Key Points
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An object can be defined as a 'thing' that is presented to the senses. Thus, an odour object can be defined as a smell that is presented to the olfactory sense. Although the visual and olfactory systems have evolved under different ecological pressures, many of the basic principles underlying visual object perception hold for olfactory object perception.
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Studies in which olfactory behavioural states and brain activity are monitored simultaneously in the same animal offer a direct way to relate odour object percepts to their underlying cortical signatures. These approaches, in combination with high-resolution functional MRI and multivariate statistical analysis, have advanced our understanding of odour object perception.
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The human piriform cortex is situated at the junction of the frontal and temporal lobes and is the main recipient of afferent sensory input from the olfactory bulb. Its unique anatomy, physiology and connectivity suggest that this brain region is well-suited for encoding odour objects.
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Recent data indicate that the piriform cortex is involved in key elements of odour object perception, including feature synthesis, figure–ground segregation, perceptual categorization and discrimination, and attentional selection. The chemical identity of an odour stimulus is encoded in the anterior piriform cortex, whereas the integrated perceptual representation of an odour object is encoded in posterior piriform cortex.
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Categorical percepts of odour objects take the form of spatially dispersed patterns across the piriform cortex in the apparent absence of localized clusters of activity. These distributed ensemble representations may be crucial for the olfactory brain to execute content-addressable memory and pattern completion, in which object-specific patterns can be fully reconstituted from degraded or noisy odour inputs, helping to achieve perceptual constancy.
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The principal neocortical projection area of the piriform cortex is the orbitofrontal cortex, which itself sends return projections to the piriform cortex. A plausible hypothesis of olfactory orbitofrontal function is that it provides a top-down signal that helps to resolve odour object representations in the piriform cortex, particularly under conditions of high stimulus uncertainty.
Abstract
The stimulus complexity of naturally occurring odours presents unique challenges for central nervous systems that are aiming to internalize the external olfactory landscape. One mechanism by which the brain encodes perceptual representations of behaviourally relevant smells is through the synthesis of different olfactory inputs into a unified perceptual experience — an odour object. Recent evidence indicates that the identification, categorization and discrimination of olfactory stimuli rely on the formation and modulation of odour objects in the piriform cortex. Convergent findings from human and rodent models suggest that distributed piriform ensemble patterns of olfactory qualities and categories are crucial for maintaining the perceptual constancy of ecologically inconstant stimuli.
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References
Aristotle. On Sense and the Sensible. The Internet Classics Archive [online], (350 BC).
Gross, C. G. Representation of visual stimuli in inferior temporal cortex. Phil. Trans. R. Soc. Lond. B 335, 3–10 (1992).
Ungerleider, L. G. & Haxby, J. V. 'What' and 'where' in the human brain. Curr. Opin. Neurobiol. 4, 157–165 (1994).
Logothetis, N. K. & Sheinberg, D. L. Visual object recognition. Annu. Rev. Neurosci. 19, 577–621 (1996).
Tanaka, K. Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109–139 (1996).
Wallis, G. & Rolls, E. T. Invariant face and object recognition in the visual system. Prog. Neurobiol. 51, 167–194 (1997).
Treisman, A. M. & Kanwisher, N. G. Perceiving visually presented objects: recognition, awareness, and modularity. Curr. Opin. Neurobiol. 8, 218–226 (1998).
Riesenhuber, M. & Poggio, T. Neural mechanisms of object recognition. Curr. Opin. Neurobiol. 12, 162–168 (2002).
Palmeri, T. J. & Gauthier, I. Visual object understanding. Nature Rev. Neurosci. 5, 291–303 (2004).
Freedman, D. J. & Miller, E. K. Neural mechanisms of visual categorization: insights from neurophysiology. Neurosci. Biobehav. Rev. 32, 311–329 (2008).
Kubovy, M. & Van Valkenburg, D. Auditory and visual objects. Cognition 80, 97–126 (2001).
Griffiths, T. D. & Warren, J. D. What is an auditory object? Nature Rev. Neurosci. 5, 887–892 (2004).
Dubois, D. Categories as acts of meaning: the case of categories in olfaction and audition. Cogn. Sci. Quart. 1, 35–68 (2000).
Stevenson, R. J. & Wilson, D. A. Odour perception: an object-recognition approach. Perception 36, 1821–1833 (2007). Drawing from psychological studies in humans and electrophysiological studies in rodents, this review provides a thoughtful account of odour object perception.
Maplet, J. A greene forest or a naturall historie, wherein may be seene first the most sufferaigne vertues in all the whole kinde of stones and metals: next of plantes, as of herbes, trees, and shrubs, lastly of brute beastes, foules, fishes, creeping wormes, and serpents, and that alphabetically: so that a table shall not neede (H. Denham, London, 1567).
Johnson, B. A. & Leon, M. Chemotopic odorant coding in a mammalian olfactory system. J. Comp. Neurol. 503, 1–34 (2007).
Wilson, R. I. Neural and behavioral mechanisms of olfactory perception. Curr. Opin. Neurobiol. 18, 408–412 (2008).
