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11 - The construction of olfactory representations

Published online by Cambridge University Press:  14 August 2009

Christian Holscher
Affiliation:
University of Ulster
Matthias Munk
Affiliation:
Max-Planck-Institut für biologische Kybernetik, Tübingen
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Summary

Introduction

Sensory information progresses centrally from the primary sensors in the periphery to the central neural structures that derive relevant environmental information from these sensory data and determine appropriate physiological and behavioral responses. In this chapter, I present a general theory of early olfactory sensory processing in the primary olfactory epithelium and olfactory bulb (OB). The theory depicts olfactory sensory processing as a cascade of representations, each of which exhibits characteristic physical properties and is sampled by appropriate neural mechanisms in order to construct the subsequent representation. The primary olfactory representation is mediated by the activation pattern across the population of primary olfactory sensory neurons (OSNs) in the sensory epithelium. The secondary olfactory representation is similarly mediated by the activation pattern across the population of principal neurons immediately postsynaptic to the OSNs, known as mitral cells. (Mitral cell axons diverge dramatically, projecting to roughly ten different central structures within the brain; the resulting tertiary and subsequent olfactory representations are constructed outside the olfactory bulb and are not discussed at length herein.) The transformation between the primary and secondary representations is a robust, intricate, two-stage process that corrects for artefacts that can hinder the recognition of odor qualities, regulates stimulus selectivity, and transduces the underlying mechanics from a robust but costly rate-coding scheme on a slow respiratory (theta-band) timescale to a sparse dynamical representation operating on the beta- and gamma-band timescales and suitable for integration with other central neural processes.

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Publisher: Cambridge University Press
Print publication year: 2008

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References

Alonso, M., Viollet, C., Gabellec, M. M., et al. (2006). Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J Neurosci 26:10 508–10 513.CrossRefGoogle ScholarPubMed
Araneda, R. C., Peterlin, Z., Zhang, X., Chesler, A., and Firestein, S. (2004). A pharmacological profile of the aldehyde receptor repertoire in rat olfactory epithelium. J Physiol 555:743–756.CrossRefGoogle ScholarPubMed
Attwell, D. and Laughlin, S. B. (2001). An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145.CrossRefGoogle Scholar
Aungst, J. L., Heyward, P. M., Puche, A. C., et al. (2003). Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629.CrossRefGoogle ScholarPubMed
Barkai, E., Bergman, R. E., Horwitz, G., and Hasselmo, M. E. (1994). Modulation of associative memory function in a biophysical simulation of rat piriform cortex. J Neurophysiol 72:659–677.CrossRefGoogle Scholar
Bathellier, B., Lagier, S., Faure, P., and Lledo, P. M. (2006). Circuit properties generating gamma oscillations in a network model of the olfactory bulb. J Neurophysiol 95:2678–2691.CrossRefGoogle Scholar
Brennan, P., Kaba, H., and Keverne, E. B. (1990). Olfactory recognition: a simple memory system. Science 250:1223–1226.CrossRefGoogle ScholarPubMed
Bressler, S. L., Coppola, R., and Nakamura, R. (1993). Episodic multiregional cortical coherence at multiple frequencies during visual task performance. Nature 366:153–156.CrossRefGoogle ScholarPubMed
