Cortical-subcortical EEG correlates of suppressed motor behavior during sleep and waking in the cat

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

CORTICAL-SUBCORTICAL MOTOR

BEHAVIOR

DURING

EEG

CORRELATES

SLEEP

AND

681

OF SUPPRESSED

WAKING

IN THE

CAT 1

R. C. HOWE; AND M. B. STERMAN Departments of Physiology and Anatomy, University ~/" Cal([brnia, Los Angeles, Cal![i 90024 and Veterans Administration Hospital, Sepulveda, Cafi£ 91343 (U.S.A.) (Accepted for publication: November 4, 1971)

Cortical EEG synchronization resembling that seen during sleep has been found in the awake animal during behavioral inhibition (Roth et al. 1967), satiety (Clemente et al. 1964), relief from aversive stimulation (Gluck and Rowland 1959), habituation (Hernfindez-Pe6n 1960), and extinction (Sterman and Wyrwicka 1967). It has been postulated that these conditions have in common active suppressive or inhibitory processes (Hern/mdez-Pe6n 1960; Sterman and Wyrwicka 1967). During overt inhibition of motor behavior, a 12-16 c/sec EEG synchronization, generally localized over the sensorimotor cortex, has been described (Roth et al. 1967) and termed the"sensorimotor rhythm" (SMR). This rhythm was found to have the same general cortical location and characteristics as the sleep spindles which occur during quiet sleep 3. Subsequent investigations by Sterman and Wyrwicka (1967) showed that the SMR could be operantly conditioned and was associated behaviorally with a complete absence of phasic motor activity. Trained cats remained alert throughout the duration of such operant performance. Additionally, a reduction of phasic movements together with an enhancement of spindle activity in quiet sleep was demonstrated following SMR training (Sterman et al. 1970). 1 This work was supported by the Veterans Administration and by U.S. Public Health Service Grant MH-10083. 2 Present address: Department of Neurophysiology, Walter Reed Army Institute of Research, Walter Reed Army Medical Center, Washington, D.C. 20012, U.S.A. 3 See footnote 4 in Sterman et al. (1970) for selection of terms quiet and active sleep for the two basic sleep patterns in mammals.

The conclusion drawn from these various observations was that neural mechanisms associated with the suppression of CNS functions during sleep are operative also during wakefulness. The purpose of this study, therefore, was to examine the SMR and sleep spindle phenomena. Specifically, we wished to determine relationships between their cortical and subcortical electrical manifestations, their characteristics as a function of state and the possible origin and type of generation mechanisms involved. METHODS

Eighteen adult male and female cats were surgically prepared for chronic investigation under sodium pentobarbital (Nembutal) anesthesia. Bipolar stainless-steel strut electrodes, completely insulated except for the tips (1 mm intertip distance), were placed stereotaxically into various deep structures of the brain with reference to the atlases of Jasper and Ajmone Marsan (1954) and Snider and Niemer (1961), Small stainless-steel jeweler's screws were used for all cortical leads. To record the SMR and quiet sleep spindle activity, screws were placed in the skull within the frontal sinus over the cruciate and coronal gyri areas. In some cats these screws were located visually, but in most animals they were placed stereotaxically, primarily over the cruciate gyri using A25 as the cruciate sulcus reference point. For this purpose, four screws were generally arranged in a 3 x 5 mm matrix with the widest spacing in the AP plane and the most posterior screws over the postcruciate area, A23, L7 and 10. To record EEG activity from the occipital area Eh, ctroenceph, elin. Neurophysiol., 1972, 32:681 695

682 (see Roth et al. 1967), screws were located over the posterior marginal gyrus, A + 2 to - 2, L3-4. Additional screws were placed on the supraorbital bone within the frontal sinus for recording the electrooculogram (EOG). All recording leads were soldered to a 20-pin Winchester plug which was then mounted to the skull with dental cement. At the termination of the study, animals were sacrificed with an overdose of Nembutal and perfused first with saline and then 10 % formalin. The brains were removed from the skull leaving the screws in the skull cap and noting the exact location of the cortical screws in relation to the gyri. The deep electrodes were located histologically using alternate 80/x frozen sections and a Thionin stain for Nissl substance. All cortical screw placements were verified stereotaxically (AP and lateral planes only) with reference to the known location of deep electrodes. All data were collected with the animals in a modified triple-wailed, Lehigh Valley recording chamber, which had constant light, temperature and sound conditions. The chamber was equipped with a one-way window for behavioral observation of the animal. A 20-lead low noise coaxial Microdot cable connected the cat to the EEG machine. The cable was suspended from a counter-weighted Lehigh Valley slip-ring assembly to allow the animal unencumbered freedom of movement. The E E G and other marker tracings were recorded on a Grass Model 78 polygraph, with Model 7P511 amplifiers. All EEG recordings were taken with the one-half amplitude low frequency filter at 3 c/sec, the high filter at 0.1 kc/sec and the pen high frequency filter at 30 c/sec. The paper speed for all EEG records was 15 mm/sec. After a 1 2 week post-operative interval, the animals were placed in the behavioral chamber, connected to the recording cable, and allowed to adapt to the recording situation. Various combinations of sensorimotor cortical leads were tested systematically during the conditions described below. A control sleep record was obtained from all animals, with a cruciate area lead and a posterior marginal area lead always present along with as many subcortical leads as possible. The control sleep record consisted of at least one complete

