Olfactory maps in the brain.

The responses of neural elements in many sensory areas of the brain vary systematically with their physical position, leading to a topographic representation of the outside world. Sensory representation in the olfactory system has been harder to decipher, in part because it is difficult to find appropriate metrics to characterize odor space and to sample this space densely. Recent experiments have shown that the arrangement of glomeruli, the elementary units of processing, is relatively invariant across individuals in a species, yet it is flexible enough to accommodate new sensors that might be added. Evidence supports the existence of coarse spatial domains carved out on a genetic or functional basis, but a systematic organization of odor responses or neural circuits on a local scale is not evident. Experiments and theory that relate the properties of odorant receptors to the detailed wiring diagram of the downstream olfactory circuits and to behaviors they trigger may reveal the design principles that have emerged during evolution.

[1]  Lawrence C Katz,et al.  Functional Topography of Connections Linking Mirror-Symmetric Maps in the Mouse Olfactory Bulb , 2003, Neuron.

[2]  E Kiyokage,et al.  Two GABAergic intraglomerular circuits differentially regulate tonic and phasic presynaptic inhibition of olfactory nerve terminals. , 2009, Journal of neurophysiology.

[3]  Michael T Shipley,et al.  Olfactory Bulb External Tufted Cells Are Synchronized by Multiple Intraglomerular Mechanisms , 2005, The Journal of Neuroscience.

[4]  S. Itohara,et al.  Innate versus learned odour processing in the mouse olfactory bulb , 2007, Nature.

[5]  U. Kaupp Olfactory signalling in vertebrates and insects: differences and commonalities , 2010, Nature Reviews Neuroscience.

[6]  Antoniu L. Fantana,et al.  Rat Olfactory Bulb Mitral Cells Receive Sparse Glomerular Inputs , 2008, Neuron.

[7]  Nicolas Y. Masse,et al.  Olfactory Information Processing in Drosophila , 2009, Current Biology.

[8]  Thomas A. Cleland,et al.  The anatomical logic of smell , 2005, Trends in Neurosciences.

[9]  Upinder S Bhalla,et al.  Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse , 2010, Nature Neuroscience.

[10]  Serge Charpak,et al.  External Tufted Cells Drive the Output of Olfactory Bulb Glomeruli , 2009, The Journal of Neuroscience.

[11]  Masatoshi Nei,et al.  Comparative evolutionary analysis of olfactory receptor gene clusters between humans and mice. , 2005, Gene.

[12]  Jon H Kaas,et al.  Topographic Maps are Fundamental to Sensory Processing , 1997, Brain Research Bulletin.

[13]  Gordon M Shepherd,et al.  Viral tracing identifies distributed columnar organization in the olfactory bulb , 2006, Proceedings of the National Academy of Sciences.

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

[15]  Peter C. Brunjes,et al.  A field guide to the anterior olfactory nucleus (cortex) , 2005, Brain Research Reviews.

[16]  G. Ohloff,et al.  Structure-Odor Relationships , 1994 .

[17]  E. Salinas How Behavioral Constraints May Determine Optimal Sensory Representations , 2006, PLoS biology.

[18]  I. Rodriguez,et al.  Adenylyl cyclase-dependent axonal targeting in the olfactory system , 2007, Development.

[19]  Donald A Wilson,et al.  Spatial and Temporal Distribution of Odorant-Evoked Activity in the Piriform Cortex , 2007, The Journal of Neuroscience.

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

[21]  Yoshihiro Yoshihara,et al.  Mutually Exclusive Glomerular Innervation by Two Distinct Types of Olfactory Sensory Neurons Revealed in Transgenic Zebrafish , 2005, The Journal of Neuroscience.

[22]  Barry J. Dickson,et al.  Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System , 2005, Current Biology.

[23]  Hermann Riecke,et al.  Mechanisms of pattern decorrelation by recurrent neuronal circuits , 2010, Nature Neuroscience.