Kay, L. M. et al. Olfactory oscillations: the what, how and what for. Trends Neurosci. 32, 207–214 (2009).
Linster, C. & Cleland, T. A. Glomerular microcircuits in the olfactory bulb. Neural Netw. 22, 1169–1173 (2009).
Restrepo, D., Doucette, W., Whitesell, J. D., McTavish, T. S. & Salcedo, E. From the top down: flexible reading of a fragmented odor map. Trends Neurosci. 32, 525–531 (2009).
Strowbridge, B. W. Role of cortical feedback in regulating inhibitory microcircuits. Ann. NY Acad. Sci. 1170, 270–274 (2009).
Su, C. Y., Menuz, K. & Carlson, J. R. Olfactory perception: receptors, cells, and circuits. Cell 139, 45–59 (2009).
Urban, N. N. & Arevian, A. C. Computing with dendrodendritic synapses in the olfactory bulb. Ann. NY Acad. Sci. 1170, 264–269 (2009).
Zou, D. J., Chesler, A. & Firestein, S. How the olfactory bulb got its glomeruli: a just so story? Nature Rev. Neurosci. 10, 611–618 (2009).
Cleland, T. A. Early transformations in odor representation. Trends Neurosci. 33, 130–139 (2010).
Isaacson, J. S. Odor representations in mammalian cortical circuits. Curr. Opin. Neurobiol. 5 Mar 2010 (doi:10.1016/j.conb.2010.02.004).
Kay, L. M., Crk, T. & Thorngate, J. A redefinition of odor mixture quality. Behav. Neurosci. 119, 726–733 (2005).
Laing, D. G. & Francis, G. W. The capacity of humans to identify odors in mixtures. Physiol. Behav. 46, 809–814 (1989).
Livermore, A. & Laing, D. G. Influence of training and experience on the perception of multicomponent odor mixtures. J. Exp. Psychol. Hum. Percept. Perform. 22, 267–277 (1996).
de Olmos, J., Hardy, H. & Heimer, L. The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP-study. J. Comp. Neurol. 181, 213–244 (1978).
Carmichael, S. T., Clugnet, M. C. & Price, J. L. Central olfactory connections in the macaque monkey. J. Comp. Neurol. 346, 403–434 (1994). A tour de force study combining anatomical tracers and electrophysiological recordings to delineate olfactory connectivity in primate olfactory cortex.
Shipley, M. T. & Ennis, M. Functional organization of olfactory system. J. Neurobiol. 30, 123–176 (1996).
Haberly, L. B. in The Synaptic Organization of the Brain (ed. Shepherd, G. M.) 377–416 (Oxford Univ. Press, New York, 1998).
Johnson, D. M., Illig, K. R., Behan, M. & Haberly, L. B. New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that “primary” olfactory cortex functions like “association” cortex in other sensory systems. J. Neurosci. 20, 6974–6982 (2000).
Cleland, T. A., Linster, C. & Doty, R. L. in Handbook of Olfaction and Gustation (ed. Doty, R. L.) 165–180 (Marcel Dekker, New York, 2003).
Wilson, D. A., Sullivan, R. M. & Doty, R. L. in Handbook of Olfaction and Gustation (ed. Doty, R. L.) 181–201 (Marcel Dekker, New York, 2003).
Mesulam, M. M. From sensation to cognition. Brain 121, 1013–1052 (1998).
Stevenson, R. J. An initial evaluation of the functions of human olfaction. Chem. Senses 35, 3–20 (2010).
Haberly, L. B. & Price, J. L. Association and commissural fiber systems of the olfactory cortex of the rat. J. Comp. Neurol. 178, 711–740 (1978).
Kay, L. M. & Freeman, W. J. Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behav. Neurosci. 112, 541–553 (1998).
Haberly, L. B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26, 551–576 (2001).
Chen, S., Murakami, K., Oda, S. & Kishi, K. Quantitative analysis of axon collaterals of single cells in layer III of the piriform cortex of the guinea pig. J. Comp. Neurol. 465, 455–465 (2003).
O'Doherty, J. et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11, 893–897 (2000).
Dade, L. A., Zatorre, R. J. & Jones-Gotman, M. Olfactory learning: convergent findings from lesion and brain imaging studies in humans. Brain 125, 86–101 (2002).
Gottfried, J. A., O'Doherty, J. & Dolan, R. J. Appetitive and aversive olfactory learning in humans studied using event-related functional magnetic resonance imaging. J. Neurosci. 22, 10829–10837 (2002).
Gottfried, J. A., O'Doherty, J. & Dolan, R. J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104–1107 (2003).
Gottfried, J. A., Smith, A. P., Rugg, M. D. & Dolan, R. J. Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron 42, 687–695 (2004).
Zelano, C. et al. Attentional modulation in human primary olfactory cortex. Nature Neurosci. 8, 114–120 (2005).
Cerf-Ducastel, B. & Murphy, C. Neural substrates of cross-modal olfactory recognition memory: an fMRI study. Neuroimage 31, 386–396 (2006).