Buck, L. and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187.CrossRefGoogle ScholarPubMed
Buonviso, N. and Chaput, M. (2000). Olfactory experience decreases responsiveness of the olfactory bulb in the adult rat. Neuroscience 95:325–332.CrossRefGoogle ScholarPubMed
Buonviso, N., Gervais, R., Chalansonnet, M., and Chaput, M. (1998). Short-lasting exposure to one odour decreases general reactivity in the olfactory bulb of adult rats. Eur J Neurosci 10:2472–2475.CrossRefGoogle ScholarPubMed
Buonviso, N., Amat, C., and Litaudon, P. (2006). Respiratory modulation of olfactory neurons in the rodent brain. Chem Senses 31:145–154.CrossRefGoogle ScholarPubMed
Chalansonnet, M. and Chaput, M. A. (1998). Olfactory bulb output cell temporal response patterns to increasing odor concentrations in freely breathing rats. Chem Senses 23:1–9.CrossRefGoogle ScholarPubMed
Chen, W. R., Xiong, W., and Shepherd, G. M. (2000). Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron 25:625–633.CrossRefGoogle ScholarPubMed
Chess, A., Simon, I., Cedar, H., and Axel, R. (1994). Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823–834.CrossRefGoogle ScholarPubMed
Cleland, T. A. and Linster, C. (1999). Concentration tuning mediated by spare receptor capacity in olfactory sensory neurons: a theoretical study. Neur Comput 11:1673–1690.CrossRefGoogle ScholarPubMed
Cleland, T. A. and Linster, C. (2002). How synchronization properties among second-order sensory neurons can mediate stimulus salience. Behav Neurosci 116:212–221.CrossRefGoogle ScholarPubMed
Cleland, T. A. and Linster, C. (2003). Central olfactory processing. In: Handbook of Olfaction and Gustation, 2nd edn, ed. Doty, , R. L., pp. 165–180. New York: Marcel Dekker.Google Scholar
Cleland, T. A. and Linster, C. (2005). Computation in the olfactory system. Chem Senses 30:801–813.CrossRefGoogle ScholarPubMed
Cleland, T. A. and Sethupathy, P. (2006). Non-topographical contrast enhancement in the olfactory bulb. BMC Neurosci 7:7.CrossRefGoogle ScholarPubMed
Cleland, T. A., Johnson, B. A., Leon, M., and Linster, C. (2007). Relational representation in the olfactory system. Proc Natl Acad Sci USA 104:1953–1958.CrossRefGoogle ScholarPubMed
David, F., Linster, C. and Cleland, T. A. (2008). Lateral dendritic shunt inhibition can regularize mitral cell spike patterning. J Comput Neurosci PMID:18060489.
Debarbieux, F., Audinat, E., and Charpak, S. (2003). Action potential propagation in dendrites of rat mitral cells in vivo. J Neurosci 23:5553–5560.CrossRefGoogle ScholarPubMed
Desmaisons, D., Vincent, J. D., and Lledo, P. M. (1999). Control of action potential timing by intrinsic subthreshold oscillations in olfactory bulb output neurons. J Neurosci 19:10 727–10 737.CrossRefGoogle ScholarPubMed
Duchamp-Viret, P., Duchamp, A., and Vigouroux, M. (1989). Amplifying role of convergence in olfactory system a comparative study of receptor cell and second-order neuron sensitivities. J Neurophysiol 61:1085–1094.CrossRefGoogle ScholarPubMed
Eeckman, F. H. and Freeman, W. J. (1990). Correlations between unit firing and EEG in the rat olfactory system. Brain Res 528:238–244.CrossRefGoogle ScholarPubMed
Egger, V., Svoboda, K., and Mainen, Z. F. (2003). Mechanisms of lateral inhibition in the olfactory bulb: efficiency and modulation of spike-evoked calcium influx into granule cells. J Neurosci 23:7551–7558.CrossRefGoogle ScholarPubMed
Egger, V., Svoboda, K., and Mainen, Z. F. (2005). Dendrodendritic synaptic signals in olfactory bulb granule cells: local spine boost and global low-threshold spike. J Neurosci 25:3521–3530.CrossRefGoogle ScholarPubMed
