Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit

Microcircuits composed of principal neuron and interneuron dendrites have an important role in shaping the representation of sensory information in the olfactory bulb. Here we establish the physiological features governing synaptic signaling in dendrodendritic microcircuits of olfactory bulb glomeruli. We show that dendritic γ-aminobutyric acid (GABA) release from periglomerular neurons mediates inhibition of principal tufted cells, retrograde inhibition of sensory input and lateral signaling onto neighboring periglomerular cells. We find that L-type dendritic Ca2+ spikes in periglomerular cells underlie dendrodendritic transmission by depolarizing periglomerular dendrites and activating P/Q type channels that trigger GABA release. Ca2+ spikes in periglomerular cells are evoked by powerful excitatory inputs from a single principal cell, and glutamate release from the dendrites of single principal neurons activates a large ensemble of periglomerular cells.

[1]  D. Friedman,et al.  Functional role of NMDA autoreceptors in olfactory mitral cells. , 2000, Journal of neurophysiology.

[2]  T. Kosaka,et al.  How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells , 1998, Neuroscience Research.

[3]  M. T. Shipley,et al.  Centre–surround inhibition among olfactory bulb glomeruli , 2003, Nature.

[4]  F. Macrides,et al.  Olfactory Bulb Units: Activity Correlated with Inhalation Cycles and Odor Quality , 1972, Science.

[5]  J. Isaacson,et al.  Olfactory Reciprocal Synapses: Dendritic Signaling in the CNS , 1998, Neuron.

[6]  Robert A. Pearce,et al.  Physiological evidence for two distinct GABAA responses in rat hippocampus , 1993, Neuron.

[7]  G. Shepherd,et al.  Analysis of Relations between NMDA Receptors and GABA Release at Olfactory Bulb Reciprocal Synapses , 2000, Neuron.

[8]  L. C. Katz,et al.  Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. , 2001, Journal of neurophysiology.

[9]  M. Häusser,et al.  Estimating the Time Course of the Excitatory Synaptic Conductance in Neocortical Pyramidal Cells Using a Novel Voltage Jump Method , 1997, The Journal of Neuroscience.

[10]  A. Grinvald,et al.  Spatio-Temporal Dynamics of Odor Representations in the Mammalian Olfactory Bulb , 2002, Neuron.

[11]  D. Jacobowitz,et al.  Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb , 1995, Neuroscience Research.

[12]  M. Puopolo,et al.  Functional heterogeneity of periglomerular cells in the rat olfactory bulb , 1998, The European journal of neuroscience.

[13]  E. White,et al.  Synaptic organization in the olfactory glomerulus of the mouse. , 1972, Brain research.

[14]  P A Salin,et al.  Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. , 2001, Journal of neurophysiology.

[15]  M. T. Shipley,et al.  Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. , 2000, Journal of neurophysiology.

[16]  Clay Armstrong,et al.  Synaptically triggered action potentials in dendrites , 1993, Neuron.

[17]  J. Isaacson.  Glutamate Spillover Mediates Excitatory Transmission in the Rat Olfactory Bulb , 1999, Neuron.

[18]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  T. Powell,et al.  The neuropil of the glomeruli of the olfactory bulb. , 1971, Journal of cell science.

[20]  Diane Lipscombe,et al.  L-type calcium channels: the low down. , 2004, Journal of neurophysiology.

[21]  T. Powell,et al.  The synaptology of the granule cells of the olfactory bulb. , 1970, Journal of cell science.

[22]  Andreas T. Schaefer,et al.  Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system , 2003, The Journal of physiology.

[23]  Paul Antoine Salin,et al.  Spontaneous GABAA receptor-mediated inhibitory currents in adult rat somatosensory cortex. , 1996, Journal of neurophysiology.

[24]  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.

[25]  G. Westbrook,et al.  Tufted cell dendrodendritic inhibition in the olfactory bulb is dependent on NMDA receptor activity. , 2001, Journal of neurophysiology.

[26]  G. Westbrook,et al.  Dendrodendritic Inhibition in the Olfactory Bulb Is Driven by NMDA Receptors , 1998, The Journal of Neuroscience.

[27]  C. Pennartz,et al.  Diurnal modulation of pacemaker potentials and calcium current in the mammalian circadian clock , 2002, Nature.