Plailly, J., Howard, J. D., Gitelman, D. R. & Gottfried, J. A. Attention to odor modulates thalamocortical connectivity in the human brain. J. Neurosci. 28, 5257–5267 (2008).
Small, D. M., Veldhuizen, M. G., Felsted, J., Mak, Y. E. & McGlone, F. Separable substrates for anticipatory and consummatory food chemosensation. Neuron 57, 786–797 (2008).
Zelano, C., Montag, J., Khan, R. & Sobel, N. A specialized odor memory buffer in primary olfactory cortex. PLoS ONE 4, e4965 (2009).
Henkin, R. I., Comiter, H., Fedio, P. & O'Doherty, D. Defects in taste and smell recognition following temporal lobectomy. Trans. Am. Neurol. Assoc. 102, 146–150 (1977).
Abraham, A. & Mathai, K. V. The effect of right temporal lobe lesions on matching of smells. Neuropsychologia 21, 277–281 (1983).
Eskenazi, B., Cain, W. S., Novelly, R. A. & Friend, K. B. Olfactory functioning in temporal lobectomy patients. Neuropsychologia 21, 365–374 (1983).
Jones-Gotman, M. & Zatorre, R. J. Olfactory identification deficits in patients with focal cerebral excision. Neuropsychologia 26, 387–400 (1988).
Martinez, B. A. et al. Olfactory functioning before and after temporal lobe resection for intractable seizures. Neuropsychology 7, 351–363 (1993).
West, S. E. & Doty, R. L. Influence of epilepsy and temporal lobe resection on olfactory function. Epilepsia 36, 531–542 (1995).
Eichenbaum, H., Shedlack, K. J. & Eckmann, K. W. Thalamocortical mechanisms in odor-guided behavior. I. Effects of lesions of the mediodorsal thalamic nucleus and frontal cortex on olfactory discrimination in the rat. Brain Behav. Evol. 17, 255–275 (1980).
Litaudon, P., Mouly, A. M., Sullivan, R., Gervais, R. & Cattarelli, M. Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur. J. Neurosci. 9, 1593–1602 (1997).
Chabaud, P. et al. Exposure to behaviourally relevant odour reveals differential characteristics in rat central olfactory pathways as studied through oscillatory activities. Chem. Senses 25, 561–573 (2000).
Mouly, A. M., Fort, A., Ben-Boutayab, N. & Gervais, R. Olfactory learning induces differential long-lasting changes in rat central olfactory pathways. Neuroscience 102, 11–21 (2001).
Gottfried, J. A., Deichmann, R., Winston, J. S. & Dolan, R. J. Functional heterogeneity in human olfactory cortex: an event-related functional magnetic resonance imaging study. J. Neurosci. 22, 10819–10828 (2002).
Litaudon, P., Amat, C., Bertrand, B., Vigouroux, M. & Buonviso, N. Piriform cortex functional heterogeneity revealed by cellular responses to odours. Eur. J. Neurosci. 17, 2457–2461 (2003).
Martin, C., Gervais, R., Chabaud, P., Messaoudi, B. & Ravel, N. Learning-induced modulation of oscillatory activities in the mammalian olfactory system: the role of the centrifugal fibres. J. Physiol. (Paris) 98, 467–478 (2004).
Calu, D. J., Roesch, M. R., Stalnaker, T. A. & Schoenbaum, G. Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb. Cortex 17, 1342–1349 (2007). This article and those cited in references 67 and 97 represent the small handful of rodent studies that have provided methodical comparisons between odor-related single-unit responses in the piriform cortex and the orbitofrontal cortex.
Roesch, M. R., Stalnaker, T. A. & Schoenbaum, G. Associative encoding in anterior piriform cortex versus orbitofrontal cortex during odor discrimination and reversal learning. Cereb. Cortex 17, 643–652 (2007).
Sharp, F. R., Kauer, J. S. & Shepherd, G. M. Laminar analysis of 2-deoxyglucose uptake in olfactory bulb and olfactory cortex of rabbit and rat. J. Neurophysiol. 40, 800–813 (1977).
Astic, L. & Cattarelli, M. Metabolic mapping of functional activity in the rat olfactory system after a bilateral transection of the lateral olfactory tract. Brain Res. 245, 17–25 (1982).
Cattarelli, M., Astic, L. & Kauer, J. S. Metabolic mapping of 2-deoxyglucose uptake in the rat piriform cortex using computerized image processing. Brain Res. 442, 180–184 (1988).
Illig, K. R. & Haberly, L. B. Odor-evoked activity is spatially distributed in piriform cortex. J. Comp. Neurol. 457, 361–373 (2003).
Mori, K., Takahashi, Y. K., Igarashi, K. M. & Yamaguchi, M. Maps of odorant molecular features in the mammalian olfactory bulb. Physiol. Rev. 86, 409–433 (2006).
Soucy, E. R., Albeanu, D. F., Fantana, A. L., Murthy, V. N. & Meister, M. Precision and diversity in an odor map on the olfactory bulb. Nature Neurosci. 12, 210–220 (2009). A comprehensive imaging investigation of odorant-evoked sensory tuning in rodent olfactory bulb that challenges the longstanding dogma that there is a tight systematic relationship between glomerular position and odorant chemical features.
