Mechanisms of the regulation and functional significance of the theta rhythm. Roles of serotonergic and noradrenergic systems

The evidence for the role of serotonergic and noradrenergic effects on the septohippocampal theta oscillations obtained by the author and her colleagues are reviewed. Analysis of neuronal activity in the medial septal area or hippocampus and hippocampal EEG simultaneously recorded in awake rabbits exposed to different kinds of brainstem influences led to the following conclusions. 1. Serotonergic median raphe nucleus and noradrenergic locus ceruleus act as functional antagonists in theta regulation: the former structure restricts the theta rhythm generation, whereas the latter enhances this process. 2. Both transmitter systems control sensory reactions of septal and hippocampal neurons through up and down regulation of the theta activity. 3. When continuous theta activity induced by various experimental manipulations is recorded, responsiveness of septohippocampal neurons to sensory stimulation is strongly reduced. These findings provide support for the view that the theta oscillations act as an active filter in the information selection and registration. Interaction of different transmitter systems in the theta rhythm control as well as attention and memory is discussed.     

Simulation of the hippocampal theta rhythm

Centre of Theoretical and Computational Neuroscience, University of Plymouth, UK Basing on the hypothesis about the mechanisms of the theta rhythm generation, the article presents mathematical and computational models of theta activity in the hippocampus. The problem of the theta rhythm modeling is nontrivial because the slow theta oscillations (about 5 Hz) should be generated by a neural system composed of frequently firing neural populations. We studied a model of neural pacemakers in the septum. In this model, the pacemaker follows the frequency of the external signal if this frequency does not deviate too far from the natural frequency of the pacemaker, otherwise the pacemaker returns to the frequency of its own oscillations. These results are in agreement with the experimental records of medial septum neurons. Our model of the septal pacemaker of the theta rhythm is based on the hypothesis that the hippocampal theta appears as a result of the influence of the assemblies of neurons in the medial septum which are under control of pacemaker neurons. Though the model of the pacemaker satisfies many experimental facts, the synchronization of activity in different neural assemblies of the model is not as strong as it should be. Another model of the theta generation is based on the anatomical data about the existence of the inhibitory GABAergic loop between the medial septum and the hippocampus. This model shows stable oscillations at the frequency of the theta rhythm in a broad range of parameter values. It also provides explanation to the experimental data about the variation of the frequency and the amplitude of the theta rhythm under different external stimulations of the system. The role of the theta rhythm for information processing in the hippocampus is discussed.     

How do glutamatergic and GABAergic cells contribute to synchronization in the medial septum?

The medial septum-diagonal band (MSDB) complex is considered as a pacemaker for the hippocampal theta rhythm. Identification of the different cell types, their electro-physiological properties and their possible function in the generation of a synchronized activity in the MSDB is a hot topic. A recent electro-physiological study showed the presence of two antiphasically firing populations of parvalbumin containing GABAergic neurons in the MSDB. Other papers described a network of cluster-firing glutamatergic neurons, which is able to generate synchronized activity in the MSDB. We propose two different computer models for the generation of synchronized population theta oscillation in the MSDB and compare their properties. In the first model GABAergic neurons are intrinsically theta periodic cluster-firing cells; while in the second model GABAergic cells are fast-firing cells and receive periodic input from local glutamatergic neurons simulated as cluster-firing cells. Using computer simulations we show that the GABAergic neurons in both models are capable of generating antiphasic theta periodic population oscillation relying on local, septal mechanisms. In the first model antiphasic theta synchrony could emerge if GABAergic neurons form two populations preferentially innervate each other. In the second model in-phase synchronization of glutamatergic neurons does not require specific network structure, and the network of these cells are able to act as a theta pacemaker for the local fast-firing GABAergic circuit. Our simulations also suggest that neurons being non-cluster-firing in vitro might exhibit clustering properties when connected into a network in vivo. Action Editor: David Golomb     

Role of septal and entorhinal inputs in the generation of hippocampal electrical activity in the cat sleep-wake cycle