[24]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[25]  S. Waddell,et al.  Drosophila olfactory memory: single genes to complex neural circuits , 2007, Nature Reviews Neuroscience.

[26]  Karen J. Rossiter,et al.  Structure−Odor Relationships , 1996 .

[27]  Hitoshi Sakano,et al.  Neural map formation in the mouse olfactory system , 2014, Cellular and Molecular Life Sciences.

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

[29]  Peter Mombaerts,et al.  Targeting olfaction , 1996, Current Opinion in Neurobiology.

[30]  Matt Wachowiak,et al.  Odorant Representations Are Modulated by Intra- but Not Interglomerular Presynaptic Inhibition of Olfactory Sensory Neurons , 2005, Neuron.

[31]  Y. Yoshihara,et al.  Hierarchical Regulation of Odorant Receptor Gene Choice and Subsequent Axonal Projection of Olfactory Sensory Neurons in Zebrafish , 2007, The Journal of Neuroscience.

[32]  M. T. Shipley,et al.  Inhibition [corrected] of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. , 2005, Journal of neurophysiology.

[33]  Sebastian T. Bundschuh,et al.  Transformation of odor representations in target areas of the olfactory bulb , 2009, Nature Neuroscience.

[34]  H. Breer,et al.  Two classes of olfactory receptors in xenopus laevis , 1995, Neuron.

[35]  Michael T Shipley,et al.  Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. , 2006, Seminars in cell & developmental biology.

[36]  Fred Rieke,et al.  Review the Challenges Natural Images Pose for Visual Adaptation , 2022 .

[37]  R. Araneda,et al.  The molecular receptive range of an odorant receptor , 2000, Nature Neuroscience.

[38]  John R Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Antenna , 2004, Cell.

[39]  L. Haberly,et al.  Odor‐evoked activity is spatially distributed in piriform cortex , 2003, The Journal of comparative neurology.

[40]  C. Lois,et al.  Watching synaptogenesis in the adult brain. , 2010, Annual review of neuroscience.

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

[42]  Vikrant Kapoor,et al.  Activity-dependent gating of lateral inhibition in the mouse olfactory bulb , 2008, Nature Neuroscience.

[43]  Masatoshi Nei,et al.  Evolutionary dynamics of olfactory receptor genes in fishes and tetrapods , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Jennifer D. Whitesell,et al.  From the top down: flexible reading of a fragmented odor map , 2009, Trends in Neurosciences.

[45]  J. Caprio,et al.  Electrophysiological evidence for a chemotopy of biologically relevant odors in the olfactory bulb of the channel catfish. , 2001, Journal of neurophysiology.

[46]  John G. Flanagan,et al.  Development of Continuous and Discrete Neural Maps , 2007, Neuron.

[47]  C. A. Byrd,et al.  Mitral cells in the olfactory bulb of adult zebrafish (Danio rerio): Morphology and distribution , 2006, The Journal of comparative neurology.

[48]  Hitoshi Sakano,et al.  One neuron-one receptor rule in the mouse olfactory system. , 2004, Trends in genetics : TIG.

[49]  W. Cain,et al.  Quantification of odor quality. , 2000, Chemical senses.

[50]  Brett A. Johnson,et al.  Relational representation in the olfactory system , 2007, Proceedings of the National Academy of Sciences.

[51]  H. Baier,et al.  Connectional topography in the zebrafish olfactory system: random positions but regular spacing of sensory neurons projecting to an individual glomerulus. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Minmin Luo,et al.  Precise Circuitry Links Bilaterally Symmetric Olfactory Maps , 2008, Neuron.

[53]  Matthew S. Grubb,et al.  Adult neurogenesis and functional plasticity in neuronal circuits , 2006, Nature Reviews Neuroscience.

[54]  P. Mombaerts,et al.  A Contextual Model for Axonal Sorting into Glomeruli in the Mouse Olfactory System , 2004, Cell.

