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Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system

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Abstract

Oscillatory phenomena have been a focus of dynamical systems research since the time of the classical studies on the pendulum by Galileo. Fast cortical oscillations also have a long and storied history in neurophysiology, and olfactory oscillations have led the way with a depth of explanation not present in the literature of most other cortical systems. From the earliest studies of odor-evoked oscillations by Adrian, many reports have focused on mechanisms and functional associations of these oscillations, in particular for the so-called gamma oscillations. As a result, much information is now available regarding the biophysical mechanisms that underlie the oscillations in the mammalian olfactory system. Recent studies have expanded on these and addressed functionality directly in mammals and in the analogous insect system. Sub-bands within the rodent gamma oscillatory band associated with specific behavioral and cognitive states have also been identified. All this makes oscillatory neuronal networks a unique interdisciplinary platform from which to study neurocognitive and dynamical phenomena in intact, freely behaving animals. We present here a summary of what has been learned about the functional role and mechanisms of gamma oscillations in the olfactory system as a guide for similar studies in other cortical systems.

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Notes

  1. The concept contains an analogy with the equations describing dynamic equilibrium states in chemical reactions (Glasstone 1940) and with the so called “Law of mass action” established in the nineteenth century by Waage and Gulberg (1986). A second source of inspiration is found in the work of the American psychologist Karl Lashley, who defended the idea that cerebral “masses,” and not single cells, were the crucial entities to understand brain organization (Lashley 1931). And finally, the concept conveyed the idea of the importance of studing the coherent activity of large collections of neurons (“neural masses”). (Source, Walter J. Freeman, personal communication).

References

  • Acheson D (1997) From calculus to chaos. An introduction to dynamics. Oxford University Press, Oxford

    Google Scholar 

  • Adrian ED (1942) Olfactory reactions in the brain of the hedgehog. J Physiol 100:459–473

    PubMed  CAS  Google Scholar 

  • Adrian ED (1950) The electrical activity of the mammalian olfactory bulb. Electroencephalogr Clin Neurophysiol 2:377–388

    Article  PubMed  CAS  Google Scholar 

  • Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623–629

    Article  PubMed  CAS  Google Scholar 

  • Basar E, Ozesmi C (1972) The hippocampal EEG-activity and a systems analytical interpretation of averaged evoked potentials of the brain. Kybernetik 12:45–54

    Article  PubMed  CAS  Google Scholar 

  • Bathellier B, Lagier S, Faure P, Lledo PM (2006) Circuit properties generating gamma oscillations in a network model of the olfactory bulb. J Neurophysiol 95:2678–2691

    Article  PubMed  Google Scholar 

  • Beshel J, Kopell N, Kay LM (2007) Olfactory bulb gamma oscillations are enhanced with task demands. J Neurosci 27:8358–8365

    Article  PubMed  CAS  Google Scholar 

  • Borgers C, Epstein S, Kopell NJ (2005) Background gamma rhythmicity and attention in cortical local circuits: a computational study. Proc Natl Acad Sci USA 102:7002–7007

    Article  PubMed  CAS  Google Scholar 

  • Bressler SL, Freeman WJ (1980) Frequency analysis of olfactory system EEG in cat, rabbit, and rat. Electroencephalogr Clin Neurophysiol 50:19–24

    Article  PubMed  CAS  Google Scholar 

  • Buonviso N, Amat C, Litaudon P, Roux S, Royet JP, Farget V, Sicard G (2003) Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur J Neurosci 17:1811–1819

    Article  PubMed  Google Scholar 

  • Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929

    Article  PubMed  CAS  Google Scholar 

  • Chabaud P, Ravel N, Wilson DA, Gervais R (1999) Functional coupling in rat central olfactory pathways: a coherence analysis. Neurosci Lett 276:17–20

    Article  PubMed  CAS  Google Scholar 

  • Chatrian GE, Bickford RG, Uihlein A (1960) Depth electrographic study of a fast rhythm evoked from the human calcarine region by steady illumination. Electroencephalogr Clin Neurophysiol 12:167–176