The effects of septal lesion and entorhinal cortex section on hippocampal electrical activity during the cat sleep-wake cycle were investigated in chronic experiments. The medial portion of the septum only was found to participate in generation of this activity. Complete suppression of hippocampal theta rhythm during active wakefulness and paradoxical sleep were the main effects of septal lesion. In slow-wave sleep, the effects of septal lesion manifested in a slight attenuation of the intensity of the dominant frequency (of 1 Hz). Widespread septal lesion does not add to the changes occurring when the medial portion of the septum is so isolated. Section of the entorhinal cortex produces a sharp increase in hippocampal theta rhythm during waking and paradoxical sleep. Clearcut attenuation of delta and subdelta rhythm intensities were observed in slowwave sleep. It is postulated that under normal conditions hippocampal entorhinal input exerts a modulating effect on the genesis of hippocampal theta rhythm.I. S. Beritashvili Institute of Physiology, Academy of Sciences of the Georgian SSR, Tbilisi. Translated from Neirofiziologiya, Vol. 19, No. 5, pp. 622–630, September–October, 1987.     

Neuronal septal activity during hippocampal seizure discharges generation in acute model of epilepsy

The activity of the neurones of the medial septal region (MS) and the hippocampal EEG in control and during the appearance of seizure discharges provoked by electrical stimulation of the perforant path were investigated in the awake rabbit. During afterdischarge generation in the hippocampus the dense neuronal bursts separated by periods of inhibition were recorded in the MS. In one group of neurons the bursts of spikes coincided with the discharges in the hippocampus, in other group-occured during inhibitory periods. When the afterdischarge stopped, in the septal neurons with theta activity the disruption of theta pattern was recorded, which have been correlated with the occurrence of low amplitude high frequency (20-25 Hz) waves in the hippocampal EEG. As a rule, the neuronal activivity of the MS recovered much quickly than EEG of the hippocampus; in some cases the increasing of the theta regularity was observed. The definite accordance of the electrical activity of the hippocampus and MS during seizure discharges suggests that the septohippocampal system operate as integral nervous circuit in these conditions. Diverse in the temporal interrelations between the discharges of MS neurones and ictal discharges in the hippocampus in the different cells possible indicate that various groups of the septal nervous elements have different participation in the seizure development. Appearance of the high frequency bursts in the MS is a possible "precursor" of the seizure onsets.     

Dopaminergic regulation of theta activity of septohippocampal neuron in the awake rabbit

The effects of dopamine reuptake blocker nomifensine and nonselective antagonist of dopamine receptors haloperidol on the theta rhythmicity of the medial septal neurons and hippocampal EEG were investigated in the rabbit. Bilateral intracerebroventricular infusion of nomifensine (9 micrograms in each ventriculus) produced an increase in both the rate of firing and the theta modulation of medial septal neurons; the theta power of the hippocampal EEG also augmented. The degree of neuronal theta stability (time constant of damping, tao theta) significantly increased. The frequency of rhythmic bursts in the neuronal firing also substantially elevated. The amplitude, regularity and frequency of theta waves in the hippocampal EEG also increased. The antagonist haloperidol (12.5 mg) caused the opposite effect. The theta activity of medial septal neurons and the theta power of the hippocampal EEG decreased after haloperidol injection. Theta rhythmicity of septal neurons significantly diminished, the rate of rhythmic bursts in the neuronal firing also decreased, although not substantially. The theta amplitude and regularity in the hippocampal EEG also decreased. Effects of both drugs built up rapidly and then gradually attenuated. Nomifensine infusion against the background of exposure to haloperidol provoked neither increasing neuronal firing rate, nor elevating theta activity. These finding suggest that dopaminergic system produces activation of the septohippocampal system in situations that require selective attention to functionally important information.     

Network effects of glutamate on neuronal activity in the medial septum/diagonal band complex in vitro

Inter-neuronal interactions within the medial septum/diagonal band complex (MSDB) are of great interest as this region is believed to be the hippocampal theta rhythm pacemaker. However, the role of glutamatergic system in functioning of the septal cells is yet unclear. Here, we demonstrate for the first time the effects of glutamate in physiological concentration (1 microM) on the MSDB neuronal spontaneous and evoked activities in vitro. These effects (activation of 70% and inhibition of 30% of responsive neurons) differed in pacemaker and non-pacemaker cells. Pacemaker cells were always activated under glutamate, whereas non-pacemaker neurons could be either activated or inhibited. Indeed, in the burst pacemakers, glutamate increased the frequency of rhythmic activity. In a total MSDB neuron population, in 30% of neurons glutamate applications modified responses to the electrical stimulation by unifying the temporal parameters of neuron responses. Along with the increase in the theta-burst frequency, this indicates that the glutamatergic system is involved in the process ofintraseptal synchronization. Obtained data shed light on the role ofglutamatergic system in septal neuron interactions and broaden our understanding of theta oscillation mechanisms in the septo-hippocampal system.     