[55]  Benjamin R. Arenkiel,et al.  In Vivo Light-Induced Activation of Neural Circuitry in Transgenic Mice Expressing Channelrhodopsin-2 , 2007, Neuron.

[56]  Kei M. Igarashi,et al.  Maps of odorant molecular features in the Mammalian olfactory bulb. , 2006, Physiological reviews.

[57]  John R. Carlson,et al.  A Novel Family of Divergent Seven-Transmembrane Proteins Candidate Odorant Receptors in Drosophila , 1999, Neuron.

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

[59]  J. Isaacson,et al.  Odor Representations in Olfactory Cortex: “Sparse” Coding, Global Inhibition, and Oscillations , 2009, Neuron.

[60]  Akihiro Urasaki,et al.  Olfactory neural circuitry for attraction to amino acids revealed by transposon-mediated gene trap approach in zebrafish , 2009, Proceedings of the National Academy of Sciences.

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

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

[63]  J. Mainland,et al.  Odor Coding by a Mammalian Receptor Repertoire , 2009, Science Signaling.

[64]  Dan D. Stettler,et al.  Representations of Odor in the Piriform Cortex , 2009, Neuron.

[65]  Naoshige Uchida,et al.  Robust Odor Coding via Inhalation-Coupled Transient Activity in the Mammalian Olfactory Bulb , 2010, Neuron.

[66]  T. Imai,et al.  Olfactory sensory neurons expressing class I odorant receptors converge their axons on an antero‐dorsal domain of the olfactory bulb in the mouse , 2006, The European journal of neuroscience.

[67]  Markus Meister,et al.  Precision and diversity in an odor map on the olfactory bulb , 2009, Nature Neuroscience.

[68]  S. Firestein,et al.  The olfactory receptor gene superfamily of the mouse , 2002, Nature Neuroscience.

[69]  Donald A. Wilson,et al.  Smelling Sounds: Olfactory–Auditory Sensory Convergence in the Olfactory Tubercle , 2010, The Journal of Neuroscience.

[70]  S. Firestein,et al.  Absence of Adenylyl Cyclase 3 Perturbs Peripheral Olfactory Projections in Mice , 2007, The Journal of Neuroscience.

[71]  Andrey Rzhetsky,et al.  A Spatial Map of Olfactory Receptor Expression in the Drosophila Antenna , 1999, Cell.

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

[73]  Adam C. Puche,et al.  Inhibition of Olfactory Receptor Neuron Input to Olfactory Bulb Glomeruli Mediated by Suppression of Presynaptic Calcium Influx , 2005 .

[74]  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.

[75]  T. Finger,et al.  Beyond the olfactory bulb: an odotopic map in the forebrain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[76]  T. Hara Olfaction and gustation in fish: an overview. , 1994, Acta physiologica Scandinavica.

[77]  S. A. Talbot,et al.  Physiological Studies on Neural Mechanisms of Visual Localization and Discrimination , 1941 .

[78]  Shawn R. Olsen,et al.  Divisive Normalization in Olfactory Population Codes , 2010, Neuron.

[79]  L. Cohen,et al.  Interglomerular center-surround inhibition shapes odorant-evoked input to the mouse olfactory bulb in vivo. , 2006, Journal of neurophysiology.

[80]  Veronica Egger,et al.  Dynamic connectivity in the mitral cell-granule cell microcircuit. , 2006, Seminars in cell & developmental biology.

[81]  S. Higashijima,et al.  From the Olfactory Bulb to Higher Brain Centers: Genetic Visualization of Secondary Olfactory Pathways in Zebrafish , 2009, The Journal of Neuroscience.

[82]  N. Buonviso,et al.  Piriform cortex functional heterogeneity revealed by cellular responses to odours , 2003, The European journal of neuroscience.

