Skip to main content

The Rhythmic Slow Activity (Theta) of the Limbic Cortex: An Oscillation in Search of a Function

  • Chapter
Induced Rhythms in the Brain

Part of the book series: Brain Dynamics ((BD))

Abstract

The existence of a prominent electroencephalogram (EEG) activity within the theta frequency range (4–7 Hz) in the hippocampus has been one of the most studied rhythmic activities of the mammalian brain. However, in lower mammals the hippocampal EEG has a wider frequency range and may extend from 3 to 4 Hz up to 10 to 12 Hz. Therefore, it has become current practice to name this EEG activity Rhythmic Slow Activity (RSA), in order to avoid the term theta rhythm, which does not cover the entire frequency range within which the hippocampal EEG of lower animals may fall. Several reviews on RSA, particularly in relation to behavior, have appeared (Ishizuka et al., 1990; Komisaruk, 1977; Lopes da Silva and Arnolds, 1978; Robinson, 1980; Vanderwolf and Robinson, 1981). Robinson (1980) discussed in particular the influence of species differences on RSA. In this respect, a controversial point is whether hippocampal RSA occurs also in humans. Single cases have been reported in which hippocampal RSA was observed in man (Giaquinto, 1973), but Halgren et al. (1985) were not able to find RSA in recordings in humans. However, using spectral analysis, Arnolds et al. (1980) were able to demonstrate RSA in the hippocampus of epileptic patients. This RSA presented a dominant low frequency (about 3–4 Hz), which was modulated with behavior in a similar way as in lower mammals.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Similar content being viewed by others

References

  • Anden NE, Dahlstrõm K, Fuxe K, Larsson K, Olson L, Ungerstedt U (1966): Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol Scand 67:313–326

    Article  Google Scholar 

  • Apostol G, Creutzfeldt OD (1974) Cross correlation between the activity of septal units and hippocampal EEG during arousal. Brain Res 67 : 65–75

    Article  Google Scholar 

  • Arezzo JC, Tenke CE, Vaughan HG Jr (1987): Movement-related potentials within the hippocampal formation of the monkey. Brain Res 401 : 79–86

    Article  Google Scholar 

  • Arnolds DEAT, Lopes da Silva FH, Aitink JW, Kamp A (1979a): Hippocampal EEG and behaviour. I. Hippocampal EEG correlates of gross motor behaviour in dog. Electroencephalogr Clin Neurophysiol 46 : 552–570

    Article  Google Scholar 

  • Arnolds DEAT, Lopes da Silva FH, Aitink JW, Kamp A (1979b): Hippocampal EEG and behaviour. II. Hippocampal EEG correlates of elementary motor acts in dog. Electroencephalogr Clin Neurophysiol 46 : 571–580

    Article  Google Scholar 

  • Arnolds DEAT, Lopes da Silva FH, Aitink JW, Kamp A (1979c): Hippocampal EEG and behaviour. III. Hippocampal EEG correlates of stimulus response tasks and of sexual behaviour in dog. Electroencephalogr Clin Neurophysiol 46 : 581–591

    Article  Google Scholar 

  • Arnolds DEAT, Lopes da Silva FH, Aitink JW, Kamp A, Boeijinga P (1980): The spectral properties of hippocampal EEG related to behavior in man. Electroencephal o gr Clin Neuro ph ysiol 50 : 324–328

    Article  Google Scholar 

  • Artemenko DP (1972): Role of hippocampal neurons in theta-wave generation. Neurophysiology 4: 531–539

    Google Scholar 

  • Assaf SY, JJ Miller (1978): The role of a raphe serotonin system in the control of septal unit activity and hippocampal desynchronization. Neuroscience 3: 539–550

    Article  Google Scholar 

  • Babloyantz A (1985): Evidence of chaotic dynamics of brain activity during the sleep cycle. Phys Lett (A) 111 : 152–156

    Article  Google Scholar 

  • Ben-Ari Y, Knrjevìc K, Reinhardt W, Ropert N (1981): Intracellular observations on disinhibitory action of acetylcholine in hippocampus. Neuroscience 6: 2445–2463