    Article  PubMed  CAS  Google Scholar 

  • Chess A, Simon I, Cedar H, Axel R (1994) Allelic inactivation regulates olfactory receptor gene expression. Cell 78:823–834

    Article  PubMed  CAS  Google Scholar 

  • Davison AP, Feng J, Brown D (2003) Dendrodendritic inhibition and simulated odor responses in a detailed olfactory bulb network model. J Neurophysiol 90:1921–1935

    Article  PubMed  CAS  Google Scholar 

  • Di Prisco GV, Freeman WJ (1985) Odor-related bulbar EEG spatial pattern analysis during appetitive conditioning in rabbits. Behav Neurosci 99:964–978

    Article  PubMed  CAS  Google Scholar 

  • Donoghue JP, Sanes JN, Hatsopoulos NG, Gaal G (1998) Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J Neurophysiol 79:159–173

    PubMed  CAS  Google Scholar 

  • Eeckman FH, Freeman WJ (1990) Correlations between unit firing and EEG in the rat olfactory system. Brain Res 528:238–244

    Article  PubMed  CAS  Google Scholar 

  • Elsaesser R, Paysan J (2007) The sense of smell, its signalling pathways, and the dichotomy of cilia and microvilli in olfactory sensory cells. BMC Neurosci 8(Suppl 3):S1

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ (1961) Harmonic oscillation as model for cortical excitability changes with attention in cats. Science 133:2058–2059

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ (1964) A linear distributed feedback model for prepyriform cortex. Exp Neurol 10:525–547

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ (1975) Mass action in the nervous system. Academic Press, New York

    Google Scholar 

  • Freeman WJ (1979) EEG analysis gives model of neuronal template-matching mechanism for sensory search with olfactory bulb. Biol Cybern 35:221–234

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ (1987) Simulation of chaotic EEG patterns with a dynamic model of the olfactory system. Biol Cybern 56:139–150

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ (1991) The physiology of perception. Sci Am 264:78–85

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ, Schneider W (1982) Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19:44–56

    Article  PubMed  CAS  Google Scholar 

  • Freeman WJ, Skarda CA (1985) Spatial EEG patterns, non-linear dynamics and perception: the neo-Sherringtonian view. Brain Res 357:147–175

    PubMed  CAS  Google Scholar 

  • Galilei G (1638) Two new sciences. The University of Wisconsin Press, 1974, Madison, WI, p 323

  • Glasstone S (1940) Textbook of physical chemistry. D. Van Nostrand Company, New York

    Google Scholar 

  • Gray CM, Konig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337

    Article  PubMed  CAS  Google Scholar 

  • Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M (2007) Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10:348–354

    Article  PubMed  CAS  Google Scholar 

  • Halasz N, Hokfelt T, Ljungdahl A, Johansson O, Goldstein M (1977) Dopamine neurons in the olfactory bulb. Adv Biochem Psychopharmacol 16:169–177

    PubMed  CAS  Google Scholar 

  • Hall B, Delaney K (2001) Cholinergic modulation of odor-evoked oscillations in the frog olfactory bulb. Biol Bull 201:276–277

    Article  PubMed  CAS  Google Scholar 

  • Hendin O, Horn D, Tsodyks MV (1998) Associative memory and segmentation in an oscillatory neural model of the olfactory bulb. J Comput Neurosci 5:157–169

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Peon R, Lavin A, Alcocer-Cuaron C, Marcelin JP (1960) Electrical activity of the olfactory bulb during wakefulness and sleep. Electroencephalogr Clin Neurophysiol 12:41–58

    Article  PubMed  CAS  Google Scholar 

  • Hsia AY, Vincent JD, Lledo PM (1999) Dopamine depresses synaptic inputs into the olfactory bulb. J Neurophysiol 82:1082–1085

    PubMed  CAS  Google Scholar 

  • Inagaki N, Yamatodani A, Ando-Yamamoto M, Tohyama M, Watanabe T, Wada H (1988) Organization of histaminergic fibers in the rat brain. J Comp Neurol 273:283–300

