Tuning and Topography in an Odor Map on the Rat Olfactory Bulb

The sense of smell originates in a diverse array of receptor neurons, comprising up to 1000 different types. To understand how these parallel channels encode chemical stimuli, we recorded the responses of glomeruli in the olfactory bulbs of the anesthetized rat, by optical imaging of intrinsic signals. Odor stimulation produced two kinds of optical responses at the surface of the bulb: a broad diffuse component superposed by discrete small spots. Histology showed that the spots correspond to individual glomeruli, and that ∼400 of them can be monitored in this way. Based on its wavelength-dependence, this optical signal appears to derive from changes in light scattering during neural activity. Pure odorants generally activated several glomeruli in a bilaterally symmetric pattern, whose extent varied greatly with concentration. A simple formalism for ligand binding accounts quantitatively for this concentration dependence and yields the effective affinity with which a glomerulus responds to an odorant. When tested with aliphatic molecules of increasing carbon chain length, many glomeruli were sharply tuned for one or two adjacent chain lengths. Glomeruli with similar tuning properties were located near each other, producing a systematic map of molecular chain length on the surface of the olfactory bulb. Given local inhibitory circuits within the olfactory bulb, this can account for the observed functional inhibition between related odors. We explore several parallels to the function and architecture of the visual system that help interpret the neural representation of odors.

[1]  P Duchamp-Viret,et al.  Amplifying role of convergence in olfactory system a comparative study of receptor cell and second-order neuron sensitivities. , 1989, Journal of neurophysiology.

[2]  T. Sendera,et al.  Morphometry of rat olfactory bulbs stained for cytochrome oxidase reveals that the entire population of glomeruli forms early in the neonatal period. , 1993, Brain research. Developmental brain research.

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

[4]  A. Holley,et al.  Receptor cell responses to odorants: Similarities and differences among odorants , 1984, Brain Research.

[5]  J. V. van Hateren,et al.  Spatiotemporal contrast sensitivity of early vision , 1993, Vision Research.

[6]  Gilles Sicard,et al.  New studies on odour discrimination in the frog's olfactory receptor cells. I. Experimental results , 1982 .

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

[8]  K. Mori,et al.  Computation of molecular information in mammalian olfactory systems. , 1998, Network.

[9]  A. Hodgkin,et al.  Detection and resolution of visual stimuli by turtle photoreceptors , 1973, The Journal of physiology.

[10]  L. Buck,et al.  Information coding in the vertebrate olfactory system. , 1996, Annual review of neuroscience.

[11]  J. Y. Lettvin,et al.  ODOR SPECIFICITIES OF THE FROG'S OLFACTORY RECEPTORS, , 1963 .

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

[13]  P. Mombaerts,et al.  Molecular biology of odorant receptors in vertebrates. , 1999, Annual review of neuroscience.

[14]  Ying Zheng,et al.  Spectroscopic Analysis of Changes in Remitted Illumination: The Response to Increased Neural Activity in Brain , 1999, NeuroImage.

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

[16]  G. Laurent A systems perspective on early olfactory coding. , 1999, Science.

[17]  G. Shepherd,et al.  Odor maps in the olfactory bulb , 2000, The Journal of comparative neurology.

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

[19]  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.

[20]  J. Mayhew,et al.  Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity , 1996, NeuroImage.

[21]  D. F. Mathews,et al.  Response patterns of single units in the olfactory bulb of the rat to odor. , 1972, Brain research.

[22]  Setsuo Takatani,et al.  Theoretical Analysis of Diffuse Reflectance from a Two-Layer Tissue Model , 1979, IEEE Transactions on Biomedical Engineering.

[23]  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.

[24]  C. Gall,et al.  Functional mapping of odor-activated neurons in the olfactory bulb. , 1995, Chemical senses.

[25]  J S Kauer,et al.  Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. , 1995, Journal of neurophysiology.

[26]  Joseph J. Atick,et al.  What Does the Retina Know about Natural Scenes? , 1992, Neural Computation.

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

[28]  K. Naka,et al.  S‐potentials from colour units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[29]  A. Menini,et al.  The relation between stimulus and response in olfactory receptor cells of the tiger salamander. , 1993, The Journal of physiology.

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

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

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

[33]  Yoshihiro Yoshihara,et al.  Molecular recognition and olfactory processing in the mammalian olfactory system , 1995, Progress in Neurobiology.

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

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

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

[37]  A. Grinvald,et al.  Spatial Relationships among Three Columnar Systems in Cat Area 17 , 1997, The Journal of Neuroscience.

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

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

[40]  A. Grinvald,et al.  Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. , 1999, Science.

[41]  J. C. Walker,et al.  Odor psychophysics in vertebrates , 1985, Neuroscience & Biobehavioral Reviews.

[42]  M. Wong-Riley Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry , 1979, Brain Research.

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

[44]  R. Axel,et al.  The molecular biology of olfactory perception. , 1996, Cold Spring Harbor symposia on quantitative biology.

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

[46]  A. Duchamp,et al.  ODOR DISCRIMINATION BY FROG OLFACTORY RECEPTORS , 1974 .

[47]  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.

[48]  A. Duchamp,et al.  Odour discrimination by frog olfactory receptors: a second study , 1978 .

[49]  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.