Skip to main content
Log in

Model for Transition from Waves to Synchrony in the Olfactory Lobe of Limax

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

A biophysical model for the interactions between bursting (B) cells and nonbursting (NB) cells in the procerebral lobe of Limax is developed and tested. Phase-sensitivity of the NB cells is exhibited due to the strong inhibition from the rhythmically bursting B cells. Electrical and chemical junctions coupled with a parameter gradient lead to sustained periodic waves in the lobe. Excitatory interactions between the NB cells, which rarely fire, lead to stimulus evoked synchrony in the lobe oscillations. A novel calcium current is suggested to explain the effects of nitric oxide (NO) on the lobe. Gap junctions are shown both experimentally and through simulations to be required for the oscillating field potentials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahern GP, Klyachko VA, Jackson MB (2002) cGMP and S-nitrosylation: Two routes for modulation of neuronal excitability by NO. Trends Neurosci. 25: 510–517.

    Google Scholar 

  • Bazhenov M, Stopfer M, Rabinovich M, Abarbanel HD, Sejnowski TJ, Laurent G (2001) Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron 30: 569–581.

    Google Scholar 

  • Beierlein M, Gibson JR, Connors BW (2000) A network of electri cally coupled interneurons drives synchronized inhibition in neocortex. Nature Neurosci. 3: 904–910.

    Google Scholar 

  • Bem T, Rinzel J (2004) Short duty cycle destabilizes a half-center oscillator, but gap junctions can restabilize the anti-phase pattern. J. Neurophysiol. 91: 693–703

    Google Scholar 

  • Bennett MV (1997) Gap junctions as electrical synapses. J. Neurocytol. 26: 349–366.

    Google Scholar 

  • Bodmer R, Verselis V, Levitan IB, Spray DC (1988) Electronic synapses between Aplysia neurons in situ and in culture: Aspects of regulation and measurements of permeability. J. Neurosci. 8: 1656–1670.

    Google Scholar 

  • Bou-Flores C, Berger AJ (2001) Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization. J. Neurophysiol. 85: 1543–1551.

    Google Scholar 

  • Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthase, a calmodulin requiring enzyme. Proc. Natl. Acad. Sci. USA 87: 682–685.

    Google Scholar 

  • Buerk D, Ances B, Greenberg J, Detre J (2003) Temporal dynamics of brain tissue nitric oxide during functional forepaw stimulation in rats. Neuroimage. 18: 1-9.

    Google Scholar 

  • Buzsaki G, Chrobak JJ (1995) Temporal structure in spatially or ganized neuronal ensembles: A role for interneuronal networks. Curr. Opin. Neurobiol. 5: 504–510.

    Google Scholar 

  • Carter TD, Bettache N, Ogden D, Trentham DR (1993) Photochemi cal release of nitric oxide from ruthenium nitrosyl trichloride: Re laxation of rabbit isolated aortic rings mediated by photo-release of nitric oxide. J. Physiol. 467: 165P.

    Google Scholar 

  • Cleland TA (1996) Inhibitory glutamate receptor channels. Mol. Neurobiol. 13: 97–136.

    Google Scholar 

  • Cooke IRC, Edwards SL, Anderson CR (1994) The distribution of NADPH-diaphorase activity and immunoreactivity to nitric oxide synthase in the nervous system of the pulmonate mollusc Helix aspersa. Cell Tissue Research 277: 565–572.

    Google Scholar 

  • Copeland J, Gelperin A (1983) Feeding and a serotonergic interneu ron activate an identified autoactive salivary neuron in Limax max imus. Comp. Biochem. Physiol. 76A: 21–30.

    Google Scholar 

  • Davidson JS, Baumgarten IM (1988) Glycyrrhetinic acid derivatives: A novel class of inhibitors of gap-junctional intercellular commu nication. Structure-activity relationships. J. Pharmacol. Exp. Ther. 246: 1104–1107.

    Google Scholar 

  • Delaney KR, Gelperin A, Fee MS, Flores JA, Gervais R, Tank DW, Kleinfeld D (1994) Waves and stimulus-modulated dynamics in an oscillating olfactory network. Proc. Natl. Acad. Sci. USA 91: 669–673.

    Google Scholar 

  • Denk W, Svoboda K (1997) Photon upmanship: Why multiphoton imaging is more than a gimmick. Neuron 18: 351–357.

    Google Scholar 

  • Dorries KM, Kauer JS (2000) Relationship between odor-elicited oscillations in the salamander olfactory epithelium and olfactory bulb. J. Neurophysiol. 83: 754–765.

    Google Scholar 

  • Elphick MR, Kemenes G, Staras K, O'Shea M (1995) Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J. Neurosci. 15: 7653–7664.

