Hippocampal electrical activity and voluntary movement in the rat

407

Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands

H1PPOCAMPAL

ELECTRICAL

ACTIVITY

VOLUNTARY

MOVEMENT

IN

THE

AND RAT 1

C. H . VANDERWOLF 2

Department of Psychology, McMaster University, Hamilton, Ont. (Canada) (Accepted for publication: August 14, 1968)

In the past decade a number of reviews and a symposium have dealt with the anatomy, electrophysiology and pharmacology of the hippocampal formation (Adey 1959; Green 1960, 1964; Passouant 1962: Stumpf 1965a; White 1965) but its function is not, as yet, fully understood. Ablation studies have suggested its role in memory and learning (Milner 1966); experiments in which hippocampal electrical activity has been monitored in the course of learning tests have led to a variety of hypotheses. It has been proposed that the rhythmical slow activity ("theta" rhythm) which is characteristic of the hippocampus is associated with the orienting reflex (Grasty4n et al. 1959) with approach behavior (Grasty4n et al. 1966), or with learning or attention (Adey 1967; Elazar and Adey 1967a, b). Other evidence has suggested that the "theta" rhythm may be related to motor activity (Vanderwolf and Heron 1964; Yokota and Fujimori 1964; Vanderwolf 1967). The following observations extend these studies and provide a partial description of the relations between spontaneous motor activity and hippocampal electrical activity in the rat. SUBJECTS AND PROCEDURE

The main results were obtained from eighteen adult (250-350 g) male hooded rats. Incomplete data were obtained from six additional rats. Three pairs of electrodes were implanted at various brain locations in each animal and fixed 1 This research was supported by a grant from the National Research Council (APB-I 18). z Now at Departments of Psychology and Physiology, University of Western Ontario, London, Canada.

in place with watch screws and dental cement. The brain structures sampled included the dorsal hippocampal formation, the medial thalamic and septal nuclei, and the neocortex. The electrodes consisted of two 0.010 in. diameter Nichrome wires insulated to within 0.5 mm of their tips (separated by 0.5-1.0 ram). The external parts of the electrodes were made from Winchester subminiature components. After a recovery period of 2 weeks or more, records were taken with a 6-channel Grass model IV electroencephalograph and correlated with different behaviors. Three channels were used to record the EEG. The remaining three channels were connected to a set of manually operated signal markers. The rats were placed in a partially screened box measuring 10 x 12 x 14 in. An observer (the author) sat close by, recording the rat's behavior by means of the signal markers without seeing the rat and the EEG record simultaneously. Daily recording sessions lasted about 1 h per rat. Records were taken during at least two sessions for all rats, and those yielding clear "theta" activity were observed during as many as 18 sessions. Since accurate observation could be sustained only for short periods, a session was interrupted by short breaks every few minutes, and not more than three sessions were run on any one day. After other observations had been completed, experiments on shock avoidance behavior were performed, using an apparatus which consisted of a 12× 12x 12 in. plywood box mounted on foam rubber blocks. A grid floor of light steel bars, placed I1.0 in. below the top of the box, could be electrified by means of a Harvard Electroenceph. clin. Neuraphysiol., 1969, 26 : 407-418

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E/ectroenceph, Him Neurophysiol., 1969, 26 : 407M-18

HIPPOCAMPAL ACTIVITY AND MOVEMENTS

inductorium driven by a 1.5 V dry cell. A plywood shelf, 2.5 in. wide, ran around the outside of the box 0.5 in. below the upper edge. Thus, a rat could jump out of the box, catch the raised edge with its forepaws, and pull itself up onto the outside shelf. A small accelerometer fixed to the outside shelf made it possible to record the vibrations produced by the rat walking inside or jumping out. A light tap on the box produced a response from the accelerometer within about l0 msec. RESULTS