Sensory reactions of hippocampal neurons in rabbit during functional suppression of theta rythm- controlling structures

Responses to sensory stimuli were analyzed in hippocampal CA1 neurons of unanesthetized rabbits in chronic experiments before and after reversible functional blockade of the median raphe nucleus (MR) and medial septal area (MS-DB) by local microinjections of anesthetic lidocaine. The MR blockade, which resulted in an enhancement of theta-modulation of the background activity of the hippocampal neurons, was followed by a depression of sensory responsiveness (only 46.7% of the neurons reactive before the blockade retained their responses). Reactions of all types were blocked, diminished, or inverted, but inhibitory responses were affected most severely. Lidocaine injection into the MS-DB, which blocked also all brain stem afferents ascending to the hippocampus via the MS-DB input, resulted in the total absence of theta-modulation; however, responsiveness to sensory stimuli remained relatively high (76.7% of the responses were preserved); on-effects were especially resistant to the MS-DB blockade. Comparison of evoked activity in two conditions of continuous theta rhythm generation (physostigmine injection and MR blockade) revealed striking similarities. This suggests that the theta-suppressing influence of the MR (presumably serotonergic) is primarily actualized through the control of cholinergic septo-hippocampal theta-generating mechanism. The results provide support for the view that the theta-rhythm acts like an active filter in information processing performed by hippocampal neurons.     

Artificial Theta Stimulation Impairs Encoding of Contextual Fear Memory

Several experiments have demonstrated an intimate relationship between hippocampal theta rhythm (4–12 Hz) and memory. Lesioning the medial septum or fimbria-fornix, a fiber track connecting the hippocampus and the medial septum, abolishes the theta rhythm and results in a severe impairment in declarative memory. To assess whether there is a causal relationship between hippocampal theta and memory formation we investigated whether restoration of hippocampal theta by electrical stimulation during the encoding phase also restores fimbria-fornix lesion induced memory deficit in rats in the fear conditioning paradigm. Male Wistar rats underwent sham or fimbria-fornix lesion operation. Stimulation electrodes were implanted in the ventral hippocampal commissure and recording electrodes in the septal hippocampus. Artificial theta stimulation of 8 Hz was delivered during 3-min free exploration of the test cage in half of the rats before aversive conditioning with three foot shocks during 2 min. Memory was assessed by total freezing time in the same environment 24 h and 28 h after fear conditioning, and in an intervening test session in a different context. As expected, fimbria-fornix lesion impaired fear memory and dramatically attenuated hippocampal theta power. Artificial theta stimulation produced continuous theta oscillations that were almost similar to endogenous theta rhythm in amplitude and frequency. However, contrary to our predictions, artificial theta stimulation impaired conditioned fear response in both sham and fimbria-fornix lesioned animals. These data suggest that restoration of theta oscillation per se is not sufficient to support memory encoding after fimbria-fornix lesion and that universal theta oscillation in the hippocampus with a fixed frequency may actually impair memory.     

Modulation of theta-activity in the septo-hippocampal system by the alpha-2-adrenoreceptor agonist clonidine

The influence of the alpha 2-adrenoreceptors agonist clonidine on the neuronal activity of the medial septal area (MS) and hippocampal EEG was studied in unanaesthetized rabbits. A slight and short-term decrease in the theta-rhythm modulation in the MS neuronal activity and/or EEG was revealed in 30.4% of tests after the bilateral intraventricular injection of a small dose of clonidine (0.5 microgram/5 microliters of water). On the contrary, a high dose of clonidine (5 micrograms/5 microliters) substantially enhanced the theta modulation in 100% of tests. The frequency of the theta bursts in the MS increased, on average, by 1.6 +/- 0.18 Hz (from 5.25 +/- 0.19 to 6.8 +/- 0.17 Hz). The regularity of the theta modulation became almost twice higher: the time constant of damping increased from 0.34 +/- 0.04 to 0.60 +/- 0.08 s. Increase in the neuronal activity in the MS produced by the high dose of clonidine was always accompanied by appearance of continuous stable theta waves in the EEG; the spectral power in the theta range increased, on average, by 480 +/- 98%. This strong effect arose suddenly but was relatively short-lasting (12 +/- 3.5 min) and usually abruptly terminated. It is concluded that the noradrenergic system has a double control over the theta oscillations through the alpha 2-adrenoreceptors agonist. In low concentrations the agonist clonidine acts on the high affinity inhibitory presynaptic autoreceptors reducing the noradrenaline release and suppressing the theta activity. In a high dose clonidine predominantly acts on postsynaptic (low affinity) adrenoreceptors substantially increasing the frequency and regularity of the theta bursts in the activity of septal neurons. Presumably, different types of alpha 2-adrenoreceptors participate in regulation of the theta oscillations in different functional states. It is suggested that the noradrenergic locus coeruleus is a functional synergist of the activating reticular formation participating in the urgent phasic activation of the septohippocampal system during the action of sudden strong stimuli.     