    Article  PubMed  CAS  Google Scholar 

  • Isaacson JS (1999) Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23:377–384

    Article  PubMed  CAS  Google Scholar 

  • Joliot M, Ribary U, Llinas R (1994) Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc Natl Acad Sci USA 91:11748–11751

    Article  PubMed  CAS  Google Scholar 

  • Kashiwadani H, Sasaki YF, Uchida N, 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

    PubMed  CAS  Google Scholar 

  • Kay LM (2003) Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J Integr Neurosci 2:31–44

    Article  PubMed  Google Scholar 

  • Kay LM, Freeman WJ (1998) Bidirectional processing in the olfactory-limbic axis during olfactory behavior. Behav Neurosci 112:541–553

    Article  PubMed  CAS  Google Scholar 

  • Kosaka K, Kosaka T (2005) Synaptic organization of the glomerulus in the main olfactory bulb: compartments of the glomerulus and heterogeneity of the periglomerular cells. Anat Sci Int 80:80–90

    Article  PubMed  Google Scholar 

  • Lashley K (1931) Mass action in cerebral function. Science 73:245–254

    Article  PubMed  Google Scholar 

  • Lavin A, Alcocer-Cuaron C, Hernandez-Peon R (1959) Centrifugal arousal in the olfactory bulb. Science 129:332–333

    Article  PubMed  CAS  Google Scholar 

  • Levy F, Meurisse M, Ferreira G, Thibault J, Tillet Y (1999) Afferents to the rostral olfactory bulb in sheep with special emphasis on the cholinergic, noradrenergic and serotonergic connections. J Chem Neuroanat 16:245–263

    Article  PubMed  CAS  Google Scholar 

  • Li Z (1990) A model of olfactory adaptation and sensitivity enhancement in the olfactory-bulb. Biol Cybern 62:349–361

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Hopfield JJ (1989) Modeling the olfactory bulb and its neural oscillatory processings. Biol Cybern 61:379–392

    Article  PubMed  CAS  Google Scholar 

  • Liljenstrom H, Hasselmo ME (1995) Cholinergic modulation of cortical oscillatory dynamics. J Neurophysiol 74:288–297

    PubMed  CAS  Google Scholar 

  • Linster C, 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

    Article  PubMed  CAS  Google Scholar 

  • Linster C, Wyble BP, Hasselmo ME (1999) Electrical stimulation of the horizontal limb of the diagonal band of broca modulates population EPSPs in piriform cortex. J Neurophysiol 81:2737–2742

    PubMed  CAS  Google Scholar 

  • MacLeod K, Backer A, Laurent G (1998) Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395:693–698

    Article  PubMed  CAS  Google Scholar 

  • Malnic B, Hirono J, Sato T, Buck LB (1999) Combinatorial receptor codes for odors. Cell 96:713–723

    Article  PubMed  CAS  Google Scholar 

  • Martinez DP, Freeman WJ (1984) Periglomerular cell action on mitral cells in olfactory bulb shown by current source density analysis. Brain Res 308:223–233

    Article  PubMed  CAS  Google Scholar 

  • McCulloch W, Pitts W (1943) A logical calculus of the ideas immanent in nervous activity. Bull Math Biophys 7:115–133

    Article  Google Scholar 

  • Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65:37–100

    PubMed  CAS  Google Scholar 

  • Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R (1996) Visualizing an olfactory sensory map. Cell 87:675–686

    Article  PubMed  CAS  Google Scholar 

  • Neville KR, Haberly LB (2003) Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90:3921–3930

    Article  PubMed  Google Scholar 

  • Nicolis G, Prigogine I (1977) Self-organization in nonequilibrium systems: from dissipative structures to order through fluctuations. Wiley and Sons, New York

    Google Scholar 

  • Nusser Z, Kay LM, Laurent G, Homanics GE, 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

    PubMed  CAS  Google Scholar 

  • Pérez-Borja C, Tyce FA, McDonald C, Uihlein A (1961) Depth electrographic studies of a focal fast response to sensory stimulation in the human. Electroencephalogr Clin Neurophysiol 13:695–702