    Article  Google Scholar 

  • Bland BH, Andersen P, Ganes T (1975): Two generators of hippocampal theta activity in rabbits. Brain Res 94:199–218

    Article  Google Scholar 

  • Bland BH, Whishaw IQ (1976): Generators and topography of hippocampal theta (RSA) in the anaesthetized and freely moving rat. Brain Res 118 : 259–280

    Article  Google Scholar 

  • Boeijinga PH, Pennartz CMA, Lopes da Silva FH (1990): Paired-pulse facilitation in the nucleus accumbens following stimulation of subicular inputs in the rat. Neuroscience 35 : 301–311

    Article  Google Scholar 

  • Buzsaki, G, Eidelberg (1983) Phase relations of hippocampal projection cells and intereneurons to theta activity in the anesthetized rat. Brain Res. 226 : 334–339

    Article  Google Scholar 

  • Buzsàki G, Grastyàn E, Czopf J, Kellènyi L, Prohaska O (1981): Changes in neuronal transmission in the rat hippocampus during behavior. Brain Res 225 : 235–247

    Article  Google Scholar 

  • Buzsàki G, Leung LW-S, Vanderwolf CH (1983): Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev 6:139–171

    Article  Google Scholar 

  • Coenen AML (1975): Frequency analysis of rat hippocampal electrical activity. Physiol Behav 14:391–394

    Article  Google Scholar 

  • Crowne DP, Radcliffe D (1975): Some characteristics and functional relations of the electrical activity of the primate hippocampus and hypotheses of hippocampal function. In: Ihe Hippocampus, Isaacson RL, Pribam KH, eds. New York: Plenum Press, vol. 2, 185–203

    Chapter  Google Scholar 

  • Feenstra BWA, Holsheimer J (1979): Dipole-like neuronal sources of theta rhythm in dorsal hippocampus, dentate gyrus and cingulate cortex of the urethaneanesthetized rat. Electroencephalogr Clin Neurophysiol 47 : 532–538

    Article  Google Scholar 

  • Fuxe K, Johnsson G (1974): Further mapping of central 5-hydroxytryptamine neurons: studies with the neurotoxic dihydroxytryptamines. Adv Biochem Psychopharmacol 10:1–12

    Google Scholar 

  • Gaztelu JM, Buño W (1982) Septo-hippocampal relationships during EEG theta rhythm. Electroencephalogr clin Neurophysiol 54 : 375–387

    Article  Google Scholar 

  • Giaquinto S (1973): Sleep recordings from limbic structures in man. Confin Neurol 35:285–303

    Article  Google Scholar 

  • Green JD, Maxwell DS, Schindler WJ, Stumpf C (1960): Rabbit EEG “theta” rhythm: its anatomical source and relation to activity in single neurons. J Neurophysiol 23 : 403–420

    Google Scholar 

  • Green KF, Rawlins JNP (1979): Hippocampal theta in rats under urethane: generators and phase relations. Electroencephalogr Clin Neurophysiol 47 : 420–429

    Article  Google Scholar 

  • Greenstein YJ, Pavlides C, Winson J (1988): Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Res 438 : 331–334

    Article  Google Scholar 

  • Halgren E, Smith ME, Stapleton JM (1985): Hippocampal field-potentials evoked by repeated v.s. nonrepeated words. In: Electrical Activity of the Archicortex, Buszáki G, Vanderwolf CH, eds. Budapest: Akadémiai Kiadó, 67

    Google Scholar 

  • Halliwell JV, Adams PR (1982): Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250 : 71–92

    Article  Google Scholar 

  • Holsheimer J, Boer JJ, Lopes da Silva FH, Van Rotterdam A (1982): The douple dipole model of theta rhythm generation: simulation of laminar field potential profiles in dorsal hippocampus of the rat. Brain Res 235 : 31–50

    Article  Google Scholar 

  • Holsheimer J, Feenstra BWA, Nijkamp JM (1979): Distribution of field potentials and their relationships during theta and beta activity in the hippocampus and the overlying neocortex of the rat. In: Origin of Cerebral Field Potentials, Speckmann EJ, Caspers H, eds. Stuttgart: Thieme, pp 98–114