g . C. HO'vVE AND M. B. STERMAN

sleep cycle. A sleep cycle was defined as a series of quiet sleep epochs followed by a period of active sleep. Following collection of control data, the majority of animals began SMR conditioning as previously described by Wyrwicka and Sterman (1968). This procedure was employed in order to bring under experimental control the state of voluntary motor suppression and its EEG correlate, the SMR. For all conditioning sessions, the animals were deprived of food for approximately 18 h. Length of the inter-trial interval and total amount of SMR (in amplitude and time) necessary to operate the feeder were controlled by the investigator. The feeder released 0.6 ml of condensed milk and chicken broth for each reinforcement. During consumption of the reward, a 4 12 c/see EEG synchronization usually appeared over the posterior marginal gyrus. This activity has been termed post-reinforcement synchronization (PRS) (Clemente et al. 1964). The SMR conditioning continued until the animals consistently produced 2-8 sec SMR trains. Four of the animals were reinforced manually for the complete absence of motion, irrespective of the simultaneous EEG tracing. This procedure was carried out to determine if learned suppression of motor activity is itself sufficient for the occurrence of the SMR. The EEG data along with EEG filter and relay marker data were recorded on paper in the: (1) alert, non-moving, SMR and non-SMR conditions ; (2) alert, moving, non-SMR condition ; (3) alert, milk consumption, PRS condition; and during (4) drowsy condition ; (5) quiet sleep ; and (6) active sleep. The first three conditions were recorded during SMR conditioning (feeder unblocked) and the last three following termination of the conditioning (feeder blocked). Occasionally, the first and second conditions were recorded during spontaneous behavior in a non-conditioning situation. During all of the above states, behavioral observations were made to assist in state identification. Cortical and subcortical EEG tracings, recorded during awake and sleep states, were examined for the presence of rhythmic patterns or activity characteristic of any behavioral state or location or both. These results were tabled according to location and state and were quantified. Electroenceph. clin. Neurophysiol., 1972, 32:681 695

683

EEG CORRELATES DURING SLEEP AND WAKING

States were determined by using the E E G from both the sensorimotor and visual cortex areas, EOG and behavioral observations. In order to localize more precisely the EEG activity of the sensorimotor cortex area, EEG tracings from each pair of leads were evaluated quantitatively for the SMR and sleep spindles. Amplitudes of these two EEG phenomena, along with the background noise level, were measured peak to peak in microvolts. The respective background noise level was subtracted from each measurement, and a rating scale was devised to place this calculated value into one of four groups (poor, fair, good or excellent) according to amplitude. A set of coordinate maps was then constructed for both the SMR and sleep spindle. Each map was pre-assigned a different amplitude sensitivity level. The cortical leads were plotted on the maps with the cruciate sulcus as the central or zero AP point in each animal. From the coordinate maps for each amplitude sensitivity level, each data point was assigned the largest amplitude rating for that point. This procedure was followed for analysis of both the SMR and sleep spindle data, thus producing two final maps, each of which represent a threedimensional stereotaxic amplitude display of these EEG phenomena.

regardless of the ongoing EEG, it was found that the SMR did, in fact, appear eventually during trained immobility. That is, the rhythm gradually emerged as a consistent correlate of trained motionlessness, even though its presence was not required for reinforcement. The reverse situation never occurred, i.e., the SMR was never present in a behaviorally moving animal. Occasionally, suppression of motor behavior was observed without the appearance of the SMR. This usually occurred in animals who were very hungry due to the food deprivation schedule, especially at the beginning of a daily training session. The highly activated state of these animals tended to suppress the appearance of the rhythm. This was true for the newly trained as well as for the over-trained animals. The best results in SMR conditioning were achieved when animals were placed on full ad lib feeding schedules in the home cage. During suppression of motor behavior the SMR was found to be localized primarily on the postcruciate gyrus (SI projection area). It appeared only rarely near or on the precruciate cortex and then was present only at relatively low voltage. Fig. 1 displays cortical localization by amplitude of the SMR in the awake animal, with cruciate sulcus used as the zero AP reference