    Article  Google Scholar 

  • Phillips CG, Powell TP, Shepherd GM (1963) Responses of mitral cells to stimulation of the lateral olfactory tract in the rabbit. J Physiol 168:65–88

    PubMed  CAS  Google Scholar 

  • Prigogine I (1978) Time, structure, and fluctuations. Science 201:777–785

    Article  PubMed  Google Scholar 

  • Rall W (1962) Electrophysiology of a dendritic neuron model. Biophys J 2:145–167

    Article  PubMed  CAS  Google Scholar 

  • Rall W (1964) Theoretical significance of dendritic trees for neuronal input-output relations. In: Reiss RF (ed) Neural theory and modeling. Stanford University Press, Stanford

    Google Scholar 

  • Rall W, Shepherd GM (1968) Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31:884–915

    PubMed  CAS  Google Scholar 

  • Rall W, Shepherd GM, Reese TS, Brightman MW (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14:44–56

    Article  PubMed  CAS  Google Scholar 

  • Rawson NE, Eberwine J, Dotson R, Jackson J, Ulrich P, Restrepo D (2000) Expression of mRNAs encoding for two different olfactory receptors in a subset of olfactory receptor neurons. J Neurochem 75:185–195

    Article  PubMed  CAS  Google Scholar 

  • Ressler KJ, Sullivan SL, Buck LB (1993) A zonal organization of odorant receptor gene expression in the olfactory epithelium. Cell 73:597–609

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez R, Kallenbach U, Singer W, Munk MHJ (2004) Short- and long-term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. J Neurosci 24:10369–10378

    Article  PubMed  CAS  Google Scholar 

  • Schoenfeld TA, Knott TK (2004) Evidence for the disproportionate mapping of olfactory airspace onto the main olfactory bulb of the hamster. J Comp Neurol 476:186–201

    Article  PubMed  Google Scholar 

  • Schutt A, Basar E (1992) The effects of acetylcholine, dopamine and noradrenaline on the visceral ganglion of Helix pomatia. II. Stimulus evoked field potentials. Comp Biochem Physiol C 102:169–176

    Article  PubMed  CAS  Google Scholar 

  • Sem-Jacobsen CW, Bickford RG, Dodge HW Jr, Petersen MC (1953) Human olfactory responses recorded by depth electrography. Proc Staff Meet Mayo Clin 28:166–170

    PubMed  CAS  Google Scholar 

  • Senut MC, Menetrey D, Lamour Y (1989) Cholinergic and peptidergic projections from the medial septum and the nucleus of the diagonal band of Broca to dorsal hippocampus, cingulate cortex and olfactory bulb: a combined wheatgerm agglutinin-apohorseradish peroxidase-gold immunohistochemical study. Neuroscience 30:385–403

    Article  PubMed  CAS  Google Scholar 

  • Serizawa S, Ishii T, Nakatani H, Tsuboi A, Nagawa F, Asano M, Sudo K, Sakagami J, Sakano H, Ijiri T, Matsuda Y, Suzuki M, Yamamori T, Iwakura Y, Sakano H (2000) Mutually exclusive expression of odorant receptor transgenes. Nat Neurosci 3:687–693

    Article  PubMed  CAS  Google Scholar 

  • Serizawa S, Miyamichi K, Sakano H (2004) One neuron-one receptor rule in the mouse olfactory system. Trends Genet 20:648–653

    Article  PubMed  CAS  Google Scholar 

  • Shepherd GM (1972) Synaptic organization of the mammalian olfactory bulb. Physiol Rev 52:864–917

    PubMed  CAS  Google Scholar 

  • Shepherd GM, Chen WR, Greer CA (2004) Olfactory bulb. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford University Press, New York

    Google Scholar 

  • Sherrington C (1906) The integrative action of the nervous system. The University Press, Cambridge

    Google Scholar 

  • Shipley MT, McLean J, Ennis M (1995) Olfactory system. In: Paxinos G (ed) The rat nervous system. Academic Press