    Google Scholar 

  • Hounsgaard J (1978): Presynaptic inhibitory action of acetylcholine in area CA 1 of the hippocampus. Exp Neurol 62 : 787–797

    Article  Google Scholar 

  • Ishizuka N, Weber J, Amaral DG (1990): Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J Comp Neurol 295 : 580–623

    Article  Google Scholar 

  • Irmis F (1976): Hippocampal rhythmic slow theta activity in relation to certain muscle movements. Electroencephalogr Clin Neurophysiol 41 : 553

    Google Scholar 

  • Kamphuis W, Huisman E, Wadman WJ, Heizmann CW, Lopes da Silva FH (1989): Kindling induced changes in parvalbumin immunoreactivity in rat hippocampus and its relations to long-term decrease in GABA-immunoreactivity. Brain Res 479: 23–34

    Article  Google Scholar 

  • Komisaruk BR (1977): The role of rhythmical brain activity in sensorimotor integration. In: Progress in Psychobiology and Physiological Psychobiology, Sprague JM, Epstein AN, eds. New York Academic Press, vol. 7, pp. 55–90

    Google Scholar 

  • Konopacki J, Bland BH, MacIver MB, Roth SH (1987a): Cholinergic theta rhythm in transected hippocampal slices: independent CA 1 and dentate generators. Brain Res 436 : 217–222

    Article  Google Scholar 

  • Konopacki J, MacIver MB, Bland BH, Roth SH (1987b): Carbachol-induced EEG “theta” activity in hippocampal brain slices. Brain Res 405 : 196–198

    Article  Google Scholar 

  • Larson J, Lynch G (1988): Role of N-methyl-D-aspartate receptors in the induction of synaptic potentiation by burst stimulation patterned after the hippocampal theta rhythm. Brain Res 441:111–118

    Article  Google Scholar 

  • Larson J, Wong D, Lynch G (1986): Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368: 347–350

    Article  Google Scholar 

  • Leung L-WS (1980): Behavior-dependent evoked potentials in the hippocampal CA 1 region of the rat. I. Correlation with behavior and EEG . Brain Res 198 : 95–117

    Article  Google Scholar 

  • Leung L-WS (1984a): Model of gradual phase shift of theta rhythm in the rat. J. Neurophysiol 52 :1051–1065

    Google Scholar 

  • Leung L-WS (1984b): Pharmacology of theta phase shift in the hippocampal CA 1 region of freely moving rats. Electroencephalogr Clin Neurophysiol 58 :457–466

    Article  Google Scholar 

  • Leung L-WS, Lopes da Silva FH, Wadman WJ (1982): Spectral characteristics of the hippocampal EEG in the freely moving rat. Electroencephalogr Clin Neurophysiol 54 : 203–219

    Article  Google Scholar 

  • Llinás RR (1988): The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242 : 1654–1664

    Article  Google Scholar 

  • Lopes da Silvra, F.H. (1991): Neural mechanisms underlying brain waves: from neural membrane to networks, Electroencephalogr Clin Neurophysiol 79 : 81–93

    Article  Google Scholar 

  • Lopes da Silva FH, Arnolds DEAT (1978): Physiology of the hippocampus and related structures. Annu Rev Physiol 36:291–301

    Google Scholar 

  • Lopes da Silva FH, Arnolds DEAT, Neijt HC (1984): A functional link between the limbic cortex and ventral striatum: physiology of the subiculum-accumbens pathway. Exp Brain Res 55 :205–214

    Google Scholar 

  • Lopes da Silva FH, Kamp A (1969): Hippocampal theta frequency shifts and operant behaviour. Electroencephalogr Clin Neurophysiol 26 : 133–143

    Article  Google Scholar 

  • Lopes da Silva FH, van Rotterdam A, van Heuden E, Burr W (1976): Models of neuronal populations: The basic mechanisms of rhythmicity. In: Perspectives in Brain Research, Corner MA, Swaab DF, eds. Progr Brain Res 45 : 281–308

    Chapter  Google Scholar 

  • Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AHM (1990): Anatomical organisation and physiology of the limbic cortex. Physiol Rev 70:453–511.