    Google Scholar 

  • Ermentrout B (2002) Simulating, Analyzing, Animating Dynami cal Systems: A Guide to XPPAUT for Researchers and Students, SIAM, Philadelphia, PA.

    Google Scholar 

  • Ermentrout B, Flores J, Gelperin A (1998) Minimal model of os cillations and waves in the Limax olfactory lobe with tests of the model's predictive power. J. Neurophysiol. 79: 2677–2689.

    Google Scholar 

  • Ermentrout B, Wang JW, Flores J, Gelperin A (2001) Model for olfactory discrimination and learning in Limax procerebrum in corporating oscillatory dynamics and wave propagation. J. Neurophysiol. 85: 1444–1452.

    Google Scholar 

  • Ermentrout GB, Kleinfeld D (2001) Traveling electrical waves in cortex: Insights from phase dynamics and speculation on a computational role. Neuron 29: 33–44.

    Google Scholar 

  • Evans WH, Martin PEM (2002) Gap junctions: Structure and function. Mol. Membrane Biol. 19: 121–13

    Google Scholar 

  • Freeman WJ (1978) Spatial properties of an EEG event in the olfactory bulb and cortex. Electroenceph. Clin. Neurophysiol. 44: 586–605.

    Google Scholar 

  • Freund TF, Buzski G (1996) Interneurons of the hippocampus. Hippocampus. 6: 347–470.

    Google Scholar 

  • Fujie S, Aonuma H, Ito I, Gelperin A, Ito E (2002) The nitric oxide/ cyclic GMP pathway in the olfactory processing system of the terrestrial slug Limax maximus. Zoolog. Sci. 19:15-26.

    Google Scholar 

  • Gelperin A, Tank DW(1990) Odor-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345: 437–440.

    Google Scholar 

  • Gelperin A (1994) Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369: 61–63.

    Google Scholar 

  • Gelperin A (1999) Oscillatory dynamics and information processing in olfactory systems. J. Exp. Biol. 202: 1855–1864.

    Google Scholar 

  • Gelperin A, Flores J, Raccuia-Behling F, Cooke IRC (2000) Nitric oxide and carbon monoxide modulate oscillations of olfactory interneurons in a terrestrial mollusc. J. Neurophysiol. 83: 116–127.

    Google Scholar 

  • Gelperin A, Kao JPY, Cooke IRC (2001) Gaseous oxides and olfactory computation. Amer. Zool. 41: 332–345.

    Google Scholar 

  • Gervais R, Kleinfeld D, Delaney KR, Gelperin A (1996) Central and reflex neuronal responses elicited by odor in a terrestrial mollusc. J. Neurophysiol. 76: 1327–1339.

    Google Scholar 

  • Hrabie JA, Klose JR, Wink DA, Keefer LK (1993) New nitric oxide-releasing zwitterions derived from polyamines. J. Org. Chem. 58: 1472–1476.

    Google Scholar 

  • Huang S, Kerschbaum HH, Engel E, Hermann A (1997) Biochemical characterization and histochemical localization of nitric oxide synthase in the nervous system of the snail, Helix pomatia. J Neurochem 69: 2516–2528.

    Google Scholar 

  • Huang L, Keyser B, Tagmose T, Hansen J, Taylor J, Zhuang H, Zhang M, Ragsdale D, Li M (2004) NNC 55-0396 [(1S, 2S)-2-(2-(N-[( 3-benzimidazol-2-yl) propyl]-N-methylamino)ethyl)-6-fluoro-1,2,3,4-tetrahydro-1-isopropyl-2-napht yl cyclopropanecarboxy-late dihydrochloride]: A new selective inhibitor of T-type calcium channels. J. Pharmacol. Exp. Therapeutics 309: 193–

    Google Scholar 

  • Huguenard JR, McCormick DA(1992) Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophys. 68: 1373–1383.

    Google Scholar 

  • Inoue T, Watanabe S, Kawahara S, Kirino Y(2000) Phase-dependent filtering of sensory information in the oscillatory olfactory center of a terrestrial mollusk. J. Neurophysiol. 84: 1112–1115.

    Google Scholar 

  • Inoue T, Inokuma Y, Watanabe S, Kirino Y (2004) In vitro study of odor-evoked behavior in a terrestrial mollusk. J. Neurophysiol. 91: 372–381.

    Google Scholar 

  • Jacklet JW, Tieman DG (2004) Nitric oxide and histamine induce neuronal excitability by blocking background currents in neuron MCC of Aplysia. J. Neurophysiol. 91: 656–665.

    Google Scholar 

  • Kawai F, Miyachi E (2001) Modulation by cGMP of the voltage-gated currents in newt olfactory receptor cells. Neurosci Res. 39: 327–337.