1. Anatomical-EEG relations Fig. 1 illustrates the location of the electrode tips at 41 points in the brains of eighteen rats. The remaining 13 electrode placements in these animals were located at levels other than those shown, mostly in the neocortex. The points shown have been classified into three groups on the basis of the pattern of electrical activity predominating in each. Fast activity points ( " F " ) are those which yielded mostly 15-50 c/sec activity with little or no rhythmical slow activity. ( " F " points in the neocortex and thalamus did not yield rhythmical slow activity but the activity recorded there was not identical to the fast activity derived from the hippocampal formation.) Points labelled " T " yielded, at times, rhythmical slow activity (RSA) with frequencies usually between 6 and 12 c/sec with an amplitude often greater than 300 #V and minimal admixture of fast activity. The points labelled " M " yielded a pattern consisting of a mixture of the two preceding types. Examples of different patterns of activity are shown in Fig. 2 and 4. In the hippocampal formation (see Fig. 1) " F " or " M " activity was derived predominantly from the subiculum and dentate gyrus-CA4 area. Points which yielded the clearest RSA cluster in the interior of the hippocampal formation in or near the apical dendrite layer of CA1, CA2, and CA31. Electrodes placed in the medial thalamus yielded clear RSA in two cases, but the amplitude was less than in the hippo1 This confirms previous evidence that rhythmical slow activity is generated by the apical dendrites of hippocampal pyramidal cells (Green et al. 1960; Porter et al. 1964; Radulova~ki and Adey 1965).

409

campal formation. From the occipital cortex (3 electrodes), the sensori-motor cortex (9 electrodes), and the septal nuclei (1 electrode), no clear RSA was recorded at any time. 2. Behavioral-EEG relations Many of the relations to be described could be observed only when recording from points yielding clear large amplitude RSA with minimal admixture of fast activity. Except where otherwise specified, all the results to be described are based on the study of nine rats with hippocampal electrode placements yielding this EEG pattern. The small amplitude RSA derived from the medial thalamus in two additional rats showed the same relations to behavior as hippocampal RSA and a separate description has been omitted. Locomotion, freezing, head movements. Walking forward or turning, observed on over 2,000 occasions, was always accompanied by trains of RSA of an amplitude which varied from one occasion to another (200-600 #V). Walking backwards (62 occasions) and rearing up on the hind legs (283 occasions) were accompanied by the same type of hippocampal activity. At mixed activity sites ( " M " in Fig. 1) these behavior patterns occurred at times with clear RSA, at other times with little or no evidence of RSA. The neocortical records consisted of low voltage fast activity during all types of locomotion. During a period of exploration a rat would sometimes "freeze", becoming almost totally motionless, but remaining standing, sometimes on two legs. The eyelids were strongly retracted, in contrast with their half-closed position during relaxed wakefulness. The neocortical records consisted of low voltage fast activity while hippocampal records consisted of irregular slow activity (see Fig. 2). A motionless rat (either freezing or lying down) would frequently make a slight lateral or vertical movement of the head. About 9 0 ~ of 1500 such head movements were accompanied by a brief run of RSA in the hippocampus. RSA also accompanied isolated movements of a limb in the absence of simultaneous head movement (63 instances). The amplitude of the RSA accompanying such slight movements was only about 150-300/tV at sites where up to 700 #V would appear during walking or rearing. Further, Electroeneeph. clin. Neurophysiol., 1969, 26:407-418

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Fig. 2 Rat 11-66. Different behaviors as indicated. Derivations: occipital neocortex ("F" activity); hippocampal CA1 pyramids ("T" activity). Note: In CA1 pyramids, high voltage irregular activity during immobility, drinking, and biting fur on forelegs; high voltage, high frequency RSA during struggling; lower voltage, lower mean frequency RSA during isolated movements of head. RSA also present during change of posture while biting fur but not during pause in biting. Small amplitude irregular activity in hippocampus after sudden awakening. In neocortex, low voltage fast activity at all times except during drowsiness (E). Spiky neocortical record in F is EMG artifact from jaw muscles. Calibrations: 100 #V and 1 sec.

the mean frequency o f such R S A is o n l y 6-7 c/sec c o m p a r e d with 8-9 c/sec d u r i n g large-scale m o v e m e n t . These r e l a t i o n s were very clear in all rats, b u t a m o r e detailed analysis o f the frequency o f the R S A a c c o m p a n y i n g different

behaviors was m a d e in two cases (see Fig. 3). D u r i n g m o v e m e n t s o f the vibrissae w i t h o u t a c c o m p a n y i n g head m o v e m e n t s (sniffing) o r d u r i n g j a w m o v e m e n t s (chewing o r c h a m p i n g w i t h o u t a n y t h i n g in the m o u t h ) in an otherwise Electroeneeph. elin. Neurophysiol., 1969, 26:407-418