RESULTS

STEREOTAXIC MAP OF SENSORIMOTOR RHYTHM (SMR)

The SMR and sleep spindle phenomena were generally found in different thalamocortical projection systems within the brain. For this reason, the EEG activity of these systems is presented separately.

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Somatosensory system EEG Spontaneous behavioral immobility in an awake animal was often accompanied by a 12-16 c/sec EEG synchronization, the SMR, as described by Roth et al. (1967). With reinforcement of this pattern in an operant response paradigm, both the behavior of the animal and the occurrence of the SMR became stabilized, as described previously. Regular SMR activity appeared either unilaterally or bilaterally. The bilateral appearance was by far the most common under the conditions of this study. In animals behaviorally conditioned to suppress movement

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Fig. 1. Stereotaxic map of the SMR on the cerebral cortex. The cortical area covered by the map is depicted by a broken line in the insert (upper riqht). The map was constructed using the cruciate sulcus as the reference point in all animals. The largest amplitude SMR points were located on the posterior part of the postcruciate gyrus, just rostral to the postcruciate dimple.

Electroeneeph. olin. Neurophysiol.. 1972, 32: 6XI 695

684

R. C. HOWE AND M. B. STERMAN

amplitude subcortical SMR, 40 l~V and above, was located almost exclusively within VPL (Table I). The stereotaxic coordinates for this VPL activity ranged from A7-10, L6.5-8.0, H + 1-3, with best results (above 55/tV) obtained at approximately A 9-10, L8, H + 2 3. The VPL rhythm was temporally correlated with the cortical SMR in the majority of animals. Both rhythms were disrupted simultaneously by any phasic motor activity. No subcortical EEG rhythm was observed in the medial lemniscus. During the drowsy state, both the cortical and

point in all animals. The cruciate sulcus was found to have the AP coordinate A25.2+0.9 with its lateral termination at L9.4_+ 1.0. The postcruciate dimple had an AP measurement of A21.7 _+0.4. The largest amplitude SMR was located approximately 2~4 mm posterior to the cruciate sulcus at L6.5 to 10.5, or stereotaxically from A21 23, L6.5 10.5. This area lies near the postcruciate dimple or slightly anterior to it. An SMR correlate was found generally within the subcortical structures of the somatosensory system and specifically in nucleus ventralis posterior lateralis (VPL) as shown in Fig. 2. Large TABLE I

Location of subcortical sensorimotor rhythms during awake and drowsy states Subcortical structure

Amplitude rating for each point*

Awake only

Ventralis posterior lateralis n. Ventralis lateralis n. Centrum medianum n. Ventralis anterior n. Pyramidal tract Cerebral peduncle Nucleus reticularis thalami Red nucleus magnocellularis Reticular formation Hippocampus Dentate n. Cerebellar cortex Superior cerebellar peduncle Anterior ventralis n. Ventralis medialis n. Medial lemniscus

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Fig. 2. Subcortical EEG patterns in VPL and VL during SMR conditioning and drowsiness. In the SMR conditioning record, note the presence of SMR from the cruciate gyrus and VPL leads in contrast to its absence in the VL lead. SMR from the cruciate gyrus lead is displayed by the 12 14 c/sec relay marker. PRS activity is present in the posterior marginal gyrus lead following delivery of the liquid reinforcement, denoted by the feeder marker. In the drowsy records, continuous large amplitude SMR is present simultaneously in cruciate gyrus and VPL, whereas only small amplitude SMR appears in VE. All records were obtained from the same animal. The paper speed in this and all subsequent EEG figures was 15 mm/sec. A SMR CONDiTiONiNG

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Fig. 3. Different EEG patterns obtained during SMR conditioning and quiet sleep from the precruciate gyrus, postcruciate gyrus and from both gyri simultaneously. The precruciate gyrus (part I) shows almost no SMR during conditioning but very large amplitude spindles during quiet sleep. The postcruciate gyrus (part lI) is almost opposite to the precruciate gyrus in that it displays large amplitude SMR in the awake state and poorly developed spindle activity in quiet sleep. The pre- to postcruciate gyrus recording (part III) shows both the SMR during conditioning (from postcruciate gyrus) and the spindle activity of quiet sleep (from precruciate gyrus).