    Google Scholar 

  • Kimura T, Suzuki H, Kono E, Sekiguchi T (1998a) Mapping of interneurons that contribute to food aversion conditioning in the slug brain. Learning & Memory 4: 376–388.

    Google Scholar 

  • Kimura T, Toda S, Sekiguchi T, Kawahara S, Kirino Y (1998b) Optical recording analysis of olfactory response of the procerebral lobe in the slug brain. Learning & Memory 4: 289–400.

    Google Scholar 

  • Kimura T, Toda S, Sekiguchi T, Kirino Y (1998c) Behavioral modulation induced by food odor aversive conditioning and its influence on the olfactory responses of an oscillatory brain net-work in the slug Limax marginatus. Learning & Memory 4: 365–375.

    Google Scholar 

  • Kleinfeld D, Delaney KR, Fee MS, Flores JA, Tank DW, Gelperin A (1994) Dynamics of propagating waves in the olfactory network of a terrestrial mollusc: An electrical and optical study. J. Neurophysiol. 72: 1402–1419.

    Google Scholar 

  • Kopell N, Ermentrout GB (1986) Symmetry and phaselocking in chains of weakly coupled oscillators. Comm Pure Appl. Math. 39: 623–660.

    Google Scholar 

  • Korneev SA, Piper MR, Picot J, Phillips R, Korneeva EI, O'Shea M (1998) Molecular characterization of NOS in a mollusc: Expression in a giant modulatory neuron. J. Neurobiol. 35: 65-76.

    Google Scholar 

  • Korneev SA, Kemenes I, Straub V, Staras K, Korneeva EI, Kemenes G, Benjamin PR, OÕShea M. Suppression of nitric oxide (NO)-dependent behavior by double-stranded RNA-mediated silencing of a neuronal NO synthase gene. J. Neurosci. 22: RC227(1-5).

  • Lam Y-W, Cohen LB, Wachowiak M, Zochowski MR (2000) Odors elicit three different oscillations in the turtle olfactory bulb. J. Neurosci. 20: 749–762.

    Google Scholar 

  • Largo C, Tombaugh GC, Aitken PG, Herreras O, Somjen GG (1997) Heptanol but not fluoroacetate prevents the propagation of spreading depression in rat hippocampal slices. J. Neurophysiol. 77: 9–16.

    Google Scholar 

  • Laurent G, Stopfer M, Friedrich RW, Rabinovich MI, Volkovskii A, Abarbanel HD (2001) Odor encoding as an active, dynamical process: Experiments, computation, and theory. Annu. Rev. Neurosci. 24: 263–297.

    Google Scholar 

  • Makings LR, Tsien RY (1994) Caged nitric oxide. J. Biol. Chem. 269: 6282–6285.

    Google Scholar 

  • Martin C, Gervais R, Hugues E, Messaoudi B, 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.

    Google Scholar 

  • Mills SL, Massey SC (2000) A series of biotinylated tracers distinguishes three types of gap junction in retina. J. Neurosci. 20: 8629–8636.

    Google Scholar 

  • Murakami M, Watanabe S, Inoue T, Kirino Y (2004) Odor-evoked responses in the olfactory center neurons in the terrestrial slug. J. Neurobiol. 58: 369–378.

    Google Scholar 

  • Murlis J, Willis MA, Carde RT (1990) Odour signals: Patterns in space and time. In: KB Doving, ed., Proceedings of the Tenth International Symposium on Olfaction and Taste, Graphic Communication Systems, Oslo, pp. 6-17.

  • Murlis J, Elkinton JS, Carde RT (1992) Odor plumes and howinsects use them. Ann. Rev. Entomol. 37: 505–532.

    Google Scholar 

  • Ozog MA, Siushansian R, Naus CC (2002) Blocked gap junctional coupling increases glutamate-induced neurotoxicity in neuron-astrocyte cocultures. J. Neuropathol. Exp. Neurol. 61: 132–141.

    Google Scholar 

  • Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S (2000) A ubiquitous family of putative gap junction molecules. Curr. Biol. 10: R473–R474.

    Google Scholar 

  • Phelan P, Starich TA (2001) Innexins get into the gap. Bioessays 23: 388–396.

    Google Scholar 

  • Prechtl J, Cohen LB, Pesaran B, Mitra PP, Kleinfeld D (1997) Visual stimuli induce waves of electrical activity in turtle cortex. Proc. Natl. Acad. Sci. USA 94: 7621–7626.

    Google Scholar 

  • Prechtl JC, Bullock TH, Kleinfeld D (2000) Direct evidence for local oscillatory current sources and intracortical phase gradients in turtle visual cortex. Proc. Natl. Acad. Sci. USA 97: 877–882.

