Symmetry, Stereotypy, and Topography of Odorant Representations in Mouse Olfactory Bulbs

The molecular basis of vertebrate odorant representations has been derived extensively from mice. The functional correlates of these molecular features were visualized using optical imaging of intrinsic signals in mouse olfactory bulbs. Single odorants activated clusters of glomeruli in consistent, restricted portions of the bulb. Patterns of activated glomeruli were clearly bilaterally symmetric and consistent in different individual mice, but the precise number, position, and intensity of activated glomeruli in the two bulbs of the same individual and between individuals varied considerably. Representations of aliphatic aldehydes of different carbon chain length shifted systematically along a rostral–caudal strip of the dorsal bulb, indicating a functional topography of odorant representations. Binary mixtures of individual aldehydes elicited patterns of glomerular activation that were topographic combinations of the maps for each individual odor. Thus the principles derived from the molecular organization of a small subset of murine olfactory receptor neuron projection patterns—bilateral symmetry, local clustering, and local variability—are reliable guides to the initial functional representation of odorant molecules.

[1]  John S. Kauer,et al.  Local sites of activity-related glucose metabolism in rat olfactory bulb during olfactory stimulation , 1975, Brain Research.

[2]  F R Sharp,et al.  Laminar analysis of 2-deoxyglucose uptake in olfactory bulb and olfactory cortex of rabbit and rat. , 1977, Journal of neurophysiology.

[3]  L. C. Skeen Odor-induced patterns of deoxyglucose consumption in the olfactory bulb of the tree shrew,Tupaia glis , 1977, Brain Research.

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

[5]  R. Rescorla Simultaneous and successive associations in sensory preconditioning. , 1980, Journal of experimental psychology. Animal behavior processes.

[6]  D. Purves,et al.  Elimination of synapses in the developing nervous system. , 1980, Science.

[7]  L. Astic,et al.  Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours , 1980, Brain Research.

[8]  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.

[9]  R. Porter,et al.  Development of olfactory bulb organization in precocial and altricial rodents. , 1984, Brain research.

[10]  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.

[11]  J. Royet,et al.  Morphometric study of the glomerular population in the mouse olfactory bulb: Numerical density and size distribution along the rostrocaudal axis , 1988, The Journal of comparative neurology.

[12]  B. Slotnick,et al.  Odor masking in the rat , 1989, Physiology & Behavior.

[13]  Responses of olfactory receptor cells of spiny lobsters to binary mixtures. I. Intensity mixture interactions. , 1991, Journal of neurophysiology.

[14]  Responses of olfactory receptor cells of spiny lobsters to binary mixtures. II. Pattern mixture interactions. , 1991, Journal of neurophysiology.

[15]  A. Hatanaka,et al.  Odor-Structure Relationships in n-Hexenols and n-Hexenais , 1992, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[16]  K. Imamura,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. , 1992, Journal of neurophysiology.

[17]  D. Purves,et al.  Vital imaging of glomeruli in the mouse olfactory bulb , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  N. Onoda Odor-induced fos-like immunoreactivity in the rat olfactory bulb , 1992, Neuroscience Letters.

[19]  C. Wysocki,et al.  Induction of olfactory receptor sensitivity in mice. , 1993, Science.

[20]  F Jourdan,et al.  C-fos expression and 2-deoxyglucose uptake in the olfactory bulb of odour-stimulated awake rats. , 1993, Neuroreport.

[21]  C. Gall,et al.  Odor-induced increases in c-fos mRNA expression reveal an anatomical "unit" for odor processing in olfactory bulb. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[22]  K. Mori,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. , 1992, Journal of neurophysiology.

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

[24]  H. Baier,et al.  Olfactory glomeruli in the zebrafish form an invariant pattern and are identifiable across animals , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[26]  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.

[27]  Peter C. Brunjes,et al.  Unilateral naris closure and olfactory system development , 1994, Brain Research Reviews.

[28]  M. Tonoike,et al.  Tuning specificities to aliphatic odorants in mouse olfactory receptor neurons and their local distribution. , 1994, Journal of neurophysiology.

[29]  R. Reed,et al.  The genetic basis for specific anosmia to isovaleric acid in the mouse , 1995, Cell.

[30]  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.

[31]  K. Mori,et al.  Relation of chemical structure to specificity of response in olfactory glomeruli , 1995, Current Opinion in Neurobiology.

[32]  W. Getz,et al.  Partitioning non-linearities in the response of honey bee olfactory receptor neurons to binary odors. , 1995, Bio Systems.

[33]  J S Kauer,et al.  Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. I. Characterization of the recording system. , 1995, Journal of neurophysiology.

[34]  D. G. Laing,et al.  Influence of training and experience on the perception of multicomponent odor mixtures. , 1996, Journal of experimental psychology. Human perception and performance.

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

[36]  C. Derby,et al.  Generalization among related complex odorant mixtures and their components: Analysis of olfactory perception in the spiny lobster , 1996, Physiology & Behavior.

[37]  K. Mori,et al.  Basic principles and molecular mechanisms of olfactory axon pathfinding , 1997, Cell and Tissue Research.

[38]  B. Smith,et al.  A computational model of the response of honey bee antennal lobe circuitry to odor mixtures: overshadowing, blocking and unblocking can arise from lateral inhibition , 1997, Behavioural Brain Research.

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

[40]  R. Menzel,et al.  Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. , 1997, The Journal of experimental biology.

[41]  R. Menzel,et al.  Representations of odours and odour mixtures visualized in the honeybee brain , 1997, Nature.

[42]  J. Kauer,et al.  Odorant Response Properties of Convergent Olfactory Receptor Neurons , 1998, The Journal of Neuroscience.

[43]  R. Axel,et al.  Odorant Receptors Govern the Formation of a Precise Topographic Map , 1998, Cell.

[44]  R G Shulman,et al.  Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[45]  D. G. Laing,et al.  The influence of odor type on the discrimination and identification of odorants in multicomponent odor mixtures , 1998, Physiology & Behavior.

[46]  M. Leon,et al.  Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb. , 1998, The Journal of comparative neurology.

[47]  W. Cain,et al.  Odor identification: perceptual and semantic dimensions. , 1998, Chemical senses.

[48]  N. Vickers,et al.  Combinatorial odor discrimination in the brain: Attractive and antagonist odor blends are represented in distinct combinations of uniquely identifiable glomeruli , 1998, The Journal of comparative neurology.

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

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

[51]  K. Mori,et al.  The olfactory bulb: coding and processing of odor molecule information. , 1999, Science.

[52]  M. Leon,et al.  Multidimensional chemotopic responses to n‐aliphatic acid odorants in the rat olfactory bulb , 1999, The Journal of comparative neurology.

[53]  R. Menzel,et al.  Associative learning modifies neural representations of odors in the insect brain , 1999, Nature Neuroscience.

[54]  H. Sakano,et al.  Olfactory Neurons Expressing Closely Linked and Homologous Odorant Receptor Genes Tend to Project Their Axons to Neighboring Glomeruli on the Olfactory Bulb , 1999, The Journal of Neuroscience.

[55]  A. Chess,et al.  Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe , 2000, Nature Neuroscience.

[56]  H Breer,et al.  Local Permutations in the Glomerular Array of the Mouse Olfactory Bulb , 2000, The Journal of Neuroscience.

[57]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[58]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[59]  M. Leon,et al.  Odorant molecular length: One aspect of the olfactory code , 2000, The Journal of comparative neurology.

[60]  J. Hildebrand,et al.  Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles , 2000, Nature Neuroscience.

[61]  M. Leon,et al.  Modular representations of odorants in the glomerular layer of the rat olfactory bulb and the effects of stimulus concentration , 2000, The Journal of comparative neurology.

[62]  R G Shulman,et al.  Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI. , 2000, Proceedings of the National Academy of Sciences of the United States of America.