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Fig. 3 Frequency distributions of well-defined RSA in two rats during 4 different behaviors. Mean frequencies for walking and rearing, 8.0 8.3 c/sec; for head movements and manipulatory movements, 6.6-7.1 c,,'sec. Modal frequency is 7.5 c"sec for all 4 behaviors. Measurements based on 11,139 waves, accompanying about 1,200 different acts.

motionless rat, the hippocampal record remained irregular. RSA did not appear. Grooming behavior. Grooming behavior in the rat comprises a variety of motor patterns, each consisting of a repetitive series of movements of the head, limbs, jaws or tongue superimposed upon a stably maintained posture. Thus, a rat may sit up in a low crouch and wash its mouth and vibrissae with a repetitive bilaterally symmetrical movement of both forepaws. A moment later a more vertical posture may be assumed as the rat bites at the fur on its side. The performance of all such motor patterns was accompanied by irregular activity in the hippocampus. However, the shift of posture occurring at the initiation of a particular grooming pattern, or during the transition from one pattern to another, was usually accompanied by RSA (see Fig. 2). Over 90% of 576 occasions (in 4 rats) on which postural shifts during grooming

411

were observed, were accompanied by clear RSA in the hippocampus. This activity was variable in appearance, but tended to have a lower frequency and smaller amplitude than the RSA accompanying gross motor activity such as walking. Hippocampal sites from which mixtures of fast activity and RSA were recorded usually did not yield RSA during the postural shifts occurring during grooming (see also Klingberg and Pickenhain 1965). Two kinds of change in grooming pattern were not usually accompanied by well developed RSA. One was the shift from washing the mouth and vibrissae to washing the top of the head and ears. The other such instance occurred during a bout of scratching when the rats would pause briefly to lick the digits of the active paw. Feeding behavior. Feeding was studied after 20 h of food deprivation during 3-5 daily sessions in seven rats with " T " electrode placements. (Other rats were observed for 1-2 days only.) A rat would advance toward a food pellet, pick it up in the mouth with a quick movement, then turn and run to the back of the cage. All these movements were always accompanied by a train of RSA which continued until the rat stopped moving. Manipulation of the food pellet with the mouth and forepaws occurred each time a piece was bitten off. This behavior was accompanied by a short run of RSA much like that accompanying an isolated head orpaw movement in a motionless rat (see Fig. 3, 4). Chewing was accompanied by irregular activity in the hippocampus. Manipulation of large food pellets, requiring movement of the entire forelimb, appeared to be accompanied by better developed RSA than manipulation of small food pellets which could be rotated by movements confined largely to the wrist and digits. Thus, as a food pellet was eaten, the RSA accompanying its manipulation tended to diminish progressively or disappear. This change was probably not due to satiation or a habituation process since if the rats were given a pea-sized bit of food at the start of a recording session, RSA was slight at the outset. At mixed ( " M " ) activity sites the RSA accompanying the manipulation of food could not usually be detected, the record consisting mainly of irregular fast activity. Electroenceph. clin. Neurophysiol., 1969, 26:407-418

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Fig. 4 Rat 1-67. Different behaviors as indicated. Large food pellet, about 1.0 in. long; small food pellet, pea-sized. Derivations: From above downwards, CA2 or CA3 pyramids ("T" activity); dentate-CA4 area ("F" activity); dentate-CA4 area ("F" activity). Note: In pyramidal layer, clear RSA during handling of large food pellet, little or no RSA during handling of small food pellet, high voltage, high frequency RSA during walking, irregular activity during chewing, and face-washing; in dentate-CA4 area, little evidence of RSA at any time. Calibrations: 100/~V; 1 sec.

A p p r o a c h to water and turning away after drinking were always accompanied by RSA. Lapping water with the tongue was accompanied by an irregular hippocampal record (see Fig. 2). Arousal, attention and sleep. The movements

involved in lying down, getting up, or shifting b o d y posture slightly while lying down, were all accompanied by R S A (generally o f smaller amplitude and lower mean frequency than that a c c o m p a n y i n g more vigorous movements).