Membrane and network theta-rhythm generation in hippocampal slices

The hippocampal rhythms observed in vivo are the result of a complex interplay between cellular and synaptic properties within the hippocampus, and extra-hippocampal tonic as well as periodic inputs. For the stable rhythm to occur, the hippocampal circuitry should have the potential to oscillate at the specific frequencies. The in vitro studies revealed multiple mechanisms supporting the generation of the theta rhythm, which is the main operational mode of the hippocampus. In the hippocampus and related structures cellular membranes can oscillate at theta rhythm when they are depolarized to near-threshold membrane potentials; membranes are also adjusted to resonate with the external signal applied at theta frequency. Synaptically connected hippocampal network alone can generate theta rhythm when a necessary tonic excitation is provided. Finally, rhythmic inputs in theta range from the septum and entorhinal cortex have a propensity to synchronize oscillations in the whole hippocampal formation and associated structures to operate in a unified mode of activity. Based on the results obtained in slices and slice cultures, the present review shows this multilevel hierarchy, which serves to guarantee easy occurrence and reliable maintenance of the theta rhythm in the hippocampus.     

GABAergic contributions to gating, timing, and phase precession of hippocampal neuronal activity during theta oscillations

Successful spatial exploration requires gating, storage, and retrieval of spatial memories in the correct order. The hippocampus is known to play an important role in the temporal organization of spatial information. Temporally ordered spatial memories are encoded and retrieved by the firing rate and phase of hippocampal pyramidal cells and inhibitory interneurons with respect to ongoing network theta oscillations paced by intra- and extrahippocampal areas. Much is known about the anatomical, physiological, and molecular characteristics as well as the connectivity and synaptic properties of various cell types in the hippocampal microcircuits, but how these detailed properties of individual neurons give rise to temporal organization of spatial memories remains unclear. We present a model of the hippocampal CA1 microcircuit based on observed biophysical properties of pyramidal cells and six types of inhibitory interneurons: axo-axonic, basket, bistratistified, neurogliaform, ivy, and oriens lacunosum-moleculare cells. The model simulates a virtual rat running on a linear track. Excitatory transient inputs come from the entorhinal cortex (EC) and the CA3 Schaffer collaterals and impinge on both the pyramidal cells and inhibitory interneurons, whereas inhibitory inputs from the medial septum impinge only on the inhibitory interneurons. Dopamine operates as a gate-keeper modulating the spatial memory flow to the PC distal dendrites in a frequency-dependent manner. A mechanism for spike-timing-dependent plasticity in distal and proximal PC dendrites consisting of three calcium detectors, which responds to the instantaneous calcium level and its time course in the dendrite, is used to model the plasticity effects. The model simulates the timing of firing of different hippocampal cell types relative to theta oscillations, and proposes functional roles for the different classes of the hippocampal and septal inhibitory interneurons in the correct ordering of spatial memories as well as in the generation and maintenance of theta phase precession of pyramidal cells (place cells) in CA1. The model leads to a number of experimentally testable predictions that may lead to a better understanding of the biophysical computations in the hippocampus and medial septum.     

Prefrontal phase locking to hippocampal theta oscillations

The interactions between cortical and hippocampal circuits are critical for memory formation, yet their basic organization at the neuronal network level is not well understood. Here, we demonstrate that a significant portion of neurons in the medial prefrontal cortex of freely behaving rats are phase locked to the hippocampal theta rhythm. In addition, we show that prefrontal neurons phase lock best to theta oscillations delayed by approximately 50 ms and confirm this hippocampo-prefrontal directionality and timing at the level of correlations between single cells. Finally, we find that phase locking of prefrontal cells is predicted by the presence of significant correlations with hippocampal cells at positive delays up to 150 ms. The theta-entrained activity across cortico-hippocampal circuits described here may be important for gating information flow and guiding the plastic changes that are believed to underlie the storage of information across these networks.     

Effect of electrical stimulation of the septum on subicular neurons with different kinds of spontaneous activity in rabbits

The effect of electrical stimulation of the medial nucleus of the septum and of hippocampal area CA₁ on subicular neurons with three different types of spontaneous activity (with theta-modulation, with delta-modulation and complex spikes, and with irregular single-spike activity) was studied in unanesthetized rabbits by extracellular recording of unit activity. Cells with theta-activity were found to respond in a distinctive functional manner to stimulation of the medial nucleus of the septum: Their reactivity was higher but latent periods of their responses were much shorter than those of cells with delta-activity and irregular discharges. Stability of modulation of theta-cell activity increased both during and after stimulation of the medial septal nucleus. Electrical stimulation of hippocampal area CA₁, on the other hand, led to disappearance of rhythm modulation. Average response latencies of all three types of cells to stimulation of area CA₁ were equal. The results indicate special properties of the septal input to subicular cells with theta-modulation.Institute of Biological Physics, Academy of Sciences of the USSR, Pushchino-on-Oka. Translated from Neirofiziologiya, Vol. 17, No. 3, pp. 326–333, May–June, 1985.     

The theta modulation of rabbit hippocampal neurons and its correlation with other indices of spontaneous and evoked activity]

Reliability of the existing functional criteria for differentiation of pyramidal ("complex spike neurones") and inhibitory ("theta neurones") cells in the hippocampus of waking rabbit is evaluated on the basis of statistical analysis of neuronal spontaneous and evoked activity. The analysis shows, that the criteria of mean frequency, presence of theta modulation, neuronal behaviour in situations provoking EEG theta rhythm (e.g., excitation or inhibition during presentation of sensory stimuli), effects of medial septum and intrahippocampal stimulation do not permit reliable identification of the hippocampal neuronal types in the waking rabbit. The data on functional classification of the hippocampal neurones are discussed in connection with existing suggestions about their state in situations inducing theta rhythm generation.     

Sensory responses of neurons in the medial septal area to modulation of the theta-activity by alpha2-adrenergic receptor agonist clonidine

It was shown by us earlier that bilateral intracerebroventricular injection of alpha2-adrenoreceptor agonist clonidine produced a dose-dependent effect on theta oscillations in the septohippocampal system of awake rabbits. A relatively low dose of clonidine (0.5 microgram) attenuated and a high dose (5 micrograms) significantly enhanced the rhythmic activity. It was suggested that the effect of the low dose of clonidine is mediated by presynaptic alpha2-adrenoreceptors were as postsynaptic alpha2-adrenoreceptors. In this article sensory neuronal responses in the medial septal area (MS) were analyzed against the background of the theta activity modulation by different clonidine doses. Different effects of the low and high doses of the agonist were revealed. The low dose of clonidine (0.5 microgram in 5 microliters into each lateral ventricle) which produced a decrease in the theta activity resulted in attenuation of excitation and enhancement of inhibition, i.e., the number of activating effects significantly decreased and inhibitory responses were more frequent and distinct. The high dose of clonidine (5 micrograms in 5 microliters) which produced a sharp increase in the theta activity led to a significant decrease in the reactions of the MS cells to sensory stimuli (from 76.8% in the control to 45% under clonidine) independently on the initial reaction character. Persisted excitatory and inhibitory responses became less distinct than the initial ones except single excitatory reactions. The results suggest that alpha2-adrenoreceptors are involved in the control of the sensory reactivity of MS neurons. A sharp decrease in neuronal reactivity during stable rhythmical oscillations developing under the influence of high dose of clonidine confirm the role of the theta rhythm in the septohippocampal system as an active filter in information selection and registration.     