    Google Scholar 

  • MacVicar BA, Dudek FE (1980): Local synaptic circuits in rat hippocampus: interactions between pyramidal cells. Brain Res 184 : 220–223

    Article  Google Scholar 

  • MacVicar BA, Tse FWY (1989): Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices. J. Physiol 417 : 197–212

    Google Scholar 

  • McLennan H, Miller JJ (1976): Frequency-related inhibitory mechanisms controlling rhythmical activity in the septal area. J Physiol (Lond) 254 : 827–841

    Google Scholar 

  • Miles R, Wong RKS (1986): Excitatory synaptic interactions between CA3 neurons in the guinea-pig hippocampus in vitro. J Physiol (Lond) 373 : 397–418

    Google Scholar 

  • Nuñez A, Garcia-Austt E, Buño W Jr (1987): Intracellular 0-rhythm generation in identified hippocampal pyramids. Brain Res 416 : 289–300

    Article  Google Scholar 

  • Paiva T, Lopes da Silva FH, Mollevanger W (1976): Modulating systems of hippocampal EEG. Electroencephalogr Clin Neurophysiol 40 : 470–480

    Article  Google Scholar 

  • Pavlides C, Greenstein YJ, Goudman M, Winson J (1988): Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439 : 383–387

    Article  Google Scholar 

  • Petsche H, Stumpf Ch, Gogolák G (1962): The significance of the rabbit’s septum as a relay station between the midbrain and the hippocampus. The contral of hippocampus arousal activity by septum cells. Electroencephalogr Clin Neurophysiol 14: 202–211

    Article  Google Scholar 

  • Pijn JPM (1990): Quantitative evaluation of EEG signals in epilepsy-nonlinear associations, time delays and nonlinear dynamics. Ph.D. Thesis, University of Amsterdam.

    Google Scholar 

  • Pijn, JP, van Nerveen, J, Noest A, Lopes da Silva FH (1991) Chaos or noise in EEG signals; dependence on state and brain site. Electroencephalogr Clin Neurophysiol 79:371–381

    Article  Google Scholar 

  • Rawlins JNP (1985): Associations across time: the hippocampus as a temporary memory store. Behav Brain Sci 8:479–496

    Article  Google Scholar 

  • Robinson TE (1980): Hippocampal rhythmic slow activity (RSA; theta): A critical analysis of selected studies and discussion of possible species-differences. Brain Res Rev 2 : 69–101

    Article  Google Scholar 

  • Rose GM, Dunwiddie TV (1986): Induction of hippocampal long-term potentiation using physiologically patterned stimulation. Neurosci Lett 69 : 244–248

    Article  Google Scholar 

  • Rudell AP, Fox SE, Ranck JB Jr (1980): Hippocampal excitability phase-locked to theta rhythm in waking rats. Exp Neurol 68 : 87–96

    Article  Google Scholar 

  • Sainsbury RS (1970): Hippocampal activity during natural behaviour in the guineapig. Physiol Behav 5:317–324

    Article  Google Scholar 

  • Steriade M, Gloor P, Llinás RR, Lopes da Silva FH, Mesulam M (1990): Basic mechanisms of cerebral rhythmic activities. Electroencephalogr Clin Neurophysiol 76 : 481–508

    Article  Google Scholar 

  • Traub RD, Miles R, Wong RKS (1989): Model of the origin of rhythmic population oscillations in the hippocampal slice. Science 243 :1319–1325.

    Article  Google Scholar 

  • Vanderwolf CH (1969): Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407–418

    Article  Google Scholar 

  • Vanderwolf CH (1975): Neocortical and hippocampal activation in relation to behav- ior: effects of atropine, eserine, phenothiazines and amphetamine. J Comp Physiol Psychol 88 : 300–323

    Article  Google Scholar 

  • Vanderwolf CH, Baker GB (1986): Evidence that serotonin mediates noncholinergic neocortical low voltage fast activity, non-cholinergic hippocampal rhytmical slow activity and contributes to intelligent behavior. Brain Res 374 : 342–356

    Article  Google Scholar 

  • Vanderwolf CH, Kramis R, Robinson TE (1978): Hippocampal electrical activity during waking behaviour and sleep: analyses using centrally acting drugs. In: Functions of the Septo-Hippocampal System, Ciba Foundation Symposium 58 (new series). Amsterdam: Excerpta Medica