Electroenceph. clin. Neurophysiol., 1969, 26:407-418

l

HIPPOCAMPAL ACTIVITY AND MOVEMENTS

When drowsy or sleeping rats awakened (spontaneously or by the experimenter) the hippocampal records often assumed a pattern of small amplitude fast activity somewhat like the pattern seen in the neocortex (see Fig. 2) but if the rats began to move about, RSA appeared 1. An intense arousal reaction, as demonstrated by neocortical activation, was not sufficient, in itself, to produce hippocampal RSA: this appeared to require voluntary movement or preparation for it (see below). At times when the rats appeared to be closely attentive to environmental stimuli, RSA would appear only if certain types of movement were also performed. For example, if a rat was engaged in a repetitive behavior such as face-washing or lapping water, mild sensory stimuli would produce a momentary cessation of the ongoing motor activity. Such short pauses in the ongoing behavior without visible movement resulted in no particular change in the irregular pattern of hippocampal activity on about 75 ~ of the 282 occurrences observed in four rats (see Fig. 2). Some degree of regularization appeared on the remaining 2 5 ~ . If visible movement occurred (raising the head, lowering the forepaws slightly, etc.) RSA appeared on about 90 ~ of the 89 such occasions observed. "Paradoxical" sleep was observed in three rats. This state was characterized by a reduction of muscle tone, twitching of the vibrissae, slight limb movements, and hippocampal RSA with an amplitude and frequency much like the RSA accompanying vigorous walking or rearing in the alert state. The most obvious difference between the two situations was that during this phase of sleep RSA tended to occur in longer trains. Other behaviors. Climbing behavior was elicited by placing a rat vertically on the side of a board clamped vertically to a testing table. When so placed, with the weight supported mainly by the forepaws, the rats usually pulled themselves up on the table in a second or less. Well-developed RSA always appeared as the rats climbed up, 1 These observations may account for previous discrepancies (Grastyan et al. 1959; Radulovaf~ki and Adey 1965) concerning whether a completely novel stimulus will elicit RSA or not. The different results obtained may have been related to the presence or absence of movements.

413

but the record only showed irregular activity if they remained hanging motionless on the board for several seconds. Struggling movements, elicited by handling a rat, were accompanied by high frequency large amplitude RSA. RSA disappeared if a rat stopped struggling for several seconds while continuing to be held (see Fig. 2). Struggling movements of small extent, such as attempts to jerk free a forepaw held between the experimenter's thumb and finger, tended to be accompanied by small amplitude RSA. Avoidance behavior. Rats were trained on a shock avoidance task to provide information on : (a) the relation between frequency of RSA and the time of occurrence of a motor act; and (b) the possible effects of extended training on the appearance of RSA. Observations were made on four rats. Two of these had " T " placements in the hippocampus, one had a " T " placement in the medial thalamus, and one had an "M'" placement in the hippocampus. Training was begun by allowing a rat 5 rain to explore the apparatus. None of the rats climbed or jumped out during this period. Next, the rat was picked up and replaced in the apparatus, and 15 sec later intermittent shocks were applied until it jumped out. After receiving 3-5 shock trials (at 30 sec intervals) all four rats began to jump out of the box before shock was applied. Recording leads were attached after 10 trials and an additional 20 trials were administered while records were taken. After 8-11 days of additional avoidance training (30 trials/day) a second recording session was run.

After prolonged training, the act of jumping out of the apparatus became stereotyped; the movements exhibited were much the same on one trial as on another. During intertrial periods the rats would sit motionless on the side of the box. Low voltage fast activity was usually present in the neocortex, accompanied by irregular activity in the hippocampus. The jump response was preceded by a period of immobility (except for slight movements of the head and tensing of the body) while the rat stood crouched with the forelegs off the floor. RSA was continuously present during this period, and also during the sudden thrust of the hind legs which propelled Electroenceph. elin. Neurophysiol., 1969, 2 6 : 4 0 7 - 4 1 8

414

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the rat to the edge of the box. The RSA had a frequency of 6-7 c/sec when it first appeared, but would increase regularly to a peak of 8-12 c/sec (usually 10 c/sec) just before the jump. RSA frequency declined rapidly as the rat assumed a motionless position on the edge of the box. Fig. 5 illustrates these frequency shifts in three rats. Data from the fourth rat ( " M " placement) are not included, because it exhibited RSA for a shorter period prior to the jump response than the other rats. Hippocampal electrical activity did not change in any obvious way during the course of the experiment. DISCUSSION