[83]  Hitoshi Sakano,et al.  Continuous and Overlapping Expression Domains of Odorant Receptor Genes in the Olfactory Epithelium Determine the Dorsal/Ventral Positioning of Glomeruli in the Olfactory Bulb , 2005, The Journal of Neuroscience.

[84]  Gordon M Shepherd,et al.  High-throughput microarray detection of olfactory receptor gene expression in the mouse. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[85]  Wei R. Chen,et al.  Differential Axonal Projection of Mitral and Tufted Cells in the Mouse Main Olfactory System , 2010, Front. Neural Circuits.

[86]  Minmin Luo,et al.  Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice , 2010, The Journal of Neuroscience.

[87]  R. Axel,et al.  A novel multigene family may encode odorant receptors: A molecular basis for odor recognition , 1991, Cell.

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

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

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

[91]  Michael Leon,et al.  Chemotopic odorant coding in a mammalian olfactory system , 2007, The Journal of comparative neurology.

[92]  Hitoshi Sakano,et al.  Odorant Receptor–Derived cAMP Signals Direct Axonal Targeting , 2006, Science.

[93]  G. Mitchison Neuronal branching patterns and the economy of cortical wiring , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[94]  D. C. Essen,et al.  Visual cortex: cartography, connectivity, and concurrent processing , 1992, Current Biology.

[95]  L. Haberly,et al.  Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. , 2001, Chemical senses.

[96]  D. Wilson Binaral interactions in the rat piriform cortex. , 1997, Journal of neurophysiology.

[97]  David Harel,et al.  A metric for odorant comparison , 2008, Nature Methods.

[98]  Jie Tan,et al.  Odor Information Processing by the Olfactory Bulb Analyzed in Gene-Targeted Mice , 2010, Neuron.

[99]  John R. Carlson,et al.  Coding of Odors by a Receptor Repertoire , 2006, Cell.

[100]  Heinz Wässle,et al.  Parallel processing in the mammalian retina , 2004, Nature Reviews Neuroscience.

[101]  Hitoshi Sakano,et al.  Spatial arrangement of glomerular molecular-feature clusters in the odorant-receptor class domains of the mouse olfactory bulb. , 2010, Journal of neurophysiology.

[102]  Lawrence C. Katz,et al.  Odorant receptors instruct functional circuitry in the mouse olfactory bulb , 2002, Nature.

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

[104]  Y. Yoshihara,et al.  Odorant Receptor Map in the Mouse Olfactory Bulb: In Vivo Sensitivity and Specificity of Receptor-Defined Glomeruli , 2006, Neuron.

[105]  J. Amoore,et al.  EVIDENCE FOR THE CHEMICAL OLFACTORY CODE IN MAN , 1974, Annals of the New York Academy of Sciences.

[106]  Leonardo Belluscio,et al.  Activity-Dependent Plasticity in the Olfactory Intrabulbar Map , 2006, The Journal of Neuroscience.

[107]  E I Knudsen,et al.  Computational maps in the brain. , 1987, Annual review of neuroscience.

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

[109]  J. Isaacson,et al.  Odor representations in mammalian cortical circuits , 2010, Current Opinion in Neurobiology.

[110]  S. Schiffman Physicochemical correlates of olfactory quality. , 1974, Science.

[111]  Peter Mombaerts,et al.  Mapping of Class I and Class II Odorant Receptors to Glomerular Domains by Two Distinct Types of Olfactory Sensory Neurons in the Mouse , 2009, Neuron.

[112]  H. Sakano,et al.  Sequential Arrival and Graded Secretion of Sema3F by Olfactory Neuron Axons Specify Map Topography at the Bulb , 2010, Cell.

[113]  David H Gire,et al.  Control of On/Off Glomerular Signaling by a Local GABAergic Microcircuit in the Olfactory Bulb , 2009, The Journal of Neuroscience.

[114]  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.

[115]  C. Poo,et al.  Odor representations in olfactory cortex , 2010 .

