Abstract
A statistical analysis of the baseline activity of neurons, recorded intracellularly in the hippocampus of awake, nonimmobilized rabbits in three states, control and during the systemic administration of eserine and scopolamine, was carried out. Neurons of the hippocampus were additionally tested in a similar manner following the chronic basal undercutting of the septum, removing stem influences. The cholinergic substances regulate the number of neurons of the hippocampus having theta modulation and the degree of its stability, but do not influence its frequency. When the cholinergic theta rhythm is activated, regularization of the activity takes place with the suppression of delta modulation and of “complex spikes”; its blockade is accompanied by the opposite changes. Both substances stably alter the level of the baseline frequency of discharges of the majority of neurons, although the total average frequency remains constant. Regression analysis shows the predominance of a decrease in the activity in highfrequency (> 25 spikes/sec) and an increase in the lowf-requency (< 25 spikes/sec) neurons during the effect of both substances. The constancy of the total average frequency and the unidirectionality of the shifts in the level of discharges of the neurons during the intensification (eserine) and blockade (scopolamine) of the cholinergic component of the theta rhythm points to the fact that the cholinergic septal input directly influences mainly the structure but not the level of the activity of the hippocampal neurons.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
D. P. Artemenko, “Participation of neurons of the hippocampus in the generation of theta waves,”Neirofiziologiya,4, No. 5, 531–539 (1972).
O. S. Vinogradova,The Hippocampus and Memory [in Russian], Nauka, Moscow (1975).
O. S. Vinogradova, E. S. Brazhnik, V. F. Kichigina, and V. S. Stafekhina, “Theta-modulation of neurons of the hippocampus of the rabbit and its interrelationship with other indices of spontaneous and evoked activity,”Zhurn. Vyssh. Nervn. Deyat.,42, No. 1, 95–111 (1992).
B. I. Kotlyar, O. B. Zubova, and N. O. Timofeeva, “Electrophysiological correlates of behavioral reactions,”Biol. Nauki, No. 11, 38–42 (1969).
G. I. Shul'gina, A. V. Korinevskii, and A. Kh. Lyapkusova, “An increase of orderliness of neuronal activity of the new cortex and hippocampus against the background of EEG activation,”Zhurn. Vyssh. Nervn. Deyat.,22, No. 1, 116–125 (1972).
A. Alonso and E. Garcia-Austt, “Neuronal sources of theta rhythm in the entorhinal cortex of the rat. 1. Laminar distribution of theta field potentials,”Exptl Brain Res.,67, No. 3, 493–501 (1987).
L. S. Bernardo and D. A. Prince, “Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells,”Brain Res.,249, No. 2, 333–344 (1982).
D. K. Bilkey and G. V. Goddard, “Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneuron,”Brain Res.,361, No. 1/2, 99–106 (1985).
B. H. Bland, M. G. Seto, B. R. Sinclair, and S. M. Fraser, “The pharmacology of hippocampal theta cells: evidence that the sensory processing correlate is cholinergic,”Brain Res.,299, No. 1, 121–131 (1984).
S. K. Bland and B. H. Bland, “Medial septal modulation of hippocampal theta cells discharges,”Brain Res.,375, No. 1, 102–116 (1986).
J. Brankack and G. Buzsaki, “Hippocampal responses evoked by tooth pulp and acoustic stimulation: depth profiles and effect of behavior,”Brain Res.,378, No. 2, 303–314 (1986).
E. S. Brazhnik and O. S. Vinogradova, “Control of the neuronal rhythmic bursts in the septal pacemaker of thetarhythm: effects of anaesthetic and anticholinergic drugs,”Brain Res.,380, No. 1, 94–106 (1986).
G. Buzsaki, L. W. S. Leung, and C. H. Vanderwolf, “Cellular bases of hippocampal EEG in the behaving rat,”Brain Res. Rev.,6, No. 2, 139–171 (1983).
A. E. Cole and R. A. Nicoll, “The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells,”Brain Res.,305, No. 2, 283–290 (1984).
J. C. Eccles, “Mammalian systems for storing and retrieving information,” in:Cellular Mechanisms of Conditioning and Behavioral Plasticity, C. D. Woody, et al. (eds.), Plenum Press, New York; London (1988), pp. 289–302.