At least three distinguishable patterns of electrical activity can be recorded in or near the apical dendrite layer of the hippocampal pyramids of a waking rat. The patterns are: rhythmical slow activity (RSA) of varying frequency and amplitude, large amplitude irregular activity, and small amplitude irregular activity. Stumpf (1965b) has distinguished three analogous patterns of activity in the rabbit hippocampus. In an alert rat, the subiculum and

dentate gyrus-CA4 area produce mainly fast activity. These different patterns of hippocampal activity are associated with different classes of behavior. A prominent finding has been that "automatic" behaviors (licking, chewing, facewashing, etc.) are accompanied by irregular activity in the hippocampus. More voluntary types of movement (walking, manipulation, etc.) are accompanied by RSA. Related results have been reported in the dog where walking is accompanied by regular activity, and eating and defecation are accompanied by irregular activity in the hippocampus (Yoshii et al. 1966). Such findings suggest differences in the neural organization of automatic and voluntary movements. One of the fundamental concepts of Jackson (see Taylor 1958) was that different movement patterns could be ranged in a rough continuum from most automatic to most voluntary. Part of the difference between the two may be that the occurrence of many automatic movements is dependent on the presence of a particular motive state. For example, when someone "feels cold" shivering movements occur and cannot easily be suppressed. Shivering does not occur during the state of "feeling warm" and cannot then be made to occur by voluntary effort. A large class of somatic and autonomic activities including emotional expression, yawning, vomiting, etc., resemble this example in that they are difficult to suppress when the appropriate motive state is present and difficult or impossible to produce when it is absent. In contrast, the type of movement said to be "voluntary" can easily be controlled by any one of a number of different motive states. For example, walking can be brought into the service of food getting, attack, flight, reproduction, etc. The extent to which different components of behavior in the rat are voluntary in this sense is not known, but the fact that "cross-drive conditioning" is often difficult to obtain, especially in lower animals (Breland and Breland 1966), suggests that many movement patterns occur only in the presence of a limited number of motive states. For example, a hungry cow normally walks to graze and cannot, apparently, be taught to run to food since running is primarily a flight pattern. Electroenceph. clin. Neurophysiol., 1969, 26: 407-418

HIPPOCAMPAL ACTIVITY AND MOVEMENTS

Another way in which the organization of voluntary acts is different from the automatic acts studied here is that the sequence of movements is not fixed. Raising the head may be preceded or followed by any one of a large number of movements, but in an act such as chewing, a small number of movements follow one another in a stereotyped repetitive succession. Thus, the neural organization of a voluntary movement must be very complex compared to an automatic movement. Switching circuitry will be necessary to control voluntary movement patterns if they are to be connected with different drives on different occasions. This would be less important in the control of automatic movements. Further, if a number of movements are always made in the same serial order, as in many automatic movements, sequential control could be much simpler th,~,n when a few movements must be selected from a large number of possibilities, arranged in a sequence which can be varied from one occasion to another, and finally, triggered off (see Lashley 1951). The rhythmical activity produced by the hippocampus may be a reflection of the activity of some of the complex circuitry which appears necessary for voluntary movement. This is suggested primarily by the fact that voluntary types of movement are associated with RSA whereas automatic movements are not. Further, the pattern of hippocampal activity is similar during ordinary alert immobility and during the performance of automatic movements. This suggests that the patterning of such movements is determined largely by the lower levels of the nervous system while the higher levels remain inactive. Other evidence also suggests this. Local seizure activity produced by stimulation of the hippocampus of the cat did not interrupt ongoing lapping movements (drinking milk) but did prevent the occurrence of more voluntary acts such as an instrumental avoidance response (Flynn and Wasman 1960; Akert 1961). Another point concerning the behavioral correlates of hippocampal RSA is that it is associated with phasic voluntary motor activity and does not occur during the maintenance of a fixed posture even when this requires considerable muscular effort. This observation supports the view that central mechanisms concerned with