Electroenceph. clin. Neurophysiol., 1972, 32:681 695

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R . C . HOWE AND M. B. STERMAN

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Fig. 4. Subcortical EEG patterns in VPL and VL during quiet and active sleep. In quiet sleep, VPL shows almost no spindle activity, whereas VL shows very discrete spindles correlated with the cortical spindles. In active sleep, VPL displays a distinct SMR correlate in non-phasic portions, whereas only a small amplitude sporadic SMR correlate appears ir~ VL. All records were obtained from the same animal.

subcortical SMR in the somatosensory system increased further in amplitude and became more continuous in nature (Fig. 2, I). These SMR trains eventually decreased in amplitude and in continuity during the transition to quiet sleep. In considering cortical-subcortical EEG correlations during quiet sleep, it becomes necessary to make a distinction between activity in pre- and postcruciate cortices. As mentioned above, the SMR was localized primarily to postcruciate gyrus (Fig. 1). In quiet sleep, the SMR disappeared (Fig. 3, II, A and B), and the postcruciate gyrus and VPL showed no correlated slow wave activity. Clear spindle burst activity was noted on the precruciate gyrus (Fig. 3, I, A and B). However, this pattern showed no correlation with VPL activity (Fig. 4, A-I). The precruciate sleep spindle localization will be elaborated further below. The cortical SMR and its subcortical VPL

correlate appeared again during active sleep in those intervals devoid of any of its characteristic phasic phenomena, i.e., in non-phasic portions of active sleep (Fig. 4, B-I; Table II). The SMR in active sleep is quite similar to the awake SMR in that it has the same cortical subcortical location, appears in the absence of phasic activity and is easily disrupted by even small phasic phenomena. The rhythm, however, was generally smaller in amplitude during active sleep than in the awake state. 2. M o t o r system EEG

The precruciate (motor) cortex displayed little distinguishing EEG activity during waking behavior with or without movement (low voltage fast EEG only). Occasionally, a vcry small amplitude SMR occurred on precruciate cortex during trained immobility but was usually spoElectroenceph. clin. Neurophrsiol.. 1972, 32:681 695

687

EEG C O R R E L A T E S D U R I N G SLEEP A N D W A K I N G

TABLE 11 Location of subcortical spindles during quiet sleep and subcortical S M R d u r i n g active sleep Subcortical s t r u c t u r e

Amplitude rating for each point

Quiet sleep only* Ventralis lateralis n. Cerebral peduncle C e n t r u m m e d i a n u m n.

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radio in appearance (Fig. 3, A-I). A low voltage subcortical SMR correlate appeared in n.ventralis lateralis (VL) in only three out of seven cats. No subcortical EEG correlates were apparent in the red nucleus (magnocellularis). During drowsiness, the precruciate cortex began to show a definite but still low voltage SMR which also appeared in VL approximately 86~,i of the time (Table I). In the transition between drowsiness and quiet sleep, the electrical activity of precruciate cortex and VL changed drastically. Both simultaneously displayed EEG sleep-spindle activity (Fig. 3, BI, 4, A-II and 5).

The spindle activity continued to be present in both structures throughout quiet sleep. The cortical sleep spindle was found to be localized on the precruciate gyrus with some extension onto the anterior part of the postcruciate gyrus. Fig. 6 is a three-dimensional stereotaxic amplitude display of sleep-spindle activity. The largest amplitude spindles were located on precruciate gyrus (solid black dots), whereas smaller amplitude spindles extended 2 mm posterior onto postcruciate gyrus. The sleep spindles, like the SMR, could occur unilaterally or bilaterally. Large amplitudes sleep spindles in VL were Electroenceph. clin. Neurophysiol., 1972, 32:681 695

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observed in all animals (Fig. 4, A-II and 7 ; Table II). The stereotaxic coordinates for the VL leads ranged from AI0.5-11.5, L4-4.5, H + 0 . 5 2.5,

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with the largest amplitude spindles located approximately A l l , L4, H + 2 . In addition to the spindle activity, large EEG spikes were present in VL in some cats throughout quiet sleep episodes. Toward the end of quiet sleep, usually within 1 rain preceding active sleep, cortical and VL spindle bursts (and VL spikes) appeared more frequently and continued to increase in frequency to the onset of active sleep. The EEG activity of the motor system in active sleep was similar to the awake states. Only the smallest amplitude SMR was present sporadically on the precruciate gyrus in non-phasic active sleep. SMR correlated activity was noted in VL during active sleep in only 33 °il of the subjects (Fig. 4, BII). Usually, the precruciate gyrus and VL displayed no specific EEG activity throughout active sleep. E E G in other brain areas

No specific EEG pattern, other than desynchronized activity, was observed in the thalamic centrum medianum (CM) nucleus during waking behavior with movement and milk consumption. Electroenceph. clin. Neurophysiol., 1972, 32:681 695

EEG CORRELATES DURING SLEEP AND W A K I N G

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Electroenceph. clin. Neurophysiol., 1972, 32 : 681-695

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2 sec (RHI) 20,uV Fig. 9. Spindle activity in quiet sleep. Note the subcortical spindle correlates in cerebral peduncles (1) and in ccntrum medianum (II). The medial lemniscus (lI) showed a complete absence of sleep spindle activity.

A small amplitude SMR correlate (16 35 #V) was definitely present in CM during suppression of motor behavior (Fig. 8). This activity increased further in amplitude (36-55 #V) and became more pronounced during the drowsy state. Spindleburst activity began appearing in CM in the transition between drowsiness and quiet sleep. In quiet sleep, CM displayed EEG spindle-bursts (Fig. 9, II). This activity was smaller in amplitude than the subcortical sleep spindles in VL. In addition to the sleep spindles, large EEG spikes were sometimes present in quiet sleep. In active sleep, CM showed very little distinguishing EEG activity except for an occasional low voltage SMR correlate during non-phasic portions. The CM electrodes were located at A7-7.5, L3 4, H + 1-1.5. It should be noted that CM was the only subcortical structure observed in this study which clearly displayed both an awake SMR and a quiet sleep spindle correlate. During behavior with movement, milk consumption and behavioral motor suppression, no distinguishing EEG activity was observed in the pyramidal tract (PT). In 60 ~ of the cats, a small amplitude SMR correlate appeared in the PT during drowsiness. Generally, little or no quiet

sleep spindle activity was observed in the medullary PT (Fig. 7, II). Similarly, no distinct EEG phenomenon occurred in this tract throughout active sleep. The pyramidal tract electrodes were histologically located at P3 3.5, Lt.5, H - 10 to -11. The EEG activity of the cerebral peduncle (C P) was quite similar to that of ventralis lateralis. No distinct patterns occurred in the CP during the three waking conditions. A clear but small SMR correlate appeared in CP during drowsiness. In quiet sleep, the CP displayed well developed EEG spindle bursts 30 120#V in amplitude (Fig. 9, I), similar to those in VL. No particular EEG phenomenon was noted in the CP during active sleep. CP electrode placements ranged from A2 to A9. Two of the better leads for the patterns described above were located at A5, L6.5, H - 4, and A9, L7, H - 1. The poorest lead was also the most posterior at A2, L3.5, H - 5.5. DISCUSSION

The appearance of a cortical EEG synchronization during inhibitory behavior in cats confirms those described by several investigators Electroenceph. olin. Neurophysiol., 1972, 32:681 695

EEG CORRELATES DURING SLEEP AND WAKING

(Donhoffer and Lissak 1962; Roth et al. 1967; Sterman and Wyrwicka 1967). Donhoffer and Lissak (1962) described the activity as an " e n a r c e a u r y t h m e " (EAR), a well known term used to describe a similar rhythm in humans (Gastaut 1952; Gastaut et al. 1952). Roth et al. (1967) and Sterman and Wyrwicka (1967) used the term "sensorimotor rhythm" (SMR), as they found the EEG activity generally in sensorimotor cortex. In this study, the SMR was localized primarily within the somatosensory system. Therefore, a more precise anatomical notation would be "somatosensory rhythm". From a functional point of view, however, the suppression of phasic motor behavior involves both sensory and motor systems. The term SMR can thus be retained as an appropriate designation which considers both anatomy and function. The similarity between the SMR in cats and the en a r c e a u rhythm or rolandic "wicket rhythm" in humans is striking. The SMR in cats was localized to the sensorimotor area, whereas in humans the rolandic a r c e a u rhythm was observed from a functionally synonymous area around the central sulcus (Gastaut et al. 1952). Both rhythms may appear unilaterally or bilaterally (Chatrian e t al. 1959; Donhoffer and Lissak 1962), and both are blocked by phasic motor activity (Chatrian et al. 1959; Gastaut et al. 1952; Roth et al. 1967; Sterman and Wyrwicka 1967). Moreover, the SMR was not disrupted by sensory stimuli, provided no movement occurred in relationship to these stimuli. Similar observations have been reported in humans (Chatrian e t al. 1959; Klass and Bickford 1957). Therefore, it is likely that the SMR in cats and the rolandic a r c e a u rhythm in humans are synonymous, and represent, functionally, EEG correlates of voluntary phasic motor suppression. The postcruciate area to which the SMR was localized corresponds to the somatosensory projection area from the trunk and limbs in the cat (Adrian 1941 ; Woolsey 1947; Rose and Woolsey 1949; Kaada 1951). Additionally, the somatosensory cortex near the postcruciate dimple, where the greatest SMR amplitudes were observed, was implicated recently as a primary receiving: area from the vestibular system (Sans et al. 1970). This same primary cortical area receives input from Group I thalamocortical relay

691 cells (Andersson et al. 1966; Rosen 1969) and has strong reciprocal corticothalamic projections to these same relay cells (Rosen 1969). The postcruciate dimple area was shown to project to the more dorsal and lateral parts of VPL (Kawana 1969), the primary subcortical structure associated with the SMR in this study. The localization of SMR correlated activity in VPL also implicates these same sensory projections, since this area of the nucleus is known to receive somatosensory afferents from the trunk and limbs (Mountcastle and Henneman 1949; Rose and Mountcastle 1952) and from the vestibular system (Sans et al. 1970). Numerous studies have demonstrated a well defined topographical organization of projections from V PL to somatosensory cortex (Jones and Powell 1969; Manson 1969; Hand and Morrison 1970; Heath 1970; Morrison et ai. 1970) with no apparent projections to the motor cortex and area 5 (Jones and Powell 1969). Since no subcortical SMR correlate was ever observed in ML (medial lemniscus), it can be concluded that the SMR is located primarily in the somatosensory system, that it involves VPL and its cortical projection area, and that il has the possibility of showing a topographical organization. Investigations into the thalamic control of spontaneous cortical activity have demonstrated that rhythmic synchronization is generated by thalamic neurons (see Andersson and Manson 1971). In the present study, it was noted that the cortical SMR and correlated VPL activity were disrupted simultaneously by phasic motor activity. Thus, the SMR may be generated by neurons within the ventro-basal thalamus through similar synaptic depolarization and recurrent inhibitory processes as discussed by Andersson and Manson (1971). The appearance of slow waves in somatosensory cortex during quiet sleep, without SMR activity, could result from the marked depression of ventro-basal elements during this state which has been suggested by numerous evoked potential studies (Allison 1965; Favale et al. 1965; Steriade 1970). The reappearance of the SMR and its VPL correlate in active sleep suggests that the thalamic generator mechanism is again active and that mediating thalamocortical relationships have been re-established. Electroenceph. clin. Neurophysiol., 1972, 32:681 695

692 The spindle activity in quiet sleep was reflected primarily in VL and motor cortex and to some extent in CM and CPs. Localization of the sleep spindle on the precruciate gyrus and anterior portion of the postcruciate gyrus corresponds quite well with the topographical representation of the motor cortex in the cat (Woolsey 1947; Rose and Woolsey 1949; Kaada 1951). Sobieszek (1968) reported recently that spontaneous 14~16 c/sec sleep spindles in the dog were recorded maximally from anterior sigmoid (precruciate) gyrus and the anterior part of the posterior sigmoid gyrus, and that there was a marked independence of spindle formation in the two hemispheres. This is in agreement with the results of this investigation in the cat. The occurrence of large subcortical spindles in VL is appropriate for the location of corresponding cortical sleep spindles. Anatomical projections of VL efferents were found to include primarily the precruciate and anterior lateral coronal gyri, cruciate sulcus and presylvian sulcus (Strick 1970). Other studies have shown that antidromic and orthodromic responses in VL are elicited primarily from precruciate cortex (Sakata et al. 1966 ; Nakamura and Schlag 1968 ; Dormont and Massion 1970). Sleep spindles may, therefore, be generated by a thalamocortico-thalamic circuit involving VL and motor cortex. A spindle generator mechanism, similar to that attributed to VPL for the generation of the SMR, is also potentially present in VL. Several investigators have reported the presence of excitatory postsynaptic potentials followed by inhibitory postsynaptic potentials in VL (Purpura et al. 1