Sugai, T., Miyazawa, T., Fukuda, M., Yoshimura, H. & Onoda, N. Odor-concentration coding in the guinea-pig piriform cortex. Neuroscience 130, 769–781 (2005).
Luna, V. M. & Pettit, D. L. Asymmetric rostro-caudal inhibition in the primary olfactory cortex. Nature Neurosci. 13, 533–535 (2010).
Franks, K. M. & Isaacson, J. S. Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49, 357–363 (2006).
Poo, C. & Isaacson, J. S. Odor representations in olfactory cortex: “sparse” coding, global inhibition, and oscillations. Neuron 62, 850–861 (2009).
Luna, V. M. & Schoppa, N. E. GABAergic circuits control input-spike coupling in the piriform cortex. J. Neurosci. 28, 8851–8859 (2008).
Rennaker, R. L., Chen, C. F., Ruyle, A. M., Sloan, A. M. & Wilson, D. A. Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J. Neurosci. 27, 1534–1542 (2007).
Stettler, D. D. & Axel, R. Representations of odor in the piriform cortex. Neuron 63, 854–864 (2009). Results from this in vivo optical imaging study indicate that odorant-related response patterns are spatially distributed and overlapping across neuronal ensembles in the mouse piriform cortex. These findings complement well the human data in reference 137.
Mountcastle, V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J. Neurophysiol. 20, 408–434 (1957).
Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195, 215–243 (1968).
Woolsey, T. A. & Van der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17, 205–242 (1970).
Kay, L. M. & Sherman, S. M. An argument for an olfactory thalamus. Trends Neurosci. 30, 47–53 (2007).
Shepherd, G. M. Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann. NY Acad. Sci. 1121, 87–101 (2007).
Sherman, S. M. & Guillery, R. W. The role of the thalamus in the flow of information to the cortex. Phil. Trans. R. Soc. Lond. B 357, 1695–1708 (2002).
Jones, E. G. The Thalamus (Cambridge Univ. Press, Cambridge, UK, 2006).
Kastner, S., Schneider, K. A. & Wunderlich, K. Beyond a relay nucleus: neuroimaging views on the human LGN. Prog. Brain Res. 155, 125–143 (2006).
Yarita, H., Iino, M., Tanabe, T., Kogure, S. & Takagi, S. F. A transthalamic olfactory pathway to orbitofrontal cortex in the monkey. J. Neurophysiol. 43, 69–85 (1980).
Price, J. L. & Slotnick, B. M. Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study. J. Comp. Neurol. 215, 63–77 (1983).
Zelano, C., Montag, J., Johnson, B., Khan, R. & Sobel, N. Dissociated representations of irritation and valence in human primary olfactory cortex. J. Neurophysiol. 97, 1969–1976 (2007).
Sela, L. et al. Spared and impaired olfactory abilities after thalamic lesions. J. Neurosci. 29, 12059–12069 (2009).
Tham, W. W., Stevenson, R. J. & Miller, L. A. The functional role of the medio dorsal thalamic nucleus in olfaction. Brain Res. Rev. 62, 109–126 (2009).
Jerison, H. J. in Development of the Prefrontal Cortex: Evolution, Neurobiology, and Behavior (eds Krasnegor, N. A., Lyon, G. R. & Goldman-Rakic, P. S.) 27–47 (Paul, H. Brookes, Baltimore, Maryland, 1997).
Gottfried, J. A. What can an orbitofrontal cortex-endowed animal do with smells. Ann. NY Acad. Sci. 1121, 102–120 (2007).
Tanabe, T., Iino, M. & Takagi, S. F. Discrimination of odors in olfactory bulb, pyriform-amygdaloid areas, and orbitofrontal cortex of the monkey. J. Neurophysiol. 38, 1284–1296 (1975).
Schoenbaum, G. & Eichenbaum, H. Information coding in the rodent prefrontal cortex. I. Single-neuron activity in orbitofrontal cortex compared with that in pyriform cortex. J. Neurophysiol. 74, 733–750 (1995).
Critchley, H. D. & Rolls, E. T. Olfactory neuronal responses in the primate orbitofrontal cortex: analysis in an olfactory discrimination task. J. Neurophysiol. 75, 1659–1672 (1996).
Critchley, H. D. & Rolls, E. T. Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex. J. Neurophysiol. 75, 1673–1686 (1996).
Rolls, E. T. & Baylis, L. L. Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J. Neurosci. 14, 5437–5452 (1994).
Small, D. M., Jones-Gotman, M., Zatorre, R. J., Petrides, M. & Evans, A. C. Flavor processing: more than the sum of its parts. Neuroreport 8, 3913–3917 (1997).
Royet, J. P. et al. Functional anatomy of perceptual and semantic processing for odors. J. Cogn. Neurosci. 11, 94–109 (1999).
Savic, I., Gulyas, B., Larsson, M. & Roland, P. Olfactory functions are mediated by parallel and hierarchical processing. Neuron 26, 735–745 (2000).
