Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb

We have investigated the membrane properties and excitatory synaptic transmission of mitral cells in a slice preparation of rat olfactory bulb. In response to intracellular injection of depolarizing current, most mitral cells showed several distinct membrane properties: (1) delayed onset of firing (suggesting the presence of a type of potassium A current); (2) subthreshold oscillation of the membrane potential; and (3) repetitive firing of clustered action potentials during prolonged threshold stimulation. Olfactory nerve (ON) stimulation evoked a long-lasting EPSP in most of the mitral cells. This long EPSP was completely blocked by combined application of NMDA and non-NMDA receptor antagonists (20 microM CNQX and 100 microM APV), confirming that glutamate is the neurotransmitter at the synapses from ON to mitral cells. The ON-evoked EPSP was preceded by a prespike, which was resistant to membrane potential hyperpolarization at the soma. This fast prepotential may be indicative of an active response in the primary dendritic tufts of the mitral cells. Stimulation of the lateral olfactory tract evoked an antidromic pulse followed by a short EPSP, which could also be elicited independently of an antidromic spike in the recorded cell. Since the asymmetrical synapses so far observed on the mitral cells are all form the ON, this antidromically evoked EPSP may reflect self-excitation of a mitral cell by glutamate released from its own dendrites by antidromic impulse invasion, or/and lateral excitation by neighboring invaded dendrites.

[1]  X. Wang,et al.  Ionic basis for intrinsic 40 Hz neuronal oscillations. , 1993, Neuroreport.

[2]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[3]  P. Schwartzkroin,et al.  Further characteristics of hippocampal CA1 cells in vitro , 1977, Brain Research.

[4]  D. Wellis,et al.  Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. , 1990, Journal of neurophysiology.

[5]  T. Powell,et al.  The termination of centrifugal fibres in the glomerular layer of the olfactory bulb. , 1972, Journal of cell science.

[6]  T. A. Harrison,et al.  Discrimination among odorants by single neurons of the rat olfactory bulb. , 1989, Journal of neurophysiology.

[7]  R. Petralia,et al.  Light and electron immunocytochemical localization of AMPA‐selective glutamate receptors in the rat brain , 1992, The Journal of comparative neurology.

[8]  S. P. Schneider,et al.  Orthodromic response properties of rat olfactory bulb mitral and tufted cells correlate with their projection patterns. , 1983, Journal of neurophysiology.

[9]  G. Shepherd,et al.  Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. , 1968, Journal of neurophysiology.

[10]  J S Kauer,et al.  GABAA and glutamate receptor involvement in dendrodendritic synaptic interactions from salamander olfactory bulb. , 1993, The Journal of physiology.

[11]  G M Shepherd,et al.  Evidence for glutamate as the olfactory receptor cell neurotransmitter. , 1994, Journal of neurophysiology.

[12]  W J Freeman,et al.  Measurement of oscillatory responses to electrical stimulation in olfactory bulb of cat. , 1972, Journal of neurophysiology.

[13]  R. Nicoll,et al.  An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb , 1982, The Journal of physiology.

[14]  G. Shepherd,et al.  GABAergic mechanisms of dendrodendritic synapses in isolated turtle olfactory bulb. , 1981, Journal of neurophysiology.

[15]  R. Nicoll,et al.  Dendrodendritic inhibition: demonstration with intracellular recording. , 1980, Science.

[16]  Michael A. Rogawski,et al.  The A-current: how ubiquitous a feature of excitable cells is it? , 1985, Trends in Neurosciences.

[17]  G. Shepherd,et al.  Synaptic excitation and long-lasting inhibition of mitral cells in the in vitro turtle olfactory bulb , 1979, Brain Research.

[18]  G M Shepherd,et al.  Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. , 1966, Experimental neurology.

[19]  G M Shepherd,et al.  Analysis of a long‐duration inhibitory potential in mitral cells in the isolated turtle olfactory bulb. , 1981, The Journal of physiology.

[20]  G. Shepherd,et al.  Analysis of synaptic potentials in mitral cells in the isolated turtle olfactory bulb. , 1981, The Journal of physiology.

[21]  G. Laurent,et al.  Encoding of Olfactory Information with Oscillating Neural Assemblies , 1994, Science.

[22]  G M Shepherd,et al.  Blockade of synaptic inhibition reveals long-lasting synaptic excitation in isolated turtle olfactory bulb. , 1981, Journal of neurophysiology.

[23]  G. Shepherd,et al.  Synaptic excitatory and inhibitory interactions at distal dendritic sites on mitral cells in the isolated turtle olfactory bulb , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  W. T. Nickell,et al.  Orthodromic synaptic activation of rat olfactory bulb mitral cells in isolated slices , 1996, Brain Research Bulletin.

[25]  K. Mori,et al.  Spike generation in the mitral cell dendrite of the rabbit olfactory bulb , 1975, Brain Research.

[26]  R. Wenthold,et al.  Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  P. Schwartzkroin,et al.  Electrophysiology of Hippocampal Neurons , 1987 .

[28]  G M Shepherd,et al.  Electrophysiological analysis of mitral cells in the isolated turtle olfactory bulb. , 1981, The Journal of physiology.

[29]  Johan F. Storm,et al.  Temporal integration by a slowly inactivating K+ current in hippocampal neurons , 1988, Nature.

[30]  R. Nicoll,et al.  Self-excitation of olfactory bulb neurones , 1982, Nature.

[31]  S. Nakanishi,et al.  Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb , 1993, Nature.

[32]  J S Kauer,et al.  GABAergic and glutamatergic synaptic input to identified granule cells in salamander olfactory bulb. , 1994, The Journal of physiology.

[33]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[34]  J. Kauer,et al.  Responses of mitral/tufted cells to orthodromic and antidromic electrical stimulation in the olfactory bulb of the tiger salamander. , 1988, Journal of neurophysiology.

[35]  A. N. van den Pol,et al.  Presynaptic metabotropic glutamate receptors in adult and developing neurons: Autoexcitation in the olfactory bulb , 1995, The Journal of comparative neurology.

[36]  Gordon M. Shepherd,et al.  Synaptic transmission and modulation in the olfactory bulb , 1993, Current Opinion in Neurobiology.

[37]  B LIBET,et al.  The behaviour of chromatolysed motoneurones studied by intracellular recording , 1958, The Journal of physiology.

[38]  T. Powell,et al.  The mitral and short axon cells of the olfactory bulb. , 1970, Journal of cell science.

[39]  E Orona,et al.  Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb , 1984, The Journal of comparative neurology.

[40]  Hideto Kaba,et al.  INDUCTION OF AN OLFACTORY MEMORY BY THE ACTIVATION OF A METABOTROPIC GLUTAMATE RECEPTOR , 1994 .

[41]  D. Tank,et al.  Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc , 1990, Nature.

[42]  R. Nicoll,et al.  Recurrent Excitation of Secondary Olfactory Neurons: A Possible Mechanism for Signal Amplification , 1971, Science.

[43]  Alan Gelperin,et al.  Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc , 1994, Nature.

[44]  G. Shepherd,et al.  Impulse activity in presynaptic dendrites: analysis of mitral cells in the isolated turtle olfactory bulb , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  D. McCormick,et al.  Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons. , 1991, Journal of neurophysiology.

[46]  S. Nakanishi,et al.  Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[47]  R. Nicoll,et al.  Inhibitory mechanisms in the rabbit olfactory bulb: dendrodendritic mechanisms. , 1969, Brain research.