Abstract
The mammalian olfactory system shows many types of sensory and perceptual processing accompanied by oscillations at the level of the local field potential, and much is already known about the cellular and synaptic origins of these markers of coherent population activity. Complex, but chemotopic input patterns describe the qualitative similarity of odors, but animals can discriminate even very similar odorants. Coherent population activity signified by oscillations may assist the animals in discrimination of closely related odors. Manipulations to olfactory bulb centrifugal input and GABAergic circuitry can alter the degree of gamma (40-100 Hz) oscillatory coupling within the olfactory bulb, affecting animals’ ability to discriminate highly overlapping odors. The demands of an odor discrimination can also enhance gamma oscillations, but this may depend on the cognitive demands of the task, with some tasks spreading the processing over many brain regions, accompanied by beta (15-30 Hz) instead of gamma oscillations.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsPreview
Unable to display preview. Download preview PDF.
References
Abraham, N.M., Spors, H., Carleton, A., Margrie, T.W., Kuner, T., Schaefer, A.T.: Maintaining accuracy at the expense of speed: Stimulus similarity defines odor discrimination time in mice. Neuron 44, 865–876 (2004)
Adrian, E.D.: The electrical activity of the mammalian olfactory bulb. Electroencephalography and Clinical Neurophysiology 2, 377–388 (1950)
Adrian, E.D.: Olfactory reactions in the brain of the hedgehog. Journal of Physiology 100, 459–473 (1942)
Araneda, R.C., Kini, A.D., Firestein, S.: The molecular receptive range of an odorant receptor. Nature Neuroscience 3, 1248–1255 (2000)
Aroniadou-Anderjaska, V., Ennis, M., Shipley, M.T.: Current-source density analysis in the rat olfactory bulb: laminar distribution of kainate/AMPA- and NMDA-receptor-mediated currents. Journal of Neurophysiology 81, 15–28 (1999)
Bernasconi, C., Konig, P.: On the directionality of cortical interactions studied by structural analysis of electrophysiological recordings. Biological Cybernetics 81, 199–210 (1999)
Beshel, J., Kopell, N., Kay, L.M.: Olfactory bulb gamma oscillations are enhanced with task demands. Journal of Neuroscience 27, 8358–8365 (2007)
Bhalla, U.S., Bower, J.M.: Multiday recordings from olfactory bulb neurons in awake freely moving rats: spatially and temporally organized variability in odorant response properties. Journal of Computational Neuroscience 4, 221–256 (1997)
Biella, G., De Curtis, M.: Olfactory inputs activate the medial entorhinal cortex via the hippocampus. Journal of Neurophysiology 83, 1924–1931 (2000)
Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., Buzsaki, G.: Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. Journal of Neuroscience 15, 47–60 (1995)
Braver, T.S., Barch, D.M., Gray, J.R., Molfese, D.L., Snyder, A.: Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. Cerebral Cortex 11, 825–836 (2001)
Brovelli, A., Ding, M.Z., Ledberg, A., Chen, Y.H., Nakamura, R., Bressler, S.L.: Beta oscillations in a large-scale sensorimotor cortical network: Directional influences revealed by Granger causality. Proc. Natl. Acad. 101, 9849–9854 (2004)
Brunig, I., Sommer, M., Hatt, H., Bormann, J.: Dopamine receptor subtypes modulate olfactory bulb gamma-aminobutyric acid type A receptors. Proc. Natl. Acad. Sci. 96, 2456–2460 (1999)
Buck, L., Axel, R.: A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175–187 (1991)
Buonviso, N., Amat, C., Litaudon, P., Roux, S., Royet, J.P., Farget, V., Sicard, G.: Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. European Journal of Neuroscience 17, 1811–1819 (2003)
Chabaud, P., Ravel, N., Wilson, D.A., Gervais, R.: Functional coupling in rat central olfactory pathways: a coherence analysis. Neuroscience Letters 276, 17–20 (1999)
