Functional organization of sensory input to the olfactory bulb glomerulus analyzed by two-photon calcium imaging

Glomeruli in the olfactory bulb are anatomically discrete modules receiving input from idiotypic olfactory sensory neurons. To examine the functional organization of sensory inputs to individual glomeruli, we loaded olfactory sensory neurons with a Ca2+ indicator and measured odorant-evoked presynaptic Ca2+ signals within single glomeruli by using two-photon microscopy in anaesthetized mice. Odorants evoked patterns of discrete Ca2+ signals throughout the neuropil of a glomerulus. Across glomeruli, Ca2+ signals occurred with equal probability in all glomerular regions. Within single glomeruli, the pattern of intraglomerular Ca2+ signals was indistinguishable for stimuli of different duration, identity, and concentration. Moreover, the response time course of the signals was similar throughout the glomerulus. Hence, sensory inputs to individual glomeruli are spatially heterogeneous but seem to be functionally indiscriminate. These results support the view of olfactory glomeruli as functional units in representing sensory information.

[1]  W. L. Clark.  The Ferrier Lecture - Inquiries into the anatomical basis of olfactory discrimination , 1957, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[2]  J. Kauer,et al.  Responses of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander , 1974, The Journal of physiology.

[3]  G. Shepherd,et al.  Functional organization of rat olfactory bulb analysed by the 2‐deoxyglucose method , 1979, The Journal of comparative neurology.

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

[5]  R. Nicoll,et al.  Primary afferent depolarization in the in vitro frog olfactory bulb , 1981, The Journal of physiology.

[6]  J S Kauer,et al.  Mapping of odor-related neuronal activity in the olfactory bulb by high-resolution 2-deoxyglucose autoradiography. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[7]  P. Sheehe,et al.  "Imposed" and "inherent" mucosal activity patterns. Their composite representation of olfactory stimuli , 1987, The Journal of general physiology.

[8]  Colin J. R. Sheppard,et al.  Image formation in two-photon fluorescence microscopy , 1990 .

[9]  J. Kauer,et al.  Intracellular injection of vital dyes into single cells in the salamander olfactory epithelium , 1992, Neuroscience Letters.

[10]  J. Kauer,et al.  Are there structural and functional modules in the vertebrate olfactory bulb? , 1993, Microscopy research and technique.

[11]  C. Greer,et al.  Terminal arborizations of olfactory nerve fibers in the glomeruli of the olfactory bulb , 1993, The Journal of comparative neurology.

[12]  Linda B. Buck,et al.  A zonal organization of odorant receptor gene expression in the olfactory epithelium , 1993, Cell.

[13]  Gordon M. Shepherd,et al.  Discrimination of molecular signals by the olfactory receptor neuron , 1994, Neuron.

[14]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

[15]  P. Saggau,et al.  Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  Linda B. Buck,et al.  Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb , 1994, Cell.

[17]  J. W. Scott,et al.  Regional distribution of rat electroolfactogram. , 1995, Journal of neurophysiology.

[18]  W G Regehr,et al.  Calcium transients in cerebellar granule cell presynaptic terminals. , 1995, Biophysical journal.

[19]  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.

[20]  M Ennis,et al.  Functional organization of olfactory system. , 1996, Journal of neurobiology.

[21]  M M Mozell,et al.  The interaction of imposed and inherent olfactory mucosal activity patterns and their composite representation in a mammalian species using voltage-sensitive dyes , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  T. Kosaka,et al.  Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb: prominent differences in the intraglomerular dendritic arborization and their relationship to olfactory nerve terminals , 1996, Neuroscience.

[23]  B. Key,et al.  Olfactory glomeruli are innervated by more than one distinct subset of primary sensory olfactory neurons in mice , 1996, The Journal of comparative neurology.

[24]  Richard Axel,et al.  Visualizing an Olfactory Sensory Map , 1996, Cell.

[25]  T. I. Chao,et al.  Distribution of astroglia in glomeruli of the rat main olfactory bulb: Exclusion from the sensory subcompartment of neuropil , 1997, The Journal of comparative neurology.