Anderson, A. K. et al. Dissociated neural representations of intensity and valence in human olfaction. Nature Neurosci. 6, 196–202 (2003).
De Araujo, I. E., Rolls, E. T., Kringelbach, M. L., McGlone, F. & Phillips, N. Taste-olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur. J. Neurosci. 18, 2059–2068 (2003).
Gottfried, J. A. & Dolan, R. J. The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 39, 375–386 (2003).
Gottfried, J. A. & Dolan, R. J. Human orbitofrontal cortex mediates extinction learning while accessing conditioned representations of value. Nature Neurosci. 7, 1144–1152 (2004).
Small, D. M. et al. Experience-dependent neural integration of taste and smell in the human brain. J. Neurophysiol. 92, 1892–1903 (2004).
Osterbauer, R. A. et al. Color of scents: chromatic stimuli modulate odor responses in the human brain. J. Neurophysiol. 93, 3434–3441 (2005).
Boyle, J. A., Frasnelli, J., Gerber, J., Heinke, M. & Hummel, T. Cross-modal integration of intranasal stimuli: a functional magnetic resonance imaging study. Neuroscience 149, 223–231 (2007).
Potter, H. & Butters, N. An assessment of olfactory deficits in patients with damage to prefrontal cortex. Neuropsychologia 18, 621–628 (1980).
Zatorre, R. J. & Jones-Gotman, M. Human olfactory discrimination after unilateral frontal or temporal lobectomy. Brain 114, 71–84 (1991).
Jones-Gotman, M. & Zatorre, R. J. Odor recognition memory in humans: role of right temporal and orbitofrontal regions. Brain Cogn. 22, 182–198 (1993).
Li, W. et al. Right orbitofrontal cortex mediates conscious olfactory perception. Psychol. Sci. (in the press).
Stevenson, R. J. Phenomenal and access consciousness in olfaction. Conscious. Cogn. 18, 1004–1017 (2009).
Sekiwa, Y., Kubota, K. & Kobayashi, A. Characteristic flavor components in the brew of cooked clam (Meretrix lusoria) and the effect of storage on flavor formation. J. Agric. Food Chem. 45, 826–830 (1997).
Wilson, D. A. Rapid, experience-induced enhancement in odorant discrimination by anterior piriform cortex neurons. J. Neurophysiol. 90, 65–72 (2003). References 117, 147 and 148 comprise an important set of studies establishing that odour configural processing occurs in rodent anterior piriform cortex as a consequence of olfactory habituation; a non-associative form of perceptual learning. Insights from this study paved the way for a similar but human-based study that is described in reference 129.
Gottfried, J. A., Winston, J. S. & Dolan, R. J. Dissociable codes of odor quality and odorant structure in human piriform cortex. Neuron 49, 467–479 (2006).
Kadohisa, M. & Wilson, D. A. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc. Natl Acad. Sci. USA 103, 15206–15211 (2006).
Schwob, J. E. & Price, J. L. The cortical projection of the olfactory bulb: development in fetal and neonatal rats correlated with quantitative variations in adult rats. Brain Res. 151, 369–374 (1978).
Haberly, L. B. Neuronal circuitry in olfactory cortex: anatomy and functional implications. Chem. Senses 10, 219–238 (1985). An authoritative review of olfactory cortical anatomy and function. It was among the first to propose that the piriform cortex might serve as a content-addressable memory system for efficient perceptual reconstruction of odour inputs.
Kadohisa, M. & Wilson, D. A. Olfactory cortical adaptation facilitates detection of odors against background. J. Neurophysiol. 95, 1888–1896 (2006).
Yoshida, I. & Mori, K. Odorant category profile selectivity of olfactory cortex neurons. J. Neurosci. 27, 9105–9114 (2007).
Lamme, V. A. The neurophysiology of figure-ground segregation in primary visual cortex. J. Neurosci. 15, 1605–1615 (1995).
Linster, C., Henry, L., Kadohisa, M. & Wilson, D. A. Synaptic adaptation and odor-background segmentation. Neurobiol. Learn. Mem. 87, 352–360 (2007).
Best, A. R., Thompson, J. V., Fletcher, M. L. & Wilson, D. A. Cortical metabotropic glutamate receptors contribute to habituation of a simple odor-evoked behavior. J. Neurosci. 25, 2513–2517 (2005).
Yadon, C. A. & Wilson, D. A. The role of metabotropic glutamate receptors and cortical adaptation in habituation of odor-guided behavior. Learn. Mem. 12, 601–605 (2005).
Sobel, N. et al. Time course of odorant-induced activation in the human primary olfactory cortex. J. Neurophysiol. 83, 537–551 (2000). This pioneering olfactory fMRI experiment demonstrated that continuous odour stimulation elicits profound response habituation in the human piriform cortex, providing an important foundation for the design of subsequent fMRI studies.
Li, W., Luxenberg, E., Parrish, T. & Gottfried, J. A. Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbitofrontal cortices. Neuron 52, 1097–1108 (2006).
Verhagen, J. V., Wesson, D. W., Netoff, T. I., White, J. A. & Wachowiak, M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nature Neurosci. 10, 631–639 (2007).