Cleland, T.A., Morse, A., Yue, E.L., Linster, C.: Behavioral models of odor similarity. Behavioral Neuroscience 116, 222–231 (2002)
Davila, N.G., Blakemore, L.J., Trombley, P.Q.: Dopamine modulates synaptic transmission between rat olfactory bulb neurons in culture. Journal of Neurophysiology 90, 395–404 (2003)
Diprisco, G.V., Freeman, W.J.: Odor-related bulbar EEG spatial pattern-analysis during appetitive conditioning in rabbits. Behavioral Neuroscience 99, 964–978 (1985)
Eeckman, F.H., Freeman, W.J.: Correlations between unit firing and EEG in the rat olfactory system. Brain Research 528, 238–244 (1990)
Ferreyra Moyano, H., Cinelli, A.R., Molina, J.C.: Current generators and properties of early components evoked in rat olfactory cortex. Brain Research Bulletin 15, 237–248 (1985)
Fletcher, M.L., Wilson, D.A.: Olfactory bulb mitral-tufted cell plasticity: Odorant-specific tuning reflects previous odorant exposure. Journal of Neuroscience 23, 6946–6955 (2003)
Fontanini, A., Bower, J.M.: Variable coupling between olfactory system activity and respiration in ketamine/xylazine anesthetized rats. Journal of Neurophysiology 93, 3573–3581 (2005)
Freeman, W.J.: Distribution in time and space of prepyriform electrical activity. Journal of Neurophysiology 22, 644–665 (1959)
Freeman, W.J.: Linear distributed feedback model for prepyriform cortex. Experimental Neurology 10, 525–547 (1964)
Freeman, W.J.: Mass Action in the Nervous System, p. 489. Academic Press, New York (1975)
Freeman, W.J.: Relations between unit activity and evoked potentials in prepyriform cortex of cats. Journal of Neurophysiology 31, 337–348 (1968)
Freeman, W.J., Schneider, W.: Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19, 44–56 (1982)
Gilad, Y., Wiebel, V., Przeworski, M., Lancet, D., Paabo, S.: Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. Plos. Biology 2, 120–125 (2004)
Giocomo, L.M., Hasselmo, M.E.: Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Molecular Neurobiology 36, 184–200 (2007)
Glusman, G., Yanai, I., Rubin, I., Lancet, D.: The complete human olfactory subgenome. Genome Research 11, 685–702 (2001)
Gray, C.M., Skinner, J.E.: Centrifugal regulation of neuronal activity in the olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Experimental Brain Research 69, 378–386 (1988)
Grossman, K.J., Mallik, A.K., Ross, J., Kay, L.M., Issa, N.P.: Glomerular activation patterns and the perception of odor mixtures. European Journal of Neuroscience 27(10), 2676–2685 (2008)
Gulyas, A.I., Toth, K., McBain, C.J., Freund, T.F.: Stratum radiatum giant cells: a type of principal cell in the rat hippocampus. European Journal of Neuroscience 10, 3813–3822 (1998)
Heale, V.R., Vanderwolf, C.H., Kavaliers, M.: Components of weasel and fox odors elicit fast wave bursts in the dentate gyrus of rats. Behavioural Brain Research 63, 159–165 (1994)
Homanics, G.E., DeLorey, T.M., Firestone, L.L., Quinlan, J.J., Handforth, A., Harrison, N.L., Krasowski, M.D., Rick, C.E., Korpi, E.R., Makela, R., Brilliant, M.H., Hagiwara, N., Ferguson, C., Snyder, K., Olsen, R.W.: Mice devoid of gamma-aminobutyrate type A receptor beta3 subunit have epilepsy, cleft palate, and hypersensitive behavior. Proc. Natl. Acad. Sci. 94, 4143–4148 (1997)
Imamura, K., Mataga, N., Mori, K.: Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. Journal of Neurophysiology 68, 1986–2002 (1992)
Insausti, R., Herrero, M.T., Witter, M.P.: Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7, 146–183 (1997)
Johnson, B.A., Farahbod, H., Xu, Z., Saber, S., Leon, M.: Local and global chemotopic organization: General features of the glomerular representations of aliphatic odorants differing in carbon number. Journal of Comparative Neurology 480, 234–249 (2004)
Kandel, A., Buzsaki, G.: Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat. Journal of Neuroscience 17, 6783–6797 (1997)