[116]  Kei Ito,et al.  Integration of Chemosensory Pathways in the Drosophila Second-Order Olfactory Centers , 2004, Current Biology.

[117]  G. Laurent,et al.  Odor encoding as an active, dynamical process: experiments, computation, and theory. , 2001, Annual review of neuroscience.

[118]  T. Hummel,et al.  Olfactory map formation in the Drosophila brain: genetic specificity and neuronal variability , 2011, Current Opinion in Neurobiology.

[119]  Thomas A. Cleland,et al.  Early transformations in odor representation , 2010, Trends in Neurosciences.

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

[121]  Rainer W. Friedrich,et al.  Olfactory pattern classification by discrete neuronal network states , 2010, Nature.

[122]  L. Astic,et al.  Anatomical mapping of the neuroepithelial projection to the olfactory bulb in the rat , 1986, Brain Research Bulletin.

[123]  Peter Mombaerts,et al.  Odorant receptor gene choice in olfactory sensory neurons: the one receptor–one neuron hypothesis revisited , 2004, Current Opinion in Neurobiology.

[124]  Matt Wachowiak,et al.  In Vivo Imaging of Neuronal Activity by Targeted Expression of a Genetically Encoded Probe in the Mouse , 2004, Neuron.

[125]  P. Mombaerts,et al.  Development and topography of the lateral olfactory tract in the mouse: imaging by genetically encoded and injected fluorescent markers. , 2006, Journal of neurobiology.

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

[127]  R. Khan,et al.  Predicting Odor Pleasantness from Odorant Structure: Pleasantness as a Reflection of the Physical World , 2007, The Journal of Neuroscience.

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

[129]  John R. Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Larva , 2005, Neuron.

[130]  Yuchio Yanagawa,et al.  Molecular Identity of Periglomerular and Short Axon Cells , 2010, The Journal of Neuroscience.

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

[132]  Hokto Kazama,et al.  Homeostatic Matching and Nonlinear Amplification at Identified Central Synapses , 2008, Neuron.

[133]  Hitoshi Sakano,et al.  Topographic mapping--the olfactory system. , 2010, Cold Spring Harbor perspectives in biology.

[134]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[135]  Rainer W Friedrich,et al.  Topological Reorganization of Odor Representations in the Olfactory Bulb , 2007, PLoS biology.

[136]  Richard Axel,et al.  Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum , 2002, Cell.

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

[138]  K. Abe,et al.  Gustation in fish: search for prototype of taste perception. , 2009, Results and problems in cell differentiation.

[139]  J. Carlson,et al.  Olfactory Perception: Receptors, Cells, and Circuits , 2009, Cell.

[140]  Keita Endo,et al.  Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages , 2007, Nature Neuroscience.

[141]  H. Ojima,et al.  The trajectory of mitral cell axons in the rabbit olfactory cortex revealed by intracellular HRP injection , 1984, The Journal of comparative neurology.

[142]  Peter Mombaerts,et al.  Axonal wiring in the mouse olfactory system. , 2006, Annual review of cell and developmental biology.

[143]  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.

[144]  Teuvo Kohonen,et al.  Where the abstract feature maps of the brain might come from , 1999, Trends in Neurosciences.

[145]  S. Firestein,et al.  How the olfactory bulb got its glomeruli: a just so story? , 2009, Nature Reviews Neuroscience.

[146]  D. Chklovskii,et al.  Maps in the brain: what can we learn from them? , 2004, Annual review of neuroscience.

[147]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[148]  W. Gao,et al.  Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears , 2000, Nature Neuroscience.

[149]  Y. Yoshihara,et al.  Molecular genetic dissection of the zebrafish olfactory system. , 2009, Results and problems in cell differentiation.

[150]  Nathalie Buonviso,et al.  Mitral cell‐to‐glomerulus connectivity: An HRP study of the orientation of mitral cell apical dendrites , 1991, The Journal of comparative neurology.