bulb slices by stimulation in the olfactory nerve (ON) layer or mitral cell layer (MCL) and to identify the field potential generators and the characteristics of synaptic activity in this network. Single pulses to the ON evoked a prolonged (400 ms) sink (S1_ON) in the glomerular layer (GL) with corresponding sources in the external plexiform layer (EPL) and MCL and a relatively brief sink (S2_ON) in the EPL, reversing in the internal plexiform and granule cell layers. These sink/source distributions suggested that S1_ON and S2_ON were generated in the apical dendrites of mitral/tufted cells and granule cells, respectively. The kainate/AMPA-receptor antagonist CNQX (10 µM) reduced the early phase of S1_ON, blocked S2_ON, and revealed a low amplitude, prolonged sink at the location of S2_ON in the EPL. Reduction of Mg²⁺, in CNQX, enhanced both the CNQX-resistant component of S1_ON and the EPL sink. This EPL sink reversed below the MCL, suggesting it was produced in granule cells. The NMDA-receptor antagonist APV (50 µM) reversibly blocked the CNQX-resistant field potentials in all layers. Single pulses were applied to the MCL to antidromically depolarize the dendrites of mitral/tufted cells. In addition to synaptic currents of granule cells, a low-amplitude, prolonged sink (S1_mcl) was evoked in the GL. Corresponding sources were in the EPL, suggesting that S1_mcl was generated in the glomerular dendritic tufts of mitral/tufted cells. Both S1_mcl and the granule cell currents were nearly blocked by CNQX (10 µM) but enhanced by subsequent reduction of Mg²⁺; these currents were blocked by APV. S1_mcl also was enhanced by -aminobutyric acid-A-receptor antagonists applied to standard medium; this enhancement was reduced by APV. ON activation produces prolonged excitation in the apical dendrites of mitral/tufted cells, via kainate/AMPA and NMDA receptors, providing the opportunity for modulation and integration of sensory information at the first level of synaptic processing in the olfactory system. Granule cells respond to input from the lateral dendrites of mitral/tufted cells via both kainate/AMPA and NMDA receptors; however, in physiological concentrations of extracellular Mg²⁺, NMDA-receptor activation does not contribute significantly to the granule cell responses. The glomerular sink evoked by antidromic depolarization of mitral/tufted cell dendrites suggests that glutamate released from the apical dendrites of mitral/tufted cells may excite the same or neighboring mitral/tufted cell dendrites.

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