Summary
The influences of centrifugal projections to the olfactory bulb were examined on the bulbar EEG and mitral-tufted cell activity in waking rabbits. Each of 6 rabbits was implanted, under surgical anesthesia, with fine wire electrodes for recording of the EEG and mitral-tufted cell unit activity and for stimulating the lateral olfactory tract. Two cooling probes, for reversible cryogenic blockade, were implanted on either side of the left olfactory peduncle. Records of EEG and unit activity were taken for 200 s before, during and after cooling of the probes to 3 degrees centigrade. Antidromic evoked potentials were used to assess the efficacy of the blockade. During the cryogenic blockade bursts of EEG activity, evoked in the bulb by inspiration through the nose, were augmented in amplitude and reduced in frequency. Mitral-tufted cell unit activity was reduced in rate but was more highly correlated with the phase and amplitude of the EEG bursts. Analysis of individual EEG bursts revealed that the variance in frequency of bulbar activity was significantly reduced in the isolated state. The data demonstrate that oscillatory bursting activity in the olfactory bulb is intrinsically maintained within a relatively fixed frequency range during receptor input and does not depend on centrifugal projections for its electrogenesis. Changes in EEG frequency, amplitude and correlation with unit activity support the hypothesis that centrifugal projections act in part to inhibit mitral-tufted cell output by direct excitation of granule cells. These findings are supported by a theoretical model in which distributed feedback to the granule cells from more central olfactory structures acts to regulate the coherency of bulbar activity.
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References
Becker CJ, Freeman WJ (1968) Prepyriform electrical activity after loss of peripheral or central input or both. Physiol Behav, 597–599
Broadwell RD, Jacobowitz DM (1976) Olfactory relationships of the telencephalon and diencephalon in the rabbit. III. The ipsilateral centrifugal fibers to the olfactory bulbar and retrobulbar formations. J Comp Neurol 170: 321–346
Cajal SR (1955) Studies on the cerebral cortex (limbic structures). Translated by L.M. Kraft Lloyd-Luke Ltd, London, 179 pp
Cattarelli M (1982) The role of the medial olfactory pathways in olfaction: behavioral and electrophysiological data. Behav Brain Res 6: 339–364
Chaput MA (1983) Effects of peduncle sectioning on the single unit responses of olfactory bulb neurons to odor presentation in awake rabbits. Chem Senses 8: 161–177
Chaput MA, Holley A (1985) Responses of olfactory bulb neurons to repeated odor stimulations in awake freely-breathing rabbits. Physiol Behav 34: 249–258
Davis BJ, Macrides F, Youngs WM, Schneider SP, Rosene DL (1978) Efferents and centrifugal afferents of the main and the accessory olfactory bulb in the hamster. Brain Res Bull 3: 59–72
Dennis BJ, Kerr DIB (1968) An evoked potential study of centripetal and centrifugal connections of the olfactory bulb in the cat. Brain Res 11: 373–396
Doving KB, Hyvärinen J (1969) Afferent and efferent influences on the activity pattern of single olfactory neurons. Acta Physiol Scand 75: 111–123
Fox SS, O'Brian JH (1965) Duplication of evoked potential waveform by curve of probability of firing of a single cell. Science 147: 888–890
Freeman WJ (1972) Depth recording of averaged evoked potential of olfactory bulb. J Neurophysiol 35: 780–796
Freeman WJ (1974) Average transmission distance from mitraltufted to granule cells in olfactory bulb. Electroencephalogr Clin Neurophysiol 36: 609–618
Freeman WJ (1975) Mass action in the nervous system. Academic Press, New York
Freeman WJ (1979a) Nonlinear gain mediating cortical stimulusresponse relations. Biol Cybern 33: 237–247
Freeman WJ (1979b) Nonlinear dynamics of paleocortex manifested in the olfactory EEG. Biol Cybern 35: 21–37
Freeman WJ (1979c) EEG analysis gives model of neuronal template-matching mechanism for sensory search with olfactory bulb. Biol Cybern 35: 221–234
Freeman WJ, Schneider W (1982) Changes in spatial pattern of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19: 44–56
Freeman WJ (1987a) Analytic techniques used in the search for the physiological basis of the EEG. In: Gevins A, Redmond A (eds) Handbook of electroencephalography and clinical neurophysiology, Vol 3A, Part 2, Chap 14. Elsevier, Amsterdam