[26]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[27]  R. Friedrich,et al.  Combinatorial and Chemotopic Odorant Coding in the Zebrafish Olfactory Bulb Visualized by Optical Imaging , 1997, Neuron.

[28]  Rainer W. Friedrich,et al.  Chemotopic, Combinatorial, and Noncombinatorial Odorant Representations in the Olfactory Bulb Revealed Using a Voltage-Sensitive Axon Tracer , 1998, The Journal of Neuroscience.

[29]  Thomas A. Cleland,et al.  Concentration Tuning Mediated by Spare Receptor Capacity in Olfactory Sensory Neurons: A Theoretical Study , 1999, Neural Computation.

[30]  L. Cohen,et al.  Presynaptic Inhibition of Primary Olfactory Afferents Mediated by Different Mechanisms in Lobster and Turtle , 1999, The Journal of Neuroscience.

[31]  M Ennis,et al.  Dendrodendritic recurrent excitation in mitral cells of the rat olfactory bulb. , 1999, Journal of neurophysiology.

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

[33]  P. Mombaerts.  Seven-transmembrane proteins as odorant and chemosensory receptors. , 1999, Science.

[34]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[35]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[36]  B. Key,et al.  Development of P2 Olfactory Glomeruli in P2-Internal Ribosome Entry Site-Tau-LacZ Transgenic Mice , 1999, The Journal of Neuroscience.

[37]  A. Kaneko,et al.  Adrenaline enhances odorant contrast by modulating signal encoding in olfactory receptor cells , 1999, Nature Neuroscience.

[38]  P. Duchamp-Viret,et al.  Odor response properties of rat olfactory receptor neurons. , 1999, Science.

[39]  C. Greer,et al.  Compartmental organization of the olfactory bulb glomerulus , 1999, The Journal of comparative neurology.

[40]  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.

[41]  D. Tank,et al.  Action potentials reliably invade axonal arbors of rat neocortical neurons. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. T. Shipley,et al.  Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. , 2001, Journal of neurophysiology.

[43]  M. Spehr,et al.  Phosphorylation of voltage‐gated ion channels in rat olfactory receptor neurons , 2001, The European journal of neuroscience.

[44]  A. Keller,et al.  Ephaptic Interactions in the Mammalian Olfactory System , 2001, The Journal of Neuroscience.

[45]  Steve M. Potter,et al.  Structure and Emergence of Specific Olfactory Glomeruli in the Mouse , 2001, The Journal of Neuroscience.

[46]  L. Cohen,et al.  Representation of Odorants by Receptor Neuron Input to the Mouse Olfactory Bulb , 2001, Neuron.

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

[48]  Rainer W Friedrich,et al.  Recent dynamics in olfactory population coding , 2001, Current Opinion in Neurobiology.

[49]  Bert Sakmann,et al.  Reciprocal intraglomerular excitation and intra‐ and interglomerular lateral inhibition between mouse olfactory bulb mitral cells , 2002, The Journal of physiology.

[50]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[51]  S. Korsching,et al.  Selective imaging of presynaptic activity in the mouse olfactory bulb shows concentration and structure dependence of odor responses in identified glomeruli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[52]  D. Restrepo,et al.  Expression of connexin 45 in the olfactory system , 2002, Brain Research.

[53]  G. Westbrook,et al.  AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli , 2002, Nature Neuroscience.

[54]  Peter Mombaerts,et al.  Odorant Receptor Expression Defines Functional Units in the Mouse Olfactory System , 2002, The Journal of Neuroscience.

[55]  Peter Mombaerts,et al.  Specificity of Glomerular Targeting by Olfactory Sensory Axons , 2002, The Journal of Neuroscience.

[56]  N. Schoppa,et al.  Dendritic processing within olfactory bulb circuits , 2003, Trends in Neurosciences.

[57]  H. Breer,et al.  Subzonal organization of olfactory sensory neurons projecting to distinct glomeruli within the mouse olfactory bulb , 2003, The Journal of comparative neurology.

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

[59]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.