415

phasic movement are not identical with those controlling posture (Sherrington 1947; DennyBrown 1966). Bach and Magoun (1947) have shown that the mesencephalic reticular formation is more concerned with phasic than with tonic motor activity. This may be related to the fact that stimulation at reticular loci which facilitates phasic motor activity tends to produce RSA in the hippocampus. Stimulation at somato-motor inhibitory points produces irregular activity in the hippocampus (Yokota and Fujimori 1964). Paradoxical sleep presents an apparent exception to the relation between RSA and voluntary movement. During this state large amplitude, high frequency RSA was observed, but only very slight movements were made. However, current research indicates that there is a good deal of activity in cerebro-spinal pathways during paradoxical sleep, and that movement is largely prevented because the spinal motoneurones are simultaneously inhibited by other descending pathways (Pompeiano 1967). Therefore, it is quite possible that volitional mechanisms are active during paradoxical sleep even though gross movements do not occur. Hippocampal RSA varied in both amplitude and frequency but the two parameters were not clearly related. Product-moment correlations made between amplitude and period in small samples of waves in three rats turned out to be -0.30, - 0 . 0 7 and -0.19. It is possible that the amplitude of the RSA is related to the extent of the accompanying movement since it was generally found that vigorous large-scale movements were associated with larger amplitude RSA than lesser movements. The frequency of the RSA appears to be related to the temporal occurrence of a movement. In the shock avoidance experiment, the act of jumping was preceded by a steady increase in the frequency of the hippocampal activity, reaching a peak just prior to the occurrence of the jump. Frequency increases also precede many untrained movements. Similar results have been obtained by others (see Pickenhain and Klingberg 1967). Such frequency shifts may be due to increased activity in the brain-stem. Stimulation of the unspecific systems can produce RSA in the hippocampus, and the frequency of such activity is a function of the intensity of stimulaElectroenceph. olin. Neurophysiol., 1969, 26:an7-418

416

c. H. VANDERWOLF

tion (Sailer and Stumpf 1957; Yoshii et al. 1966). Further, destruction of the medial thalamus or the posterior hypothalamic-subthalanaic area reduces or prevents the appearance of RSA in the hippocampus (Eidelberg et al. 1959; Kawamura et al. 196l; Adey et al. 1962; Corazza and Parmeggiani 1963). These facts may be related to other work suggesting the existence of a movement triggering system whose operation is impaired following medial thalamic destruction (Vanderwolf 1962). It may be that when an animal prepares to perform a voluntary act, the level of activity in a brainstem system rises until a threshold (represented by hippocampal activity of about 10 c/sec in the present case) is reached and the act is performed. Medial thalamic lesions interfere with this process, but only to a slight degree; posterior hypothalamic-subthalamic area lesions have a more severe effect, amounting to akinesia (see Magoun 1950). The more ventral lesion also has the more severe effect on hippocampal activity (Kawamura et al. 1961). All these facts support the view that voluntary movement is initiated by a brain-stem mechanism (Penfield 1954). Other

theories

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Grastyfin et al. (1959) suggested that hippocampal RSA was an accompaniment of the orienting reflex of Parlor. This generalization appears too limited. RSA does accompany exploratory head movements, but it also accompanies movements which are not exploratory and do not involve the head; e.g., an isolated movement of one limb. The suggestion by Grastyfin et al. (1966) that hippocampal RSA is associated with approach behavior, whereas irregular activity is associated with withdrawal, is not supported by the present observations. Chewing food and lapping water were not accompanied by RSA. Startling a rat by tapping it on the snout with a pencil would produce a limited reflexive type of withdrawal which tended to be associated with irregular hippocampal activity (a few regular waves often appeared) but if the animal ran away or withdrew by backing up, clear runs of RSA always occurred. Further, brain-stem points where stimulation produces hippocampal RSA tend to be motivationally neutral in a self-stimulation test (Ito 1966).

However, in agreement with the hypotheses presented here, such points do facilitate phasic somato-motor activity (Yokota and Fujimori t964). It has been suggested frequently that hippocampal RSA is associated with attention, processing of afferent information, or more simply, with the alert state. The present results do not support such hypotheses. Behavior which is clearly indicative of attention, such as cessation of face-washing in response to a stimulus, is not usually associated with RSA unless movement occurs. Further, if attention to a signal is indicated by immobility in animals (dogs) trained to press a bar to avoid electric shock, RSA does not appear, although it appears clearly in association with the bar-pressing movements themselves (Dalton 1968). In some situations, low freque~lcy RSA may continue for considerable periods in the absence of visible movement. This is very common in the rabbit (Harper 1968). Possibly, low frequency RSA indicates that a motor response is "programmed" but the necessary triggering frequency is not reached and no movement occurs. The finding that phase relations and frequency distributions of hippocampal activity are altered during the course of learning (Adey 1962, 1967; Elazar and Adey 1967a) is compatible with the hypothesis that hippocampal RSA is related to attention or memory formation, but does not prove this. Training inevitably produces systematic changes in motor activity. According to the present results the different behaviors which occur will be accompanied by different patterns of hippocampal activity regardless of whether they occur spontaneously or as a result of training. It is possible that many of the changes in hippocampal activity which have been observed during the course of learning experiments are not directly related to the learning process itself, but are instead, a consequence of the fact that training changes the character of the motor performance. SUMMARY