Leinders-Zufall, T., Greer, C. A., Shepherd, G. M. & Zufall, F. Imaging odor-induced calcium transients in single olfactory cilia: specificity of activation and role in transduction. J. Neurosci. 18, 5630–5639 (1998).
Duchamp-Viret, P., Duchamp, A. & Chaput, M. A. Peripheral odor coding in the rat and frog: quality and intensity specification. J. Neurosci. 20, 2383–2390 (2000).
McGann, J. P. et al. Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48, 1039–1053 (2005).
Wachowiak, M. et al. Inhibition [corrected] of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J. Neurophysiol. 94, 2700–2712 (2005).
Rosch, E. H. in Cognition and Categorization (eds Rosch, E. H. & Lloyd, B.) 27–48 (Erlbaum Associates, Hillsdale, New Jersey, 1978).
Miller, E. K., Nieder, A., Freedman, D. J. & Wallis, J. D. Neural correlates of categories and concepts. Curr. Opin. Neurobiol. 13, 198–203 (2003).
Howard, J. D., Plailly, J., Grueschow, M., Haynes, J. D. & Gottfried, J. A. Odor quality coding and categorization in human posterior piriform cortex. Nature Neurosci. 12, 932–938 (2009). In this study, high-resolution olfactory fMRI was combined with multivariate pattern analyses to show that odour object categories are encoded as spatially distributed ensemble representations in the human posterior piriform cortex. These findings complement well the mouse data in reference 80.
Kriegeskorte, N. & Bandettini, P. Analyzing for information, not activation, to exploit high-resolution fMRI. Neuroimage 38, 649–662 (2007).
Barnes, D. C., Hofacer, R. D., Zaman, A. R., Rennaker, R. L. & Wilson, D. A. Olfactory perceptual stability and discrimination. Nature Neurosci. 11, 1378–1380 (2008). This article presents compelling evidence for the role of rodent piriform cortex, but not olfactory bulb, in the perceptual pattern completion of degraded odour inputs.
Laurent, G. A systems perspective on early olfactory coding. Science 286, 723–728 (1999).
Haxby, J. V. et al. Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293, 2425–2430 (2001).
Cox, D. D. & Savoy, R. L. Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex. Neuroimage 19, 261–270 (2003).
Haushofer, J., Livingstone, M. S. & Kanwisher, N. Multivariate patterns in object-selective cortex dissociate perceptual and physical shape similarity. PLoS Biol. 6, e187 (2008).
Potter, B. The Tale of Samuel Whiskers, or The Roly-Poly Pudding (Frederick Warne & Co., London, 1908).
Gibson, E. J. An Odyssey in Learning and Perception (MIT Press, Cambridge, Massachusetts, 1991).
Goldstone, R. L. Perceptual learning. Annu. Rev. Psychol. 49, 585–612 (1998).
Wilson, D. A. Habituation of odor responses in the rat anterior piriform cortex. J. Neurophysiol. 79, 1425–1440 (1998).
Wilson, D. A. Comparison of odor receptive field plasticity in the rat olfactory bulb and anterior piriform cortex. J. Neurophysiol. 84, 3036–3042 (2000).
Pager, J. & Royet, J. P. Some effects of conditioned aversion on food intake and olfactory bulb electrical responses in the rat. J. Comp. Physiol. Psychol. 90, 67–77 (1976).
Freeman, W. J. & Schneider, W. Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19, 44–56 (1982).
Coopersmith, R., Lee, S. & Leon, M. Olfactory bulb responses after odor aversion learning by young rats. Brain Res. 389, 271–277 (1986).
Wilson, D. A. & Sullivan, R. M. Neurobiology of associative learning in the neonate: early olfactory learning. Behav. Neural Biol. 61, 1–18 (1994).
Sullivan, R. M. & Wilson, D. A. Dissociation of behavioral and neural correlates of early associative learning. Dev. Psychobiol. 28, 213–219 (1995).
Li, W., Howard, J. D., Parrish, T. B. & Gottfried, J. A. Aversive learning enhances perceptual and cortical discrimination of indiscriminable odor cues. Science 319, 1842–1845 (2008). Following rodent models of aversive learning (references 149–153), this human imaging study demonstrated that previously indistinguishable odorants become discriminable after odour–footshock conditioning. This was observed both at the level of odour perception and at the level of functional MRI ensemble pattern activity in the human posterior piriform cortex.
Sabri, M., Radnovich, A. J., Li, T. Q. & Kareken, D. A. Neural correlates of olfactory change detection. Neuroimage 25, 969–974 (2005).
Friston, K. J., Harrison, L. & Penny, W. Dynamic causal modelling. Neuroimage 19, 1273–1302 (2003).
Murakami, M., Kashiwadani, H., Kirino, Y. & Mori, K. State-dependent sensory gating in olfactory cortex. Neuron 46, 285–296 (2005).
Rasch, B., Büchel, C., Gais, S. & Born, J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315, 1426–1429 (2007).
