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.
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.
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.
Beierlein M, Gibson JR, Connors BW (2000) A network of electri cally coupled interneurons drives synchronized inhibition in neocortex. Nature Neurosci. 3: 904–910.
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
Bennett MV (1997) Gap junctions as electrical synapses. J. Neurocytol. 26: 349–366.
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.
Bou-Flores C, Berger AJ (2001) Gap junctions and inhibitory synapses modulate inspiratory motoneuron synchronization. J. Neurophysiol. 85: 1543–1551.
Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthase, a calmodulin requiring enzyme. Proc. Natl. Acad. Sci. USA 87: 682–685.
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.
Buzsaki G, Chrobak JJ (1995) Temporal structure in spatially or ganized neuronal ensembles: A role for interneuronal networks. Curr. Opin. Neurobiol. 5: 504–510.
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.
Cleland TA (1996) Inhibitory glutamate receptor channels. Mol. Neurobiol. 13: 97–136.
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.
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.
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.
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.
Denk W, Svoboda K (1997) Photon upmanship: Why multiphoton imaging is more than a gimmick. Neuron 18: 351–357.
Dorries KM, Kauer JS (2000) Relationship between odor-elicited oscillations in the salamander olfactory epithelium and olfactory bulb. J. Neurophysiol. 83: 754–765.
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.
Ermentrout B (2002) Simulating, Analyzing, Animating Dynami cal Systems: A Guide to XPPAUT for Researchers and Students, SIAM, Philadelphia, PA.
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.
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.
Ermentrout GB, Kleinfeld D (2001) Traveling electrical waves in cortex: Insights from phase dynamics and speculation on a computational role. Neuron 29: 33–44.
Evans WH, Martin PEM (2002) Gap junctions: Structure and function. Mol. Membrane Biol. 19: 121–13
Freeman WJ (1978) Spatial properties of an EEG event in the olfactory bulb and cortex. Electroenceph. Clin. Neurophysiol. 44: 586–605.
Freund TF, Buzski G (1996) Interneurons of the hippocampus. Hippocampus. 6: 347–470.
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.
Gelperin A, Tank DW(1990) Odor-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345: 437–440.
Gelperin A (1994) Nitric oxide mediates network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 369: 61–63.
Gelperin A (1999) Oscillatory dynamics and information processing in olfactory systems. J. Exp. Biol. 202: 1855–1864.
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.
Gelperin A, Kao JPY, Cooke IRC (2001) Gaseous oxides and olfactory computation. Amer. Zool. 41: 332–345.
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.
Hrabie JA, Klose JR, Wink DA, Keefer LK (1993) New nitric oxide-releasing zwitterions derived from polyamines. J. Org. Chem. 58: 1472–1476.
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.
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–
Huguenard JR, McCormick DA(1992) Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophys. 68: 1373–1383.
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.
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.
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.
Kawai F, Miyachi E (2001) Modulation by cGMP of the voltage-gated currents in newt olfactory receptor cells. Neurosci Res. 39: 327–337.
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.
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.
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.
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.
Kopell N, Ermentrout GB (1986) Symmetry and phaselocking in chains of weakly coupled oscillators. Comm Pure Appl. Math. 39: 623–660.
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.
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.
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.
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.
Makings LR, Tsien RY (1994) Caged nitric oxide. J. Biol. Chem. 269: 6282–6285.
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.
Mills SL, Massey SC (2000) A series of biotinylated tracers distinguishes three types of gap junction in retina. J. Neurosci. 20: 8629–8636.
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.
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.
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.
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.
Phelan P, Starich TA (2001) Innexins get into the gap. Bioessays 23: 388–396.
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.
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.
Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1999) Numerical Recipes in C (2nd ed.) Cambridge University Press, Cambridge, UK.
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.
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.
(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.
Spray DC, White RL, Mazet F, Bennett MV (1985) Regulation of gap junctional conductance. Am. J. Physiol. 248: H753–764.
Stopfer M, Bhagavan S, Smith BH, Laurent G(1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390: 70–74.
Teyke T, Gelperin A (1999) Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. Neuroreport 10: 1061–1068.
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.
Traub RD, Miles R (1991) Neuronal Networks of the Hippocampus. Cambridge University Press, Cambridge, UK.
Wang JW, Flores J, Gelperin A (1999) Physiological and morphological studies of olfactory interneurons in an oscillatory network. Soc. Neurosci. Abstr. 25: 126.
(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.
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.
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.
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.
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.
Wehr M, Laurent G (1996) Odor encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384: 162–166.
Wong WT, Sanes JR, Wong ROL (1998) Developmentally regulated spontaneous activity in the embryonic chick retina. J. Neurosci. 18: 8839–8852.
Yunker AMR (2003) Modulation and pharmacology of low voltage-activated ("T-type") calcium channels. J. Bioenergetics Biomembranes. 35: 577–598.
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.
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
Author information
Authors and Affiliations
Rights 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
Issue Date:
DOI: https://doi.org/10.1023/B:JCNS.0000044877.21949.44