  • Siklos L, Rickmann M, Joo F, Freeman WJ, Wolff JR (1995) Chloride is preferentially accumulated in a subpopulation of dendrites and periglomerular cells of the main olfactory bulb in adult rats. Neuroscience 64:165–172

    Article  PubMed  CAS  Google Scholar 

  • Simoes-de-Souza FM, Roque AC (2004) A biophysical model of vertebrate olfactory epithelium and bulb exhibiting gap junction dependent odor-evoked spatiotemporal patterns of activity. Biosystems 73:25–43

    Article  PubMed  Google Scholar 

  • Steriade M, Contreras D, Amzica F, Timofeev I (1996) Synchronization of fast (30–40 Hz) spontaneous oscillations in intrathalamic and thalamocortical networks. J Neurosci 16:2788–2808

    PubMed  CAS  Google Scholar 

  • Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70–74

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi Y, Kimura H, Sano Y (1982) Immunohistochemical demonstration of serotonin nerve fibers in the olfactory bulb of the rat, cat and monkey. Histochemistry 75:461–471

    PubMed  CAS  Google Scholar 

  • Tallon C, Bertrand O, Bouchet P, Pernier J (1995) Gamma-range activity evoked by coherent visual stimuli in humans. Eur J Neurosci 7:1285–1291

    Article  PubMed  CAS  Google Scholar 

  • Traub RD, Spruston N, Soltesz I, Konnerth A, Whittington MA, Jefferys GR (1998) Gamma-frequency oscillations: a neuronal population phenomenon, regulated by synaptic and intrinsic cellular processes, and inducing synaptic plasticity. Prog Neurobiol 55:563–575

    Article  PubMed  CAS  Google Scholar 

  • Vucinic D, Cohen LB, Kosmidis EK (2006) Interglomerular center-surround inhibition shapes odorant-evoked input to the mouse olfactory bulb in vivo. J Neurophysiol 95:1881–1887

    Article  PubMed  Google Scholar 

  • Waage P, Gulberg CM (1986) Studies concerning affinity. J Chem Educ 63:1044–1047

    Article  Google Scholar 

  • Wachowiak M, Shipley MT (2006) Coding and synaptic processing of sensory information in the glomerular layer of the olfactory bulb. Semin Cell Dev Biol 17:411–423

    Article  PubMed  Google Scholar 

  • Wachowiak M, McGann JP, Heyward PM, Shao Z, Puche AC, Shipley MT (2005) Inhibition [corrected] of olfactory receptor neuron input to olfactory bulb glomeruli mediated by suppression of presynaptic calcium influx. J Neurophysiol 94:2700–2712

    Article  PubMed  CAS  Google Scholar 

  • Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH (2000) Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol 38:315–336

    Article  PubMed  CAS  Google Scholar 

  • Wilson M, Bower JM (1992) Cortical oscillations and temporal interactions in a computer simulation of piriform cortex. J Neurophysiol 67:981–995

    PubMed  CAS  Google Scholar 

  • Yu GZ, Kaba H, Okutani F, Takahashi S, Higuchi T, Seto K (1996) The action of oxytocin originating in the hypothalamic paraventricular nucleus on mitral and granule cells in the rat main olfactory bulb. Neuroscience 72:1073–1082

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

DRL and LK were supported by a grant for Collaborative Research in Computational Neuroscience (CRCNS) (NIDCD R01DC007995, LK).

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  1. Committee on Neurobiology, Institute for Mind & Biology, The University of Chicago, Chicago, IL, 60637, USA

    Daniel Rojas-Líbano & Leslie M. Kay

  2. Department of Psychology, Institute for Mind & Biology, The University of Chicago, 940 E 57th St., Chicago, IL, 60637, USA

    Leslie M. Kay

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  1. Daniel Rojas-Líbano
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Correspondence to Leslie M. Kay.

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Rojas-Líbano, D., Kay, L.M. Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cogn Neurodyn 2, 179–194 (2008). https://doi.org/10.1007/s11571-008-9053-1

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