Function follows form: ecological constraints on odor codes and olfactory percepts

Sensory system function has evolved to meet the biological needs of organisms, but it is less often regarded that sensory system form has by necessity evolved to contend with the stimulus. For an olfactory system extracting meaningful information from natural scents, the ecological milieu presents unique problems. Recent studies provide new insights into the perceptual and neural mechanisms underlying how odorant elements are assembled into odor wholes, how odor percepts are reconstructed from degraded inputs, and how learning and experience sculpt olfactory categorical perception. These data show that spatial ensemble activity patterns in piriform cortex are closely linked to the perceptual meaning and identity of odor objects, substantiating theoretical models that emphasize the importance of distributed templates for the perception, discrimination, and recall of olfactory quality.

[1]  Jessica Porter,et al.  Mechanisms of scent-tracking in humans , 2007, Nature Neuroscience.

[2]  Mitchell G. A. Thomson,et al.  Generalization Mediates Sensitivity to Complex Odor Features in the Honeybee , 2008, PloS one.

[3]  Lawrence C. Katz,et al.  Encoding social signals in the mouse main olfactory bulb , 2005, Nature.

[4]  M. Laska,et al.  Olfactory sensitivity for aliphatic esters in squirrel monkeys and pigtail macaques , 2002, Behavioural Brain Research.

[5]  D. Wilson,et al.  Comparison of odor receptive field plasticity in the rat olfactory bulb and anterior piriform cortex. , 2000, Journal of neurophysiology.

[6]  Donald A Wilson,et al.  Separate encoding of identity and similarity of complex familiar odors in piriform cortex , 2006, Proceedings of the National Academy of Sciences.

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

[8]  T. Thomas-Danguin,et al.  Just noticeable differences in component concentrations modify the odor quality of a blending mixture. , 2008, Chemical senses.

[9]  Thomas A Cleland,et al.  Multiple learning parameters differentially regulate olfactory generalization. , 2009, Behavioral neuroscience.

[10]  C. Linster,et al.  Odor-reward learning and enrichment have similar effects on odor perception , 2008, Physiology & Behavior.

[11]  J. Bower,et al.  Olfactory cortex: model circuit for study of associative memory? , 1989, Trends in Neurosciences.

[12]  Walter J. Freeman,et al.  EEG analysis gives model of neuronal template-matching mechanism for sensory search with olfactory bulb , 1979, Biological Cybernetics.

[13]  John Prescott,et al.  Perceptual processing strategy and exposure influence the perception of odor mixtures. , 2007, Chemical senses.

[14]  Donald A. Wilson,et al.  Experience Modifies Olfactory Acuity: Acetylcholine-Dependent Learning Decreases Behavioral Generalization between Similar Odorants , 2002, The Journal of Neuroscience.

[15]  D. B. Dusenbery Sensory Ecology: How Organisms Acquire and Respond to Information , 1992 .

[16]  G. Preti,et al.  Human odor detection of homologous carboxylic acids and their binary mixtures. , 2007, Chemical senses.

[17]  Donald A Wilson,et al.  Olfactory perceptual stability and discrimination , 2008, Nature Neuroscience.

[18]  D. G. Laing,et al.  Quality and intensity of binary odor mixtures , 1984, Physiology & Behavior.

[19]  C. Linster,et al.  Binary mixture perception is affected by concentration of odor components. , 2007, Behavioral neuroscience.

[20]  J. Rospars,et al.  Competitive and Noncompetitive Odorant Interactions in the Early Neural Coding of Odorant Mixtures , 2008, The Journal of Neuroscience.

[21]  G. Wittemyer,et al.  Chemosignalling of musth by individual wild African elephants (Loxodonta africana): implications for conservation and management , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  K. Mori,et al.  Odorant Category Profile Selectivity of Olfactory Cortex Neurons , 2007, The Journal of Neuroscience.

[23]  Julian Partridg Sensory ecology: How organisms acquire and respond to information: by David Dusenbury, W.H. Freeman, 1992. £34.95 hbk (xx + 558 pages) ISBN 0 7167 2333 6 , 1993 .

[24]  C. Mussinan,et al.  Volatile constituents of pressure cooked pork liver , 1974 .

[25]  W. Freeman,et al.  Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. , 1982, Psychophysiology.

[26]  S. Collin,et al.  Use of gas chromatography-olfactometry to identify key odorant compounds in dark chocolate. Comparison of samples before and after conching. , 2002, Journal of agricultural and food chemistry.

[27]  T. Parrish,et al.  Aversive Learning Enhances Perceptual and Cortical Discrimination of Indiscriminable Odor Cues , 2008, Science.

[28]  E. Barkai,et al.  Olfactory Learning-Induced Long-Lasting Enhancement of Descending and Ascending Synaptic Transmission to the Piriform Cortex , 2008, The Journal of Neuroscience.

[29]  M. Roesch,et al.  Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. , 2007, Cerebral cortex.

[30]  Donald A. Wilson,et al.  Synaptic adaptation and odor-background segmentation , 2007, Neurobiology of Learning and Memory.

[31]  Ronald L. Davis,et al.  Altered Representation of the Spatial Code for Odors after Olfactory Classical Conditioning Memory Trace Formation by Synaptic Recruitment , 2004, Neuron.

[32]  M. Hasselmo,et al.  Associative memory function in piriform (olfactory) cortex: computational modeling and neuropharmacology. , 1990, Cold Spring Harbor symposia on quantitative biology.

[33]  Nathalie Mandairon,et al.  Olfactory enrichment improves the recognition of individual components in mixtures , 2006, Physiology & Behavior.

[34]  Jeffrey A. Riffell,et al.  Characterization and Coding of Behaviorally Significant Odor Mixtures , 2009, Current Biology.

[35]  Raymond J. Dolan,et al.  Dissociable Codes of Odor Quality and Odorant Structure in Human Piriform Cortex , 2006, Neuron.

[36]  M. Laska,et al.  Olfactory discrimination ability of human subjects for ten pairs of enantiomers. , 1999, Chemical senses.

[37]  Matthieu Louis,et al.  A circuit supporting concentration-invariant odor perception in Drosophila , 2009, Journal of biology.

[38]  R. Sullivan,et al.  Dissociation of behavioral and neural correlates of early associative learning. , 1995, Developmental psychobiology.

[39]  Fabian Grabenhorst,et al.  How Pleasant and Unpleasant Stimuli Combine in Different Brain Regions: Odor Mixtures , 2007, The Journal of Neuroscience.

[40]  F. N. Jones,et al.  ON THE INTENSITY OF ODOR MIXTURES * , 1964, Annals of the New York Academy of Sciences.

[41]  K. Shionoya,et al.  Ontogeny of odor-LiCl vs. odor-shock learning: similar behaviors but divergent ages of functional amygdala emergence. , 2009, Learning & memory.

[42]  T. Parrish,et al.  Learning to Smell the Roses: Experience-Dependent Neural Plasticity in Human Piriform and Orbitofrontal Cortices , 2006, Neuron.

[43]  T. Thomas-Danguin,et al.  Perception of odor blending mixtures in the newborn rabbit , 2008, Physiology & Behavior.

[44]  Nathalie Mandairon,et al.  Enrichment to odors improves olfactory discrimination in adult rats. , 2006, Behavioral neuroscience.

[45]  M. Jones-Gotman,et al.  The human brain distinguishes between single odorants and binary mixtures. , 2009, Cerebral cortex.

[46]  D. Wilson,et al.  Neurobiology of associative learning in the neonate: early olfactory learning. , 1994, Behavioral and neural biology.

[47]  Lawrence C. Katz,et al.  Representation of Natural Stimuli in the Rodent Main Olfactory Bulb , 2006, Neuron.

[48]  Donald A Wilson,et al.  Olfactory cortical adaptation facilitates detection of odors against background. , 2006, Journal of neurophysiology.

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

[50]  John-Dylan Haynes,et al.  Odor quality coding and categorization in human posterior piriform cortex , 2009, Nature Neuroscience.

[51]  E. Titchener A Beginner's Psychology , 1915 .

[52]  N. Issa,et al.  Glomerular activation patterns and the perception of odor mixtures , 2008, The European journal of neuroscience.

[53]  Michael Davis,et al.  Differential regional expression of brain-derived neurotrophic factor following olfactory fear learning. , 2007, Learning & memory.

[54]  Leslie M Kay,et al.  A critical test of the overlap hypothesis for odor mixture perception. , 2009, Behavioral neuroscience.