Phase precession through acceleration of local theta rhythm: a biophysical model for the interaction between place cells and local inhibitory neurons

Phase precession is one of the most well known examples within the temporal coding hypothesis. Here we present a biophysical spiking model for phase precession in hippocampal CA1 which focuses on the interaction between place cells and local inhibitory interneurons. The model's functional block is composed of a place cell (PC) connected with a local inhibitory cell (IC) which is modulated by the population theta rhythm. Both cells receive excitatory inputs from the entorhinal cortex (EC). These inputs are both theta modulated and space modulated. The dynamics of the two neuron types are described by integrate-and-fire models with conductance synapses, and the EC inputs are described using non-homogeneous Poisson processes. Phase precession in our model is caused by increased drive to specific PC/IC pairs when the animal is in their place field. The excitation increases the IC's firing rate, and this modulates the PC's firing rate such that both cells precess relative to theta. Our model implies that phase coding in place cells may not be independent from rate coding. The absence of restrictive connectivity constraints in this model predicts the generation of phase precession in any network with similar architecture and subject to a clocking rhythm, independently of the involvement in spatial tasks.     

Modulation of signal transmission by the septal neurons of the rabbit during action on the cholinergic system

The neurons of the medial septum-diagonal band complex (MS-DB) were examined extracellularly in chronic unanaesthetized rabbits. Low-frequency (3-21 Hz) electrical stimulation was applied to the medial forebrain bundle within the horizontal limb of DB. In a group of the MS-DB units with stable background theta bursts the typical response consisting of entrainment of the phase-locked theta cycles was changed neither by physostigmine, nor by cholinergic-blocking drugs (scopolamine and atropine). In major group of the MS-DB units (60%), physostigmine completely blocked effects of electrical stimulation. This occurred both in the units with entrainment of the theta cycles and in the units with the effects of primary suppression of activity or (to a lesser extent) with single-spike discharges following the repetitive stimuli up to high frequencies. The cholinergic-blocking drugs restored and sometimes increased the initial reactivity of the MS-DB units. It is suggested, that intraseptal cholinergic system exerts a powerful gating effect upon transmission of signals to the hippocampus, probably, by the mechanisms of presynaptic inhibition.     

Effect of electrocoagulation of the septum on the behavior and memory of the cat

Lesion effects of various areas of the septum on general behaviour, learning and memory were studied in cats. It appeared that electrocoagulation of the medial septum alone leading to the disappearance of the hippocampal theta rhythm does not result in the development of the septal syndrome signs; does not disturb the normal structure of the sleep-wakefulness cycle; does not delay the elaboration of instrumental alimentary reflexes (to approach two feeders) or their extinction, but does entirely disturb the delayed responses to conditioned stimuli. In cases when lesion involves also the lateral septum, it produces the development of all signs of the septal syndrome (hyperemotionality, hyperactivity, rage, hyperphagia, etc.), disturbance of the normal structure of the sleep-wakefulness cycle, delay of both the elaboration and extinction of instrumental alimentary reflexes, disturbance of pre-elaborated conditioned reactions with sound discrimination, entire disturbance of conditioned delayed responses. On the basis of these data, the specific significance of hippocampal theta-rhythm in the organization of learning and memory is rejected, and a more important role is attributed to the descending regulatory influence exerted by the hippocampus and other archipaleocortical structures on the activating and motivatiogenic structures of mesodiencephalon.     

Effect of transection of afferent pathways on evoked potentials,theta rhythm,and neuronal activity in the hippocampus

The effect of destruction of septo-hippocampal and subiculo-hippocampal connections on the electrical activity in the hippocampus was studied in tubocurarized rabbits. The theta rhythm and the so-called "intracellular theta rhythm" [7] were found to disappear on destruction of the septo-hippocampal connections, other consequences being the loss of neuronal capacity for responding to sciatic nerve stimulation, loss of neuronal inhibitory responses, and total or partial suppression of the negative phase of the evoked potential (EP). Destruction of subiculo-hippocampal connections entails a decrease in amplitude of the theta rhythm recorded from the hippocampal surface, retention of the "intracellular theta rhythm," and a slight decrease in amplitude of both EP phases. The number of neurons failing to respond to sciatic stimulation is increased; the character of cellular response remains unchanged. It is hypothesized that hyperpolarization of hippocampal pyramidal neurons may be responsible for generating the negative phase of the EP, and that this phase and the hippocampal theta rhythm may be of a common origin.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 2, No. 4, pp. 439–444, July–August, 1970.