Fletcher, M. L. and Wilson, D. A. (2002). Experience modifies olfactory acuity: acetylcholine-dependent learning decreases behavioral generalization between similar odorants. J Neurosci 22:RC201.CrossRefGoogle ScholarPubMed
Fletcher, M. L. and Wilson, D. A. (2003). Olfactory bulb mitral-tufted cell plasticity: odorant-specific tuning reflects previous odorant exposure. J Neurosci 23:6946–6955.CrossRefGoogle ScholarPubMed
Garcia, Y., Ibarra, C., and Jaffe, E. H. (1995). NMDA and non-NMDA receptor-mediated release of [3H]GABA from granule cell dendrites of rat olfactory bulb. J Neurochem 64:662–669.CrossRefGoogle Scholar
Getchell, T. V. (1986). Functional properties of vertebrate olfactory receptor neurons. Physiol Rev 66:772–818.CrossRefGoogle ScholarPubMed
Getchell, T. V. and Shepherd, G. M. (1978). Responses of olfactory receptor cells to step pulses of odour at different concentrations in the salamander. J Physiol 282:521–540.CrossRefGoogle ScholarPubMed
Goldman, A. L., Goes van Naters, W., Lessing, D., Warr, C. G., and Carlson, J. R. (2005). Coexpression of two functional odor receptors in one neuron. Neuron 45:661–666.CrossRefGoogle ScholarPubMed
Haberly, L. B. (2001). Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26:551–576.CrossRefGoogle ScholarPubMed
Haberly, L. B. and Bower, J. M. (1989). Olfactory cortex: model circuit for study of associative memory?Trends Neurosci 12:258–264.CrossRefGoogle ScholarPubMed
Hamilton, K. A. and Kauer, J. S. (1989). Patterns of intracellular potentials in salamander mitral/tufted cells in response to odor stimulation. J Neurophysiol 62:609–625.CrossRefGoogle ScholarPubMed
Hopfield, J. J. (1995). Pattern recognition computation using action potential timing for stimulus representation. Nature 376:33–36.CrossRefGoogle ScholarPubMed
Illig, K. R. and Haberly, L. B. (2003). Odor-evoked activity is spatially distributed in piriform cortex. J Comp Neurol 457:361–373.CrossRefGoogle ScholarPubMed
Ishii, T., Serizawa, S., Kohda, A., et al. (2001). Monoallelic expression of the odourant receptor gene and axonal projection of olfactory sensory neurones. Genes Cells 6:71–78.CrossRefGoogle ScholarPubMed
Kadohisa, M. and Wilson, D. A. (2006). Olfactory cortical adaptation facilitates detection of odors against background. J Neurophysiol 95:1888–1896.CrossRefGoogle ScholarPubMed
Kashiwadani, H., Sasaki, Y. F., Uchida, N., and Mori, K. (1999). Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J Neurophysiol 82:1786–1792.CrossRefGoogle ScholarPubMed
Kauer, J. S., Hamilton, K. A., Neff, S. R., and Cinelli, A. R. (1990). Temporal patterns of membrane potential in the olfactory bulb observed with intracellular recording and voltage-sensitive dye imaging: early hyperpolarization. In: Chemosensory Information Processing, ed. Schild, D., pp. 305–314. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Kaur, R., Zhu, X. O., Moorhouse, A. J., and Barry, P. H. (2001). IP3-gated channels and their occurrence relative to CNG channels in the soma and dendritic knob of rat olfactory receptor neurons. J Membr Biol 181:91–105.CrossRefGoogle ScholarPubMed
Kay, L. M. (2003). Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J Integr Neurosci 2:31–44.CrossRefGoogle ScholarPubMed
Kay, L. M. and Freeman, W. J. (1998). Bidirectional processing in the olfactory–limbic axis during olfactory behavior. Behav Neurosci 112:541–553.CrossRefGoogle ScholarPubMed
Kay, L. M. and Laurent, G. (1999). Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2:1003–1009.CrossRefGoogle ScholarPubMed
Koch, C., Poggio, T., and Torre, V. (1983). Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci USA 80:2799–2802.CrossRefGoogle Scholar
Kohonen, T. (1982). Self-organized formation of topology correct feature maps. Biol Cybernet 43:59–69.CrossRefGoogle Scholar
Kohonen, T. and Hari, R. (1999). Where the abstract feature maps of the brain might come from. Trends Neurosci 22:135–139.CrossRefGoogle Scholar
Lagier, S., Carleton, A., and Lledo, P. M. (2004). Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J Neurosci 24:4382–4392.CrossRefGoogle ScholarPubMed
Lei, H., Mooney, R., and Katz, L. C. (2006). Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J Neurosci 26:12 023–12 032.CrossRefGoogle ScholarPubMed
Li, Z. and Hopfield, J. J. (1989). Modeling the olfactory bulb and its neural oscillatory processings. Biol Cybernet 61:379–392.CrossRefGoogle ScholarPubMed
Lincoln, J., Coopersmith, R., Harris, E. W., Cotman, C. W., and Leon, M. (1988). NMDA receptor activation and early olfactory learning. Brain Res 467:309–312.CrossRefGoogle ScholarPubMed
Linster, C. and Cleland, T. A. (2001). How spike synchronization among olfactory neurons can contribute to sensory discrimination. J Comput Neurosci 10:187–193.CrossRefGoogle ScholarPubMed
Linster, C. and Cleland, T. A. (2002). Cholinergic modulation of sensory representations in the olfactory bulb. Neur Networks 15:709–717.CrossRefGoogle ScholarPubMed
Linster, C. and Gervais, R. (1996). Investigation of the role of interneurons and their modulation by centrifugal fibers in a neural model of the olfactory bulb. J Comput Neurosci 3:225–246.CrossRefGoogle Scholar
Linster, C., Henry, L., Kadohisa, M., and Wilson, D. A. (2007). Synaptic adaptation and odor-background segmentation. Neurobiol Learn Mem 87:352–360.CrossRefGoogle ScholarPubMed
Liu, G. (2004). Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 7:373–379.CrossRefGoogle ScholarPubMed
Lledo, P. M. and Lagier, S. (2006). Adjusting neurophysiological computations in the adult olfactory bulb. Semin Cell Dev Biol 17:443–453.CrossRefGoogle ScholarPubMed
Lledo, P. M., Alonso, M., and Grubb, M. S. (2006). Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193.CrossRefGoogle ScholarPubMed
Lowe, G. (2002). Inhibition of backpropagating action potentials in mitral cell secondary dendrites. J Neurophysiol 88:64–85.CrossRefGoogle ScholarPubMed
Mandairon, N., Jourdan, F., and Didier, A. (2003). Deprivation of sensory inputs to the olfactory bulb up-regulates cell death and proliferation in the subventricular zone of adult mice. Neuroscience 119:507–516.CrossRefGoogle ScholarPubMed
Mandairon, N., Sacquet, J., Jourdan, F., and Didier, A. (2006a). Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience 141:443–451.CrossRefGoogle ScholarPubMed
Mandairon, N., Ferretti, C. J., Stack, C. M., et al. (2006b). Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. Eur J Neurosci 24:3234–3244.CrossRefGoogle ScholarPubMed
Martin, C., Gervais, R., Hugues, E., Messaoudi, B., and Ravel, N. (2004). Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition?J Neurosci 24:389–397.CrossRefGoogle ScholarPubMed
Martin, C., Gervais, R., Messaoudi, B., and Ravel, N. (2006). Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur J Neurosci 23:1801–1810.CrossRefGoogle ScholarPubMed
McQuiston, A. R. and Katz, L. C. (2001). Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86:1899–1907.CrossRefGoogle ScholarPubMed
Mel, B. W. and Schiller, J. (2004). On the fight between excitation and inhibition: location is everything. Sci STKE 2004:PE44.Google ScholarPubMed
Meyer, M. R., Angele, A., Kremmer, E., Kaupp, U. B., and Muller, F. (2000). A cGMP-signaling pathway in a subset of olfactory sensory neurons. Proc Natl Acad Sci USA 97:10 595–10 600.CrossRefGoogle Scholar
Mombaerts, P. (1999). Seven-transmembrane proteins as odorant and chemosensory receptors. Science 286:707–711.CrossRefGoogle ScholarPubMed
Mombaerts, P. (2001). The human repertoire of odorant receptor genes and pseudogenes. Annu Rev Genomics Hum Genet 2:493–510.CrossRefGoogle ScholarPubMed
Mombaerts, P. (2004). Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 14:31–36.CrossRefGoogle ScholarPubMed
Mori, K. and Shepherd, G. M. (1994). Emerging principles of molecular signal processing by mitral/tufted cells in the olfactory bulb. Semin Cell Biol 5:65–74.CrossRefGoogle ScholarPubMed
Morrison, E. E. and Costanzo, R. M. (1990). Morphology of the human olfactory epithelium. J Comp Neurol 297:1–13.CrossRefGoogle ScholarPubMed
Morrison, E. E. and Costanzo, R. M. (1992). Morphology of olfactory epithelium in humans and other vertebrates. Microsc Res Tech 23:49–61.CrossRefGoogle ScholarPubMed
Mouly, A. M., Gervais, R., and Holley, A. (1990). Evidence for the involvement of rat olfactory bulb in processes supporting long-term olfactory memory. Eur J Neurosci 2:978–984.CrossRefGoogle ScholarPubMed
Mouly, A. M., Kindermann, U., Gervais, R., and Holley, A. (1993). Involvement of the olfactory bulb in consolidation processes associated with long-term memory in rats. Behav Neurosci 107:451–457.CrossRefGoogle ScholarPubMed
Nusser, Z., Kay, L. M., Laurent, G., Homanics, G. E., and Mody, I. (2001). Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86:2823–2833.CrossRefGoogle ScholarPubMed
Oka, Y., Omura, M., Kataoka, H., and Touhara, K. (2004). Olfactory receptor antagonism between odorants. EMBO J 23:120–126.CrossRefGoogle ScholarPubMed
Pinching, A. J. and Powell, T. P. (1971). The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347–377.Google ScholarPubMed
Pressler, R. T. and Strowbridge, B. W. (2006). Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49:889–904.CrossRefGoogle ScholarPubMed
Ravel, N., Chabaud, P., Martin, C., et al. (2003). Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60–90 Hz) and beta (15–40 Hz) bands in the rat olfactory bulb. Eur J Neurosci 17:350–358.CrossRefGoogle ScholarPubMed
Restrepo, D., Miyamoto, T., Bryant, B. P., and Teeter, J. H. (1990). Odor stimuli trigger influx of calcium into olfactory neurons of the channel catfish. Science 249:1166–1168.CrossRefGoogle ScholarPubMed
Rochefort, C., Gheusi, G., Vincent, J. D., and Lledo, P. M. (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci 22:2679–2689.CrossRefGoogle ScholarPubMed
Roskies, A. L. (1999). The binding problem. Neuron 24:7–9.CrossRefGoogle ScholarPubMed
Rospars, J. P., Lansky, P., Duchamp-Viret, P., and Duchamp, A. (2000). Spiking frequency versus odorant concentration in olfactory receptor neurons. Biosystems 58:133–141.CrossRefGoogle ScholarPubMed
Roux, S. G., Garcia, S., Bertrand, B., et al. (2006). Respiratory cycle as time basis: an improved method for averaging olfactory neural events. J Neurosci Methods 152:173–178.CrossRefGoogle ScholarPubMed
Rubin, D. B. and Cleland, T. A. (2006). Dynamical mechanisms of odor processing in olfactory bulb mitral cells. J Neurophysiol 96:555–568.CrossRefGoogle ScholarPubMed
Schoenfeld, T. A. and Cleland, T. A. (2005). The anatomical logic of smell. Trends Neurosci 28:620–627.CrossRefGoogle ScholarPubMed
Schoenfeld, T. A. and Cleland, T. A. (2006). Anatomical contributions to odorant sampling and representation in rodents: zoning in on sniffing behavior. Chem Senses 31:131–144.CrossRefGoogle ScholarPubMed
Schoppa, N. E. (2006a). Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49:271–283.CrossRefGoogle ScholarPubMed
Schoppa, N. E. (2006b). A novel local circuit in the olfactory bulb involving an old short-axon cell. Neuron 49:783–784.CrossRefGoogle ScholarPubMed
Schoppa, N. E., Kinzie, J. M., Sahara, Y., Segerson, T. P., and Westbrook, G. L. (1998). Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18:6790–6802.CrossRefGoogle ScholarPubMed
Serizawa, S., Ishii, T., Nakatani, H., et al. (2000). Mutually exclusive expression of odorant receptor transgenes. Nat Neurosci 3:687–693.CrossRefGoogle ScholarPubMed
Song, S., Miller, K. D., and Abbott, L. F. (2000). Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3:919–926.CrossRefGoogle ScholarPubMed
Spors, H., Wachowiak, M., Cohen, L. B., and Friedrich, R. W. (2006). Temporal dynamics and latency patterns of receptor neuron input to the olfactory bulb. J Neurosci 26:1247–1259.CrossRefGoogle ScholarPubMed
Stopfer, M., Bhagavan, S., Smith, B. H., and Laurent, G. (1997). Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74.Google ScholarPubMed
Stopfer, M., Jayaraman, V., and Laurent, G. (2003). Intensity versus identity coding in an olfactory system. Neuron 39:991–1004.CrossRefGoogle Scholar
Strotmann, J., Conzelmann, S., Beck, A., et al. (2000). Local permutations in the glomerular array of the mouse olfactory bulb. J Neurosci 20:6927–6938.CrossRefGoogle ScholarPubMed
Tozaki, H., Tanaka, S., and Hirata, T. (2004). Theoretical consideration of olfactory axon projection with an activity-dependent neural network model. Mol Cell Neurosci 26:503–517.CrossRefGoogle ScholarPubMed
Treisman, A. (1999). Solutions to the binding problem: progress through controversy and convergence. Neuron 24:105–110.CrossRefGoogle ScholarPubMed
Troemel, E. R., Chou, J. H., Dwyer, N. D., Colbert, H. A. and Bargmann, C. I. (1995). Divergent seven transmembrane receptors are candidate chemosensory receptors inC. elegans. Cell 83:207–218.CrossRefGoogle ScholarPubMed
Drongelen, W., Holley, A., and Doving, K. B. (1978). Convergence in the olfactory system: quantitative aspects of odour sensitivity. J Theor Biol 71:39–48.CrossRefGoogle ScholarPubMed
Wellis, D. P. and Scott, J. W. (1990). Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J Neurophysiol 64:932–947.CrossRefGoogle ScholarPubMed
White, J., Hamilton, K. A., Neff, S. R., and Kauer, J. S. (1992). Emergent properties of odor information coding in a representational model of the salamander olfactory bulb. J Neurosci 12:1772–1780.CrossRefGoogle Scholar
Willhite, D. C., Nguyen, K. T., Masurkar, A. V., et al. (2006). Viral tracing identifies distributed columnar organization in the olfactory bulb. Proc Natl Acad Sci USA 103:12 592–12 597.CrossRefGoogle ScholarPubMed
Wilson, D. A. and Leon, M. (1988). Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. J Neurophysiol 59:1770–1782.CrossRefGoogle ScholarPubMed
Wilson, D. A. and Stevenson, R. J. (2006). Learning to Smell: Olfactory Perception from Neurobiology to Behavior. Baltimore, MD: Johns Hopkins University Press.Google Scholar
Xiong, W. and Chen, W. R. (2002). Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron 34:115–126.CrossRefGoogle ScholarPubMed
Yokoi, M., Mori, K., and Nakanishi, S. (1995). Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92:3371–3375.CrossRefGoogle ScholarPubMed
Yuan, Q., Harley, C. W., and McLean, J. H. (2003). Mitral cell beta1 and 5-HT2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. Learn Mem 10:5–15.CrossRefGoogle ScholarPubMed
Zaborszky, L., Carlsen, J., Brashear, H. R., and Heimer, L. (1986). Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J Comp Neurol 243:488–509.CrossRefGoogle ScholarPubMed
Zufall, F. and Leinders-Zufall, T. (2000). The cellular and molecular basis of odor adaptation. Chem Senses 25:473–481.CrossRefGoogle ScholarPubMed

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