[28]  D. Johnston,et al.  Dihydropyridine-sensitive, voltage-gated Ca2+ channels contribute to the resting intracellular Ca2+ concentration of hippocampal CA1 pyramidal neurons. , 1996, Journal of neurophysiology.

[29]  P. Brennan,et al.  NEURAL MECHANISMS OF MAMMALIAN OLFACTORY LEARNING , 1997, Progress in Neurobiology.

[30]  R. Shigemoto,et al.  Cell type‐dependent expression of HCN1 in the main olfactory bulb , 2003, The European journal of neuroscience.

[31]  J. Power,et al.  Intracellular calcium store filling by an L‐type calcium current in the basolateral amygdala at subthreshold membrane potentials , 2005, The Journal of physiology.

[32]  R. Llinás,et al.  Localization of P-type calcium channels in the central nervous system. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[33]  G. Shepherd.  The Synaptic Organization of the Brain , 1979 .

[34]  D. Johnston,et al.  Multiple Channel Types Contribute to the Low-Voltage-Activated Calcium Current in Hippocampal CA3 Pyramidal Neurons , 1996, The Journal of Neuroscience.

[35]  L. Cadetti,et al.  Hyperpolarisation-activated current in glomerular cells of the rat olfactory bulb , 2001, Neuroreport.

[36]  Zev Balsen,et al.  Sensory Neuron Signaling to the Brain: Properties of Transmitter Release from Olfactory Nerve Terminals , 2004, The Journal of Neuroscience.

[37]  E. Perez-Reyes.  Molecular physiology of low-voltage-activated t-type calcium channels. , 2003, Physiological reviews.

[38]  T. Kosaka,et al.  Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb: III. Structural features of calbindin D28K‐immunoreactive neurons , 1998 .

[39]  G. Westbrook,et al.  Regulation of synaptic timing in the olfactory bulb by an A-type potassium current , 1999, Nature Neuroscience.

[40]  Nace L. Golding,et al.  Dendritic Sodium Spikes Are Variable Triggers of Axonal Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1998, Neuron.

[41]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .

[42]  M. T. Shipley,et al.  Olfactory Bulb Glomeruli: External Tufted Cells Intrinsically Burst at Theta Frequency and Are Entrained by Patterned Olfactory Input , 2004, The Journal of Neuroscience.

[43]  B. Strowbridge,et al.  Calcium Influx through NMDA Receptors Directly Evokes GABA Release in Olfactory Bulb Granule Cells , 2000, The Journal of Neuroscience.

[44]  K. Andreas,et al.  Different potencies of dihydropyridine derivatives in blocking T-type but not L-type Ca2+ channels in neuroblastoma-glioma hybrid cells. , 1998, European journal of pharmacology.

[45]  C. Jahr,et al.  Self-inhibition of olfactory bulb neurons , 2002, Nature Neuroscience.

[46]  Jianhua Cang,et al.  In Vivo Whole-Cell Recording of Odor-Evoked Synaptic Transmission in the Rat Olfactory Bulb , 2003, The Journal of Neuroscience.

[47]  Neil Madden,et al.  Low down , 1999, Nature.

[48]  K. Svoboda,et al.  Mechanisms of Lateral Inhibition in the Olfactory Bulb: Efficiency and Modulation of Spike-Evoked Calcium Influx into Granule Cells , 2003, The Journal of Neuroscience.

[49]  Weifeng Xu,et al.  Neuronal CaV1.3α1 L-Type Channels Activate at Relatively Hyperpolarized Membrane Potentials and Are Incompletely Inhibited by Dihydropyridines , 2001, The Journal of Neuroscience.

[50]  P Schwindt,et al.  Equivalence of amplified current flowing from dendrite to soma measured by alteration of repetitive firing and by voltage clamp in layer 5 pyramidal neurons. , 1996, Journal of neurophysiology.

[51]  G. Westbrook,et al.  Glomerulus-Specific Synchronization of Mitral Cells in the Olfactory Bulb , 2001, Neuron.

[52]  Jeffry S. Isaacson,et al.  Mechanisms governing dendritic γ-aminobutyric acid (GABA) release in the rat olfactory bulb , 2001 .

[53]  E. White,et al.  Synaptic organization of the mammalian olfactory glomerulus: new findings including an intraspecific variation. , 1973, Brain research.