Freeman WJ (1987b) Simulation of chaotic EEG patterns with a dynamic model of the olfactory system. Biol Cybern 56: 139–150
Frost JD Jr, Elazar Z (1968) Three-dimensional selective amplitude histograms: a statistical approach to EEG-single neuron relationships. Electroencephalogr Clin Neurophysiol 25: 499–503
Gervais R, Pager J (1983) Olfactory bulb excitability selectively modified in behaving rats after local 6-hydroxydopamine treatment. Behav Brain Res 9: 165–179
Gervais R, Araneda S, Pujol JF (1984) Effect of local 5,6-dihydroxytryptamine on the rat olfactory bulb responsiveness during wakefulness and sleep. Electroencephalogr Clin Neurophysiol 57: 462–472
Gray CM, Freeman WJ, Skinner JE (1986) Chemical dependencies of learning in the rabbit olfactory bulb: acquisition of the transient spatial-pattern change depends on norepinephrine. Behav Neurosci 100: 585–596
Haberly LB, Price JL (1978a) Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas J Comp Neurol 178: 711–740
Haberly LB, Bower JM (1984) Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. J Neurophysiol 51: 90–112
Hernandez-Peon R, Lavin A, Alcocer-Cuaron C, Marcelin JP (1960) Electrical activity of the olfactory bulb during wakefulness and sleep. J Electroencephalogr Clin Neurophysiol 12: 41–58
Kishi K, Mori K, Ojima H (1984) Distribution of local axon collaterals of mitral, displaced mitral, and tufted cells in the rabbit olfactory bulb. J Comp Neurol 225: 511–526
Luskin MB, Price JL (1983) The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216: 264–291
Moore GP, Perkel DH, Segundo JP (1966) Statistical analysis and functional interpretation of neuronal spike data. Ann Rev Physiol 28: 493–522
Moulton DG (1963) Electrical activity in the olfactory system of rabbits with indwelling electrodes. In: Zotterman Y (ed) Olfaction and taste I. Pergamon Press, Oxford, pp 71–84
Nakashima M, Mori K, Takagi SF (1978) Centrifugal influence on olfactory bulb activity in the rabbit. Brain Res 154: 301–316
Nicoll RA (1969) Inhibitory mechanisms in the rabbit olfactory bulb: dendrodendritic mechanisms. Brain Res 14: 157–172
Nicoll RA (1971a) Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res 35: 137–149
Nicoll RA (1971b) Recurrent excitation of secondary olfactory neurons: a possible mechanism for signal amplification. Science 171: 824–825
Nicoll RA, Jahr CE (1982) Self-excitation of olfactory bulb neurons. Nature 296: 441–444
Pager J (1978) Ascending olfactory information and centrifugal influxes contributing to a nutritional modulation of the rat mitral cell responses. Brain Res 140: 251–269
Potter H, Chorover SL (1976) Response plasticity in hamster olfactory bulb: peripheral and central processes. Brain Res 116: 417–429
Price JL, Powell TPS (1970) An electron-microscopic study of the termination of the afferent fibers to the olfactory bulb from the cerebral hemisphere. J Cell Sci 7: 157–187
Rall W, Shepherd GM, Reese TS, Brightman MW (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14: 44–56
Rall W, Shepherd GM (1968) Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J Neurophysiol 31: 884–915
Schild D (1985) Temporal changes in mitral cell response patterns during repeated odor exposure. Arch Ital Biol 123: 27–42
Schoenfeld TA, Marchand JE, Macrides F (1985) Topographic organization of tufted cell axonal projections in the hamster main olfactory bulb: an intrabulbar associational system. J Comp Neurol 235: 503–518
Skinner JE, Gray CM (1986) Habituation and sensitization in the olfactory bulb of the rabbit: EEG activity and sniffing behavior. Neuroscience Abstr 12: 140.3
Skinner JE, Lindsley DB (1968) Reversible cryogenic blockade of neural function in the brain of unrestrained animals. Science 161: 595–597
Skinner JE, Welch KMA, Reed JC, Nell JH (1978) Psychologic stress reduces cyclic 3′,5′-adenosine monophosphate levels in the cerebral cortex of conscious rats, as determined by a new cryogenic method of rapid tissue fixation. J Neurochem 30: 691–698
Vianna Di Prisco G, Freeman WJ (1985) Odor-related bulbar EEG spatial pattern analysis during appetitive conditioning in rabbits. Behav Neurosci 99: 964–978
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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. Exp Brain Res 69, 378–386 (1988). https://doi.org/10.1007/BF00247583
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DOI: https://doi.org/10.1007/BF00247583