    Google Scholar 

  • Vanderwolf CH, Leung L-WS (1983): Hippocampal rhythmical slow activity: a brief history and the effects of entorhinal lesions and phencyclindine. In: Neurobiology of the Hippocampus, Seifert W, ed. London: Academic Press, pp 275–302

    Google Scholar 

  • Vanderwolf CH, Leung L-WS, Cooley RK (1985a): Pathways through the cingulate, neo- and entorhinal cortices mediating atropine-resistant hippocampal rhythmical slow activity. Brain Res 347 : 58–73

    Article  Google Scholar 

  • Vanderwolf CH, Leung L-WS, Stewart DJ (1985b): Two afferent pathways mediating hippocampal rhythmical slow activity. In: Electrical Activity of the Archicortex, Buzsàki G, Vanderwolf CH, eds. Budapest: Akadémiai Kiadó, pp 47–66

    Google Scholar 

  • Vanderwolf CH, Robinson TE (1981): Reticulo-cortical activity and behavior: A critique of the arousal theory and a new synthesis. Behav Brain Sci 4: 459–514

    Article  Google Scholar 

  • Vinogradova OS, Brazhnik ES, Karanov AN, Zhadina SD (1980): Analysis of neuronal activity in rabbit’s septum with various conditions of deafferentiation. Brain Res 187:354–368

    Article  Google Scholar 

  • Whishaw IQ, Kolb B (1979): Neocortical and hippocampal EEG in rats during lateral hypothalamic lesion-induced hyperkinesia: relations to behavior and effects of atropine. Physiol Behav 22 : 1107–1113

    Article  Google Scholar 

  • Wilson CL, Motter BC, Lindsley DB (1976): Influences of hypothalamic stimulation upon septal and hippocampal electrical activity in the cat. Brain Res 107 : 55–68

    Article  Google Scholar 

  • Winson J (1974): Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr Clin Neurophysiol 36 : 291–301

    Article  Google Scholar 

  • Winson J (1976a): Hippocampal theta rhythm. I. Depth profiles in the curarized rat . Brain Res 103 : 57–70

    Article  Google Scholar 

  • Winson J (1976b): Hippocampal theta rhythm. II. Depth profiles in the freely moving rabbit. Brain Res 103 : 71–79

    Article  Google Scholar 

  • Winson J (1984): Neuronal transmission through the hippocampus: Dependence on behavioural state. In: Cortical Integration, Reinoso-Suárez F, Ajmone-Marsan C, eds. New York: Raven Press, p 131

    Google Scholar 

  • Winson J (1986): Behaviorally dependent neuronal gating in the hippocampus. In: The Hippocampus, Isaacson RL, Pribram KH, eds. New York: Plenum Press, vol. 4, pp 77–92

    Chapter  Google Scholar 

  • Winson J, Abzug C (1978a): Neuronal transmission through hippocampal pathways dependent on behavior. J Neurophysiol 41 : 716–732

    Google Scholar 

  • Winson J, Abzug C (1978b): Dependence upon behavior of neuronal transmission from perforant pathway through entorhinal cortex. Brain Res 147 : 422–427

    Article  Google Scholar 

  • Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AHM (1989): Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33 :161–253

    Article  Google Scholar 

  • Wong RKS, Traub RD (1983): Synchronized burst discharge in the disinhibited hippocampal slice. I. Initiation in the CA2-CA3 region. J Neurophysiol 49 : 442–458

    Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer Science+Business Media New York

About this chapter

Cite this chapter

da Silva, F.L. (1992). The Rhythmic Slow Activity (Theta) of the Limbic Cortex: An Oscillation in Search of a Function. In: Başar, E., Bullock, T.H. (eds) Induced Rhythms in the Brain. Brain Dynamics. Birkhäuser, Boston, MA. https://doi.org/10.1007/978-1-4757-1281-0_4

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-1281-0_4

  • Publisher Name: Birkhäuser, Boston, MA

  • Print ISBN: 978-1-4757-1283-4

  • Online ISBN: 978-1-4757-1281-0

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics