Journal of Neurophysiology, Vol 64, Issue 3 932-947, Copyright © 1990 by APS

ARTICLES

Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation

D. P. Wellis and J. W. Scott
Department of Anatomy and Cell Biology, Emory University School of Medicine, Atlanta, Georgia 30322.

1. Intracellular recordings were made from 28 granule cells and 6 periglomerular cells of the rat olfactory bulb during odor stimulation and electrical stimulation of the olfactory nerve layer (ONL) and lateral olfactory tract (LOT). Neurons were identified by injection of horseradish peroxidase (HRP) or biocytin and/or intracellular response characteristics. Odorants were presented in a cyclic sniff paradigm, as reported previously. 2. All interneurons could be activated from a wide number of stimulation sites on the ONL, with distances exceeding their known dendritic spreads and the dispersion of nerve fibers within the ONL, indicating that multisynaptic pathways must also exist at the glomerular region. All types of interneurons also responded to odorant stimulation, showing a variety of responses. 3. Granule cells responded to electrical stimulation of the LOT and ONL as reported previously. However, intracellular potential, excitability, and conductance analysis suggested that the mitral cell-mediated excitatory postsynaptic potential (EPSP) is followed by a long inhibitory postsynaptic potential (IPSP). An early negative potential, before the EPSP, was also observed in every granule cell and correlated with component I of the extracellular LOT-induced field potential. We have interpreted this negativity as a "field effect," that may be diagnostic of granule cells. 4. Most granule cells exhibited excitatory responses to odorant stimulation. Odors could produce spiking responses that were either nonhabituating (response to every sniff) or rapidly habituating (response to first sniff only). Other granule cells, while spiking to electrical stimulation, showed depolarizations that did not evoke spikes to odor stimulation. These depolarizations were transient with each sniff or sustained across a series of sniffs. These physiological differences to odor stimulation correlated with granule cell position beneath the mitral cell layer for 12 cells, suggesting that morphological subtypes of granule cells may show physiological differences. Some features of the granule cell odor responses seem to correlate with some of the features we have observed in mitral/tufted cell intracellular recordings. Only one cell showed inhibition to odors. 5. Periglomerular (PG) cells showed a response to ONL stimulation that was unlike that found in other olfactory bulb neurons. There was a long-duration hyperpolarization after a spike and large depolarization or burst of spikes (20-30 ms in duration). Odor stimulation produced simple bursts of action potentials, Odor stimulation produced simple bursts of action potentials, suggesting that PG cells may simply follow input from the olfactory nerve.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				N. Karpuk and A. Hayar Activation of Postsynaptic GABAB Receptors Modulates the Bursting Pattern and Synaptic Activity of Olfactory Bulb Juxtaglomerular Neurons J Neurophysiol, January 1, 2008; 99(1): 308 - 319. [Abstract] [Full Text] [PDF]

				A. Hayar and M. Ennis Endogenous GABA and Glutamate Finely Tune the Bursting of Olfactory Bulb External Tufted Cells J Neurophysiol, August 1, 2007; 98(2): 1052 - 1056. [Abstract] [Full Text] [PDF]

				H.-W. Dong, A. Hayar, and M. Ennis Activation of Group I Metabotropic Glutamate Receptors on Main Olfactory Bulb Granule Cells and Periglomerular Cells Enhances Synaptic Inhibition of Mitral Cells J. Neurosci., May 23, 2007; 27(21): 5654 - 5663. [Abstract] [Full Text] [PDF]

				T. Heinbockel, K. A. Hamilton, and M. Ennis Group I Metabotropic Glutamate Receptors Are Differentially Expressed by Two Populations of Olfactory Bulb Granule Cells J Neurophysiol, April 1, 2007; 97(4): 3136 - 3141. [Abstract] [Full Text] [PDF]

				R. Balu and B. W. Strowbridge Opposing Inward and Outward Conductances Regulate Rebound Discharges in Olfactory Mitral Cells J Neurophysiol, March 1, 2007; 97(3): 1959 - 1968. [Abstract] [Full Text] [PDF]

				Z. Zhou, W. Xiong, A. V. Masurkar, W. R. Chen, and G. M. Shepherd Dendritic Calcium Plateau Potentials Modulate Input-Output Properties of Juxtaglomerular Cells in the Rat Olfactory Bulb J Neurophysiol, November 1, 2006; 96(5): 2354 - 2363. [Abstract] [Full Text] [PDF]

				D. Rinberg, A. Koulakov, and A. Gelperin Sparse odor coding in awake behaving mice. J. Neurosci., August 23, 2006; 26(34): 8857 - 8865. [Abstract] [Full Text] [PDF]

				D. B. Rubin and T. A. Cleland Dynamical Mechanisms of Odor Processing in Olfactory Bulb Mitral Cells J Neurophysiol, August 1, 2006; 96(2): 555 - 568. [Abstract] [Full Text] [PDF]

				N. Buonviso, C. Amat, and P. Litaudon Respiratory Modulation of Olfactory Neurons in the Rodent Brain Chem Senses, February 1, 2006; 31(2): 145 - 154. [Abstract] [Full Text] [PDF]

				V. Egger, K. Svoboda, and Z. F. Mainen Dendrodendritic Synaptic Signals in Olfactory Bulb Granule Cells: Local Spine Boost and Global Low-Threshold Spike J. Neurosci., April 6, 2005; 25(14): 3521 - 3530. [Abstract] [Full Text] [PDF]

				G. Pinato and J. Midtgaard Dendritic Sodium Spikelets and Low-Threshold Calcium Spikes in Turtle Olfactory Bulb Granule Cells J Neurophysiol, March 1, 2005; 93(3): 1285 - 1294. [Abstract] [Full Text] [PDF]

				P.-M. Lledo, A. Saghatelyan, and M. Lemasson Inhibitory Interneurons in the Olfactory Bulb: From Development to Function Neuroscientist, August 1, 2004; 10(4): 292 - 303. [Abstract] [PDF]

				A. Hayar, S. Karnup, M. T. Shipley, and M. Ennis Olfactory Bulb Glomeruli: External Tufted Cells Intrinsically Burst at Theta Frequency and Are Entrained by Patterned Olfactory Input J. Neurosci., February 4, 2004; 24(5): 1190 - 1199. [Abstract] [Full Text] [PDF]

				G. Pinato and J. Midtgaard Regulation of Granule Cell Excitability by a Low-Threshold Calcium Spike in Turtle Olfactory Bulb J Neurophysiol, November 1, 2003; 90(5): 3341 - 3351. [Abstract] [Full Text] [PDF]

				V. Egger, K. Svoboda, and Z. F. Mainen Mechanisms of Lateral Inhibition in the Olfactory Bulb: Efficiency and Modulation of Spike-Evoked Calcium Influx into Granule Cells J. Neurosci., August 20, 2003; 23(20): 7551 - 7558. [Abstract] [Full Text] [PDF]

				J. Cang and J. S. Isaacson In Vivo Whole-Cell Recording of Odor-Evoked Synaptic Transmission in the Rat Olfactory Bulb J. Neurosci., May 15, 2003; 23(10): 4108 - 4116. [Abstract] [Full Text] [PDF]

				T. K. Alkasab, J. White, and J. S. Kauer A Computational System for Simulating and Analyzing Arrays of Biological and Artificial Chemical Sensors Chem Senses, March 1, 2002; 27(3): 261 - 275. [Abstract] [Full Text] [PDF]

				A. R. McQuiston and L. C. Katz Electrophysiology of Interneurons in the Glomerular Layer of the Rat Olfactory Bulb J Neurophysiol, October 1, 2001; 86(4): 1899 - 1907. [Abstract] [Full Text] [PDF]

				V. Aroniadou-Anderjaska, M. Ennis, and M. T. Shipley Current-Source Density Analysis in the Rat Olfactory Bulb: Laminar Distribution of Kainate/AMPA- and NMDA-Receptor-Mediated Currents J Neurophysiol, January 1, 1999; 81(1): 15 - 28. [Abstract] [Full Text] [PDF]

				N. E. Schoppa, J. M. Kinzie, Y. Sahara, T. P. Segerson, and G. L. Westbrook Dendrodendritic Inhibition in the Olfactory Bulb Is Driven by NMDA Receptors J. Neurosci., September 1, 1998; 18(17): 6790 - 6802. [Abstract] [Full Text] [PDF]

				A. Keller, S. Yagodin, V. Aroniadou-Anderjaska, L. A. Zimmer, M. Ennis, N. F. Sheppard Jr, and M. T. Shipley Functional Organization of Rat Olfactory Bulb Glomeruli Revealed by Optical Imaging J. Neurosci., April 1, 1998; 18(7): 2602 - 2612. [Abstract] [Full Text] [PDF]