Katoh, K., Koshimoto, H., Tani, A., Mori, K.: Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. Journal of Neurophysiology 70, 2161–2175 (1993)
Kay, L.M.: Theta oscillations and sensorimotor performance. Proceedings of the National Academy of Sciences 102, 3863–3868 (2005)
Kay, L.M.: Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. Journal of Integrative Neuroscience 2, 31–44 (2003)
Kay, L. M., Beshel, J., Martin, C.: When good enough is best. Neuron 51, 277–278 (2006)
Kay, L.M., Crk, T., Thorngate, J.: A redefinition of odor mixture quality. Behavioral Neuroscience 119, 726–733 (2005)
Kay, L.M., Freeman, W.J.: Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behavioral Neuroscience 112, 541–553 (1998)
Kay, L.M., Laurent, G.: Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nature Neuroscience 2, 1003–1009 (1999)
Kay, L.M., Sherman, S.M.: An argument for an olfactory thalamus. Trends in Neurosciences 30, 47–53 (2007)
Kay, L.M., Stopfer, M.: Information processing in the olfactory systems of insects and vertebrates. Seminars in Cell & Developmental Biology 17, 433–442 (2006)
Lagier, S., Carleton, A., Lledo, P.M.: Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. Journal of Neuroscience 24, 4382–4392 (2004)
Laurent, G., Wehr, M., MacLeod, K., Stopfer, M., Leitch, B., Davidowitz, H.: Dynamic encoding of odors with oscillating neuronal assemblies in the locust brain. Biological Bulletin 191, 70–75 (1996)
Leon, M., Johnson, B.A.: Olfactory coding in the mammalian olfactory bulb. Brain Research Reviews 42, 23–32 (2003)
Levy, F., Meurisse, M., Ferreira, G., Thibault, J., Tillet, Y.: Afferents to the rostral olfactory bulb in sheep with special emphasis on the cholinergic, noradrenergic and serotonergic connections. Journal of Chemical Neuroanatomy 16, 245–263 (1999)
Liljenstrom, H., Hasselmo, M.E.: Cholinergic modulation of cortical oscillatory dynamics. Journal of Neurophysiology 74, 288–297 (1995)
Linster, C., Johnson, B.A., Yue, E., Morse, A., Xu, Z., Hingco, E.E., Choi, Y., Choi, M., Messiha, A., Leon, M.: Perceptual correlates of neural representations evoked by odorant enantiomers. Journal of Neuroscience 21, 9837–9843 (2001)
Lowry, C.A., Kay, L.M.: Chemical factors determine olfactory system beta oscillations in waking rats. Journal of Neurophysiology 98, 394–404 (2007)
MacLeod, K., Backer, A., Laurent, G.: Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395, 693–698 (1998)
MacLeod, K., Laurent, G.: Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274, 976–979 (1996)
Martin, C., Beshel, J., Kay, L.M.: An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. Journal of Neurophysiology 98, 2196–2205 (2007)
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. Journal of Physiology-Paris 98, 467–478 (2004a)
Martin, C., Gervais, R., Hugues, E., Messaoudi, B., Ravel, N.: Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: A correlate of odor recognition? Journal of Neuroscience 24, 389–397 (2004b)
Martin, C., Gervais, R., Messaoudi, B., Ravel, N.: Learning-induced oscillatory activities correlated to odour recognition: a network activity. European Journal of Neuroscience 23, 1801–1810 (2006)
Martinez, D.P., Freeman, W.J.: Periglomerular cell action on mitral cells in olfactory bulb shown by current source density analysis. Brain Research 308, 223–233 (1984)
McNamara, A.M., Magidson, P.D., Linster, C.: Binary mixture perception is affected by concentration of odor components. Behavioral Neuroscience 121, 1132–1136 (2007)
Mitzdorf, U.: Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiological Reviews 65, 37–100 (1985)
Mombaerts, P., Wang, F., Dulac, C., Chao, S.K., Nemes, A., Mendelsohn, M., Edmondson, J., Axel, R.: Visualizing an olfactory sensory map. Cell 87, 675–686 (1996)
Motokizawa, F.: Odor representation and discrimination in mitral/tufted cells of the rat olfactory bulb. Experimental Brain Research 112, 24–34 (1996)
Neville, K.R., Haberly, L.B.: Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. Journal of Neurophysiology 90, 3921–3930 (2003)
Nusser, Z., Kay, L.M., Laurent, G., Homanics, G.E., Mody, I.: Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. Journal of Neurophysiology 86, 2823–2833 (2001)
Pager, J.: Respiration and olfactory bulb unit activity in the unrestrained rat: statements and reappraisals. Behavioural Brain Research 16, 81–94 (1985)
Pager, J.: Unit responses changing with behavioral outcome in the olfactory bulb of unrestrained rats. Brain Research 289, 87–98 (1983)
Rall, W., Shepherd, G.M.: Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. Journal of Neurophysiology 31, 884–915 (1968)
Rinberg, D., Koulakov, A., Gelperin, A.: Sparse odor coding in awake behaving mice. Journal of Neuroscience 26, 8857–8865 (2006a)
Rinberg, D., Koulakov, A., Gelperin, A.: Speed-accuracy tradeoff in olfaction. Neuron 51, 351–358 (2006b)
Rodriguez, R., Kallenbach, U., Singer, W., Munk, M.H.J.: Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. Journal of Neuroscience 24, 10369–10378 (2004)
Rubin, B.D., Katz, L.C.: Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23, 499–511 (1999)
Schoenfeld, T.A., Cleland, T.A.: The anatomical logic of smell. Trends in Neurosciences 28, 620–627 (2005)
Schoppa, N.E.: AMPA/Kainate receptors drive rapid output and precise synchrony in olfactory bulb granule cells. Journal of Neuroscience 26, 12996–13006 (2006a)
Schoppa, N.E.: Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49, 271–283 (2006b)
Seth, A.K.: Causal connectivity of evolved neural networks during behavior. Network-Computation in Neural Systems 16, 35–54 (2005)
Shepherd, G.M., Greer, C.A.: Olfactory bulb. In: Shepherd, G. (ed.) The Synaptic Organization of the Brain, p. 719. Oxford University Press, New York (2003)
Shipley, M.T., Adamek, G.D.: The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Research Bulletin 12, 669–688 (1984)
Shipley, M.T., Ennis, M., Puche, A.: Olfactory System. In: Paxinos, G. (ed.) The Rat Nervous System. Academic Press, San Diego (2004)
Stopfer, M., Bhagavan, S., Smith, B.H., Laurent, G.: Impaired odour discrimination on desynchronization of odour- encoding neural assemblies. Nature 390, 70–74 (1997)
Uchida, N., Mainen, Z.F.: Speed and accuracy of olfactory discrimination in the rat. Nature Neuroscience 6, 1224–1229 (2003)
Uchida, N., Takahashi, Y.K., Tanifuji, M., Mori, K.: Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nature Neuroscience 3, 1035–1043 (2000)
van Groen, T., Wyss, J.M.: Extrinsic projections from area CA1 of the rat hippocampus: olfactory, cortical, subcortical, and bilateral hippocampal formation projections. Journal of Comparative Neurology 302, 515–528 (1990)
Xu, F., Liu, N., Kida, I., Rothman, D.L., Hyder, F., Shepherd, G.M.: Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb. Proc. Natl. Acad. Sci. 100, 11029–11034 (2003)
Zelcer, I., Cohen, H., Richter-Levin, G., Lebiosn, T., Grossberger, T., Barkai, E.: A cellular correlate of learning-induced metaplasticity in the hippocampus. Cerebral Cortex 16, 460–468 (2006)
Zhang, X., Firestein, S.: The olfactory receptor gene superfamily of the mouse. Nature Neuroscience 5, 124–133 (2002)
Zibrowski, E.M., Vanderwolf, C.H.: Oscillatory fast wave activity in the rat pyriform cortex: relations to olfaction and behavior. Brain Research 766, 39–49 (1997)
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Kay, L.M. (2008). Dynamical Architecture of the Mammalian Olfactory System. In: Marinaro, M., Scarpetta, S., Yamaguchi, Y. (eds) Dynamic Brain - from Neural Spikes to Behaviors. NN 2007. Lecture Notes in Computer Science, vol 5286. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88853-6_6
Download citation
DOI: https://doi.org/10.1007/978-3-540-88853-6_6
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-88852-9
Online ISBN: 978-3-540-88853-6
eBook Packages: Computer ScienceComputer Science (R0)