    Google Scholar 

  • Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1999) Numerical Recipes in C (2nd ed.) Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Prior D, Gelperin A (1977) Autoactive molluscan neuron: Reflex function and synaptic modulation during feeding in the terrestrial slug Limax maximus. J. Comp. Physiol. 114: 217–232.

    Google Scholar 

  • Sanchez-Alvarez M, Lean-Olea M, Talavera E, Pellicer F, Sanchez-Islas E, Martinez-Lorenzana G (1994) Distribution of NADPH-diaphorase in the perioesophageal ganglia of the snail, Helix aspersa. Neurosci. Lett. 169: 51–55.

    Google Scholar 

  • (2004) Abiophysical model of vertebrate olfactory epithelium and bulb exhibiting gap junction dependent odor-evoked spatiotemporal patterns of activity. BioSystems 73:25-43.

  • Skinner FK, Zhang L, Perez Velazquez JL, Carlen PL(1999) Bursting in inhibitory interneuronal networks: A role for gap-junctional coupling. J. Neurophysiol. 81: 1274–1283.

    Google Scholar 

  • Spray DC, White RL, Mazet F, Bennett MV (1985) Regulation of gap junctional conductance. Am. J. Physiol. 248: H753–764.

    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.

    Google Scholar 

  • Teyke T, Gelperin A (1999) Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. Neuroreport 10: 1061–1068.

    Google Scholar 

  • Toda S, Kawahara S, Kirino y (2000) Image analysis of olfactory responses in the procerebrum of the terrestrial slug Limax marginatus. J. Exp. Biol. 203: 2895–2905.

    Google Scholar 

  • Traub RD, Miles R (1991) Neuronal Networks of the Hippocampus. Cambridge University Press, Cambridge, UK.

    Google Scholar 

  • Wang JW, Flores J, Gelperin A (1999) Physiological and morphological studies of olfactory interneurons in an oscillatory network. Soc. Neurosci. Abstr. 25: 126.

    Google Scholar 

  • (2001) Initiation and propagation of calcium-dependent action potentials in a coupled network of olfactory interneurons. J. Neurophysiol. 85: 977–985.

  • Wang XJ, Rinzel J (1993) Spindle rhythmicity in the reticularis thalami nucleus: Synchronization among mutually inhibitory neurons. Neurosci. 53: 899–904.

    Google Scholar 

  • Watanabe S, Kawahara S, Kirino Y (1998) Morphological chracterization of the bursting and nonbursting neurones in the olfactory centre of the terrestrial slug Limax marginatus. J. Exp. Biol. 201: 925–930.

    Google Scholar 

  • Watanabe S, Kawahara S, Kirino Y (1999) and K +currents in the olfactory interneurons of a terrestrial slug. J. Comp. Physiol. A 184: 553–562.

    Google Scholar 

  • Watanabe S, Inoue T, Murakami M, Inokuma Y, Kawahara S, Kirino Y(2001) Modulation of oscillatory neural activities by cholinergic activation of interneurons in the olfactory center of a terrestrial slug. Brain Res. 896: 30–35.

    Google Scholar 

  • Watanabe S, Inoue T, Kirino Y (2003) Contribution of excitatory chloride conductance in the determination of the direction of traveling waves in an olfactory center. J. Neurosci. 23(7): 2932–2938.

    Google Scholar 

  • Wehr M, Laurent G (1996) Odor encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384: 162–166.

    Google Scholar 

  • Wong WT, Sanes JR, Wong ROL (1998) Developmentally regulated spontaneous activity in the embryonic chick retina. J. Neurosci. 18: 8839–8852.

    Google Scholar 

  • Yunker AMR (2003) Modulation and pharmacology of low voltage-activated ("T-type") calcium channels. J. Bioenergetics Biomembranes. 35: 577–598.

    Google Scholar 

  • Zakharov IS, Hayes NL, Ierusalimsky VN, Nowakowski RS, Balaban PM (1998) Postembryonic neurogenesis in the procerebrum of the terrestrial snail, Helix lucorum. J. Neurobiol. 35: 271–276.

    Google Scholar 

  • Zhang Y, Perez Velazquez JL, Tian GF, Wu C-W, Skinner FK, Carlen PL, Zhang L (1998) Slow oscillations (1 Hz) mediated by GABAergic interneuronal networks in rat hippocampus. J. Neurosci. 18: 9256–9

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ermentrout, B., Wang, J.W., Flores, J. et al. Model for Transition from Waves to Synchrony in the Olfactory Lobe of Limax. J Comput Neurosci 17, 365–383 (2004). https://doi.org/10.1023/B:JCNS.0000044877.21949.44

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:JCNS.0000044877.21949.44

Navigation