S. E. Fox and J. B. Ranck, “Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats,”Exptl Neurol.,49, No. 3, 299–313 (1975).
E. S. Fox, “Membrane potential and impedance changes in hippocampal pyramidal cells during theta rhythm,”Exptl Brain Res.,77, No. 2, 283–294 (1989).
J. Fujita and T. Sato, “Intracellular records from hippocampal pyramidal cells in rabbit during theta-rhythm activity,”J. Neurophysiol.,27, No. 6, 1011–1026 (1964).
M. Gabriel and S. E. Saltwick, “Rhythmic theta-like unit activity of the hippocampal formation during acquisition and performance of avoidance behavior in rabbits,”Physiol. Behav.,24, No. 2, 303–312 (1980).
J. D. Green, D. S. Maxwell, W. J. Schindler, and C. Stumpf, “Rabbit EEG ‘theta’ rhythm: its anatomical source and relation to activity in single neuron,”J. Neurophysiol.,23, No. 4, 403–420 (1960).
Y. J. Greenstein, C. Pavlides, and J. Winson, “Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity,”Brain Res.,438, No. 1/2, 331–334 (1988).
J. J. Hagan and R. G. M. Morris, “The cholinergic hypothesis of memory: A review of animal experiments,” in:Handbook of Psychopharmacology, Vol. 20, L. L. Iversen, S. D. Iversen, and S. H. Snyder (eds.), Plenum Press, New York; London (1988), pp. 237–324.
O. Herreras, J. M. Solis, A. S. Herranz, R. Martin del Rio, et al., “Sensory modulation of hippocampal transmission. II. Evidence for a cholinergic locus of inhibition in the Shaffer-CA1 synapse,”Brain Res.,461, No. 2, 303–313 (1988).
A. Nunez, W. Buno, and E. Garcia-Austt, “Slow spikes in CA3 neurons of the hippocampus of the rat,”Trab. Inst. Cajal.,75, Suppl., 303–313 (1988).
A. Nunez, E. Garcia-Austt, and W. Buno, “Synaptic contributions to theta rhythm genesis in rat CA1-CA3 hippocampal neurons in vivo,”Brain Res.,533, No. 1, 176–179 (1990).
D. S. Olton, “Dementia: animal models of the cognitive impairments following damage to the basal forebrain cholinergic system,”Brain Res. Bull.,25, No. 3, 499–502 (1990).
K. H. Pribram, “The hippocampal system and recombinant processing,” in:The Hippocampus, Vol. 4, R. L. Isaacson and K. H. Pribram (eds.), Plenum Press, New York (1986), pp. 329–370.
E. T. Rolls, “Functions of neuronal networks in the hippocampus and neocortex in memory,” in:Neuronal Models of Plasticity, J. H. Byrne and W. O. Berry (eds.), Acad. Press, San Diego (1988), pp. 240–265.
R. S. Sainsbury, A. Heynen, and C. P. Montoya, “Behavioral correlates of hippocampal type 2 theta in the rat,”Physiol. Behav.,39, No. 4, 513–520 (1987).
L. R. Squire, A. P. Shimamura, and D. G. Amaral, “Memory and the hippocampus,” in:Neuronal Models of Plasticity, J. H. Byrne and W. O. Berry (eds.), Acad. Press, New York (1988), pp. 208–239.
R. P. Vertes, “Brainstem modulation of the hippocampus. Anatomy, physiology, and significance,” in:The Hippocampus, Vol. 4, R. L. Isaacson and K. H. Pribram (eds.), Plenum Press, New York (1986), pp. 41–75.
Author information
Authors and Affiliations
Additional information
Translated from Zhurnal Vysshei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 42, No. 5, pp. 944–954, September–October, 1992.
Rights and permissions
About this article
Cite this article
Brazhnik, E.S., Vinogradova, O.S., Stafekhina, V.S. et al. The spontaneous activity of hippocampal neurons during the modulation of theta rhythm by cholinergic substances. Neurosci Behav Physiol 23, 510–519 (1993). https://doi.org/10.1007/BF01153677
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01153677