Predicting odorant quality perceptions from multidimensional scaling of olfactory bulb glomerular activity patterns.

Odorants and their perceptions differ along multiple dimensions, requiring that a critical examination of any putative neural code directly assess the multidimensional nature of the encoding process. Previous work has examined simple, systematic odorant differences that, regardless of coding strategy, would be expected to produce simple, systematic predictions in neural and behavioral responses. In the present study, an odorant identification confusion matrix task that extracts precise quality relationships across odorants was used to determine whether spatially specific glomerular activity patterns predict perceptual quality relationships for odorants that cannot easily be classified a priori along a single chemical dimension. Multidimensional scaling (MDS) analysis of odorant pattern similarity measures derived from the comparison of [14C]-2-deoxyglucose glomerular activity pattern data yielded a two-dimensional odorant activity space that was highly significantly predictive of similarly obtained odorant perceptual spaces, uniformly across animals. These results strongly support the relevance of global spatial patterns in the olfactory bulb to the encoding of odor quality.

[1]  Donald A Wilson,et al.  Olfactory Bulb Mitral-Tufted Cell Plasticity: Odorant-Specific Tuning Reflects Previous Odorant Exposure , 2003, The Journal of Neuroscience.

[2]  Thomas A. Cleland,et al.  Behavioral models of odor similarity. , 2002, Behavioral neuroscience.

[3]  M. Chastrette,et al.  Analysis of a system of description of odors by means of four different multivariate statistical methods , 1991 .

[4]  S. Youngentob,et al.  OMP gene deletion results in an alteration in odorant quality perception. , 2001, Behavioral neuroscience.

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

[6]  P. Sheehe,et al.  Odorant confusion matrix: the influence of patient history on patterns of odorant identification and misidentification in hyposmia , 2001, Physiology & Behavior.

[7]  Fahmeed Hyder,et al.  Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Erickson,et al.  MULTIDIMENSIONAL SCALING OF ODORANTS: EXAMINATION OF PSYCHOLOGICAL AND PHYSICOCHEMICAL DIMENSIONS , 1977 .

[9]  Michael Leon,et al.  Interactions between odorant functional group and hydrocarbon structure influence activity in glomerular response modules in the rat olfactory bulb , 2005, The Journal of comparative neurology.

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

[11]  M. Leon,et al.  Differential responses to branched and unsaturated aliphatic hydrocarbons in the rat olfactory system , 2006, The Journal of comparative neurology.

[12]  W. R. Garner Applications of Information Theory to Psychology , 1959 .

[13]  B. Slotnick,et al.  Zonal ablation of the olfactory sensory neuroepithelium of the mouse: effects on odorant detection , 2004, European Journal of Neuroscience.

[14]  E. Adrian Olfactory reactions in the brain of the hedgehog , 1942, The Journal of physiology.

[15]  R. Sullivan,et al.  Early olfactory learning induces an enhanced olfactory bulb response in young rats. , 1986, Brain research.

[16]  R. Doty,et al.  Tests of human olfactory function: Principal components analysis suggests that most measure a common source of variance , 1994, Perception & psychophysics.

[17]  T. Bonhoeffer,et al.  Tuning and Topography in an Odor Map on the Rat Olfactory Bulb , 2001, The Journal of Neuroscience.

[18]  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.

[19]  Michael Leon,et al.  Perceptual Correlates of Neural Representations Evoked by Odorant Enantiomers , 2001, The Journal of Neuroscience.

[20]  P F Kent,et al.  Odorant-specific spatial patterns in mucosal activity predict perceptual differences among odorants. , 1995, Journal of neurophysiology.

[21]  D. G. Moulton,et al.  Spatial patterning of response to odors in the peripheral olfactory system. , 1976, Physiological reviews.

[22]  D. A. Stevens,et al.  Semantic-free scaling of odor quality , 1996, Physiology & Behavior.

[23]  Michael Leon,et al.  Olfactory coding in the mammalian olfactory bulb , 2003, Brain Research Reviews.

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

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

[26]  Forrest W. Young,et al.  Introduction to Multidimensional Scaling: Theory, Methods, and Applications , 1981 .

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

[28]  P F Kent,et al.  Odorant quality perception: A metric individual differences approach , 2000, Perception & psychophysics.

[29]  Michael Leon,et al.  Functional mapping of the rat olfactory bulb using diverse odorants reveals modular responses to functional groups and hydrocarbon structural features , 2002, The Journal of comparative neurology.

[30]  J. Falk Physiology and Behavior. , 1973 .

[31]  P. Sheehe,et al.  Mucosal inherent activity patterns in the rat: evidence from voltage-sensitive dyes. , 1995, Journal of neurophysiology.

[32]  Peter Mombaerts,et al.  Postnatal Refinement of Peripheral Olfactory Projections , 2004, Science.

[33]  Michael Leon,et al.  Spatial coding of odorant features in the glomerular layer of the rat olfactory bulb , 1998 .

[34]  C. Harley,et al.  Optical imaging of odor preference memory in the rat olfactory bulb. , 2002, Journal of neurophysiology.

[35]  E. Matyas,et al.  Odorant identification in rats: An update , 1991, Physiology & Behavior.

[36]  P. Dawes,et al.  The smell map: commonality of odour perception confirmed. , 2004, Clinical otolaryngology and allied sciences.

[37]  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.

[38]  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.

[39]  James M. Bower,et al.  Quantifying Olfactory Perception: Mapping Olfactory Perception Space by Using Multidimensional Scaling and Self-Organizing Maps , 2002, Neurocomputing.

[40]  Michael Leon,et al.  Effects of functional group position on spatial representations of aliphatic odorants in the rat olfactory bulb , 2005, The Journal of comparative neurology.

[41]  T. Brierley,et al.  A functional map in rat olfactory epithelium. , 1999, Chemical senses.

[42]  Michael Leon,et al.  Long hydrocarbon chains serve as unique molecular features recognized by ventral glomeruli of the rat olfactory bulb , 2006, The Journal of comparative neurology.

[43]  M. M. Mozell,et al.  Mucosal activity patterns as a basis for olfactory discrimination: comparing behavior and optical recordings , 2003, Brain Research.

[44]  B. Slotnick,et al.  Olfaction in rats with extensive lesions of the olfactory bulbs: implications for odor coding , 1998, Neuroscience.

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

[46]  David E. Hornung,et al.  A method for establishing a five odorant identification confusion matrix task in rats , 1990, Physiology & Behavior.

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

[48]  H. Farahbod,et al.  Chemotopic representations of aromatic odorants in the rat olfactory bulb , 2006, The Journal of comparative neurology.