Stainless steel macro-electrodes were chronically implanted in 24 adult male hooded rats. EEG recordings were taken from the hippocampal formation, diencephalon and neocortex Electroenceph. clin. Neurophysiol., 1969, 26:407 418

HIPPOCAMPAL ACTIVITY AND MOVEMENTS

and were correlated with observations of spontaneous or conditioned behavior. Trains of rhythmical 6-12 c/sec waves in the hippocampus and medial thalamus precede and accompany gross voluntary types of movement such as walking, rearing, jumping, etc. Behavioral immobility (in the alert state) and automatic movement patterns such as blinking, scratching, washing the face, licking or biting the fur, chewing food or lapping water are associated with irregular hippocampal activity. Small movements, such as shifts of posture or isolated movements of the head or limbs occurring during immobility, or during grooming or feeding behavior, are associated with rhythmical activity of reduced amplitude and lowered mean frequency. A shock avoidance response is preceded by an increase in wave frequency. Peak frequency is reached just before the occurrence of the motor response. It is suggested that rhythmical slow activity in the hippocampus and diencephalon are the electrical sign of activity in a forebrain mechanism which organizes or initiates higher (voluntary) motor acts. No support is found for previous suggestions that such waves are specifically related to generalized arousal, orienting responses, learning, attention or approach behavior. Rf~SUMI~ ACTIVITE t~LECTRIQUEHIPPOCAMPIQUEET MOUVEMENTVOLONTAIREDU RAT Des macro-61ectrodes d'acier inoxydable ont 6tO implantOes chroniquement chez vingt-quatre rats adultes m~les. Des tracOs EEG ont 6t6 recueillis au niveau de la formation hippocampique, du dienc6phale et du n4ocortex et ont 6t4 corr61ds aux observations du comportement spontan6 ou conditionn6. Des trains d'ondes rythmiques de 6-12 c/sec au niveau de l'hippocampe et du thalamus mOdian pr6c6dent et accompagnent des types de mouvements volontaires globaux tels que marcher, se dresser, sauter, etc. L'immobilit6 comportementale (en 6tat d'alerte) et les patterns de mouvements automatiques tels que le clignement, le grattage, le nettoyage du museau, le fait de 16cher ou de mordre sa fourrure, le fait de mficher de la nourriture ou de lapper de l'eau s'associent ~ une

417

activit6 hippocampique irr6guli6re. Les petits mouvements, tels que changements de posture ou mouvements isol6s de la t~te ou des membres survenant sur un fond d'immobilit6 ou pendant un comportement de toilette ou d'alimentation, sont associ6s & une activit6 rythmique d'amplitude r6duite et de fr6quence moyenne abaiss6e. Une r6ponse d'6vitement d'un choc 61ectrique est pr6c6d6e par une augmentation de fr6quence des ondes. La fr6quence maximum est atteinte juste avant la survenue de la r6ponse motrice. Les auteurs formulent l'hypoth6se que l'activit6 lente rythmique de l'hippocampe et du dienc6phale sont le signe 61ectrique de la raise en jeu d'un m6canisme du cerveau ant6rieur qui organise ou induit les actes moteurs plus 61abor6s (volontaires). L'auteur ne trouve aucune confirmation des hypoth6se ant6rieures selon lesquelles de telles ondes seraient sp6cifiquement corr616es ~ un arousal g6n6ralis6, ~t des r6ponses d'orientation, h l'apprentissage, /~ l'attention ou un comportement d'approche.

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Reference: VANDERWOLF,C. H. Hippocampal electrical activity and voluntary movement in tile rat. Electroenceph. olin. Neurophysiol., 1969, 26:407 -418.