Yeshurun, Y. & Sobel, N. An odor is not worth a thousand words: from multidimensional odors to unidimensional odor objects. Annu. Rev. Psychol. 61, 219–241, C211–215 (2010).
Hopfield, J. J. Neural networks and physical systems with emergent collective computational abilities. Proc. Natl Acad. Sci. USA 79, 2554–2558 (1982).
Hasselmo, M. E., Wilson, M. A., Anderson, B. P. & Bower, J. M. Associative memory function in piriform (olfactory) cortex: computational modeling and neuropharmacology. Cold Spring Harb. Symp. Quant. Biol. 55, 599–610 (1990).
Wilson, M. & Bower, J. M. Cortical oscillations and temporal interactions in a computer simulation of piriform cortex. J. Neurophysiol. 67, 981–995 (1992).
Kay, L. M. & Stopfer, M. Information processing in the olfactory systems of insects and vertebrates. Semin. Cell Dev. Biol. 17, 433–442 (2006).
Cohen, Y., Reuveni, I., Barkai, E. & Maroun, M. Olfactory learning-induced long-lasting enhancement of descending and ascending synaptic transmission to the piriform cortex. J. Neurosci. 28, 6664–6669 (2008).
Rinberg, D. & Gelperin, A. Olfactory neuronal dynamics in behaving animals. Semin. Cell Dev. Biol. 17, 454–461 (2006).
Lin, D. Y., Zhang, S. Z., Block, E. & Katz, L. C. Encoding social signals in the mouse main olfactory bulb. Nature 434, 470–477 (2005).
Lin, D. Y., Shea, S. D. & Katz, L. C. Representation of natural stimuli in the rodent main olfactory bulb. Neuron 50, 937–949 (2006).
Riffell, J. A., Lei, H., Christensen, T. A. & Hildebrand, J. G. Characterization and coding of behaviorally significant odor mixtures. Curr. Biol. 19, 335–340 (2009).
Riffell, J. A., Lei, H. & Hildebrand, J. G. Inaugural Article: Neural correlates of behavior in the moth Manduca sexta in response to complex odors. Proc. Natl Acad. Sci. USA 106, 19219–19226 (2009).
Zelano, C. & Sobel, N. Humans as an animal model for systems-level organization of olfaction. Neuron 48, 431–454 (2005).
Parrish, T., Chen, Y. F., Li, W., Howard, J. & Gottfried, J. A. High resolution 3D functional images of the human olfactory bulb using Passband SSFP at 3T. ISMRM website [online], (2008).
Firestein, S. How the olfactory system makes sense of scents. Nature 413, 211–218 (2001).
Buck, L. B. Olfactory receptors and odor coding in mammals. Nutr. Rev. 62, S184–188; discussion S224–141 (2004).
Wachowiak, M. & Shipley, M. T. Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin. Cell Dev. Biol. 17, 411–423 (2006).
Shepherd, G. M., Chen, W. R., Willhite, D., Migliore, M. & Greer, C. A. The olfactory granule cell: from classical enigma to central role in olfactory processing. Brain Res. Rev. 55, 373–382 (2007).
Malnic, B., Hirono, J., Sato, T. & Buck, L. B. Combinatorial receptor codes for odors. Cell 96, 713–723 (1999).
Linster, C. et al. Perceptual correlates of neural representations evoked by odorant enantiomers. J. Neurosci. 21, 9837–9843 (2001).
Cleland, T. A., Morse, A., Yue, E. L. & Linster, C. Behavioral models of odor similarity. Behav. Neurosci. 116, 222–231 (2002).
Maresh, A., Rodriguez Gil, D., Whitman, M. C. & Greer, C. A. Principles of glomerular organization in the human olfactory bulb — implications for odor processing. PLoS ONE 3, e2640 (2008). This important anatomical study suggests that the human olfactory bulb is organized in a fundamentally different way to the rodent analogue, raising questions about cross-species functional homologies.
Smith, G. E. Notes upon the natural subdivision of the cerebral hemisphere. J. Anat. Physiol. 35, 431–454 (1901).
Sander, J. in Archiv für Anatomie, Physiologie und wissenschaftliche Medicin (eds Reichert, C. B. & Du Bois-Reymond, E.) 750–756 (Verlag von Veit et Comp., Leipzig, 1866).
Acknowledgements
The author would like to thank the members of the Gottfried Laboratory for helpful comments and suggestions. The author is supported by grants from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health, USA.
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Glossary
- Odours
-
Perceived smells that emanate from an odorant or mixture of odorants.
- Odorant
-
A chemical stimulus that is capable of evoking a smell. In terrestrial animals, most odorants are organic molecules of low molecular weight that can gain airborne access to the olfactory system.
- Configural odour perception
-
The perception of an odour mixture that differs from the perception of the mixture elements; that is, the mixture configuration is perceived holistically rather than as the sum of its parts.
- Elemental odour perception
-
The perception of an odour mixture that is the same as the perception of the summed mixture elements.
- Chemotopy
-
The idea that information about odorant chemical composition is projected onto topographically ordered spatial maps in the olfactory brain.
- 2-deoxyglucose methods
-
A functional brain mapping technique that uses radioactive 2-[14C]deoxyglucose to measure local metabolic patterns of activity-dependent glucose uptake in the central nervous system.
- Odour quality
-
The perceptual character of a smell, such as mintiness, that emanates from an odorous object, as opposed to other perceptual features of a smell, such as intensity or pleasantness.
- Focal electrical stimulation
-
An electrophysiological technique that limits the extent of electrical stimulation to single axon fibres. This permits quantification of synaptic transmission at the level of individual synapses.
- Respiratory entrainment
-
The time at which odorant-evoked neural activity, usually in the form of single-unit spike firing, is most prominent during a particular phase of the respiratory cycle.
- Prepotent responses
-
Behavioural responses with the greatest ('most potent') tendencies of being evoked by given sensory stimuli — often innate, reflexive responses.
- Tuning specificity
-
The idea that the response activity (or 'tuning') of a given neuron is specific for a particular range of stimulus inputs. This tuning may be highly specific and 'narrow' (or non-specific and 'broad').
- Olfactory valence
-
The appetitive or aversive nature of an olfactory stimulus.
- Anosmia
-
Complete loss of the sense of smell, typically caused by trauma, infection or nasal–sinus disease, but often arising without an identifiable cause.
- fMRI cross-adaptation
-
A paradigm based on the concept that sequential presentation of stimuli that share a particular feature, such as olfactory quality, causes response decline (or adaptation) in neural populations that are sensitive to that feature.
- Figure–ground segmentation
-
The ability to discriminate, or segment, foreground details from background distracters. It is also referred to as figure–ground separation or segregation and is a necessary aspect of object perception.
- Go/No-go task
-
In this classic discrimination task, animal or human subjects are required to make a response ('go') when presented with a particular stimulus cue and to withhold a response ('no-go') when presented with a different one.
- Intraglomerular feedback inhibition
-
An important mechanism of synaptic inhibition in the olfactory bulb glomerulus, in which GABA (γ-aminobutyric acid)-ergic interneurons send direct inhibitory projections back to the same odour-activated mitral or tufted cells, forming a disynaptic feedback arc.
- Cortical flattening algorithm
-
A computational method for unfolding a three-dimensional image of the brain into a flattened two-dimensional cortical sheet, making it easier to visualise topographical patterns of functional activity. These algorithms have been widely applied in retinotopic mapping of the primary visual cortex.
- Multivariate fMRI analysis
-
A method of functional MRI data analysis designed to preserve activity-dependent signal change at the level of individual voxels and that allows the characterization of multi-voxel, pattern-based information within a brain region of interest.
- Voxel-wise pattern
-
An ensemble pattern of functional MRI activity distributed spatially across a set of voxels.
- Univariate fMRI analysis
-
A method of functional MRI data analysis in which data are spatially averaged and smoothed across trials, voxels and subjects, and that yields a mean estimate of peak fMRI activity for a given region of interest.
- Pattern completion
-
A concept that is pertinent to content-addressable memory and in which an object-specific pattern representation can be fully reconstituted, or 'completed', from an incomplete stimulus input, helping to achieve perceptual constancy.
- Virtual ensembles of single-unit activity
-
An analytical method that pools single-unit responses from different cells and different subjects into a virtual ensemble of a spatially distributed activity.
- Pattern separation
-
The opposite of pattern completion. Learning and experience can induce a divergence, or 'separation', of object-specific pattern representations that were formerly overlapping, helping to enhance perceptual discrimination.
- Perceptual learning
-
An increase in sensory acuity following a period of perceptual training that may or may not be explicit. The perceptual enhancement is relatively specific for the types of sensory stimuli that were encountered during initial learning.
- Aversive conditioning
-
A type of associative learning paradigm in which a previously innocuous stimulus acquires behavioural salience after being repetitively paired with an aversive event such as an electric shock.
- fMRI effective connectivity
-
A technique that is used to compute the causal links, or 'effects', that one brain region exerts on another, based on functional MRI data sets.
- Signal fidelity
-
In the context of neural information processing and transformation, this term refers to how closely an output signal or representation corresponds to the input.
- Content-addressable memory
-
A computationally robust form of associative memory that effectively functions as a reference table that allows the retrieval of specific memories in response to a particular smell.
- Object coding
-
The neurobiological processes by which perceptually relevant information about an object is encoded or represented in the brain.
- Diffusion-tensor imaging
-
An MRI technique that provides a three-dimensional image of water diffusion in the brain. As water diffuses more readily along the axis of myelinated nerve-fibre tracts, this method can be used to obtain a non-invasive estimate of anatomical connectivity between brain areas.
- Transcranial magnetic stimulation
-
A method that involves applying local magnetic stimulation at the scalp to induce electrical excitation of the underlying cortical areas and their projections. The technique can be used to study cortical excitability and reorganization, as well as to disrupt or enhance activity in specific brain regions.
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Gottfried, J. Central mechanisms of odour object perception. Nat Rev Neurosci 11, 628–641 (2010). https://doi.org/10.1038/nrn2883
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DOI: https://doi.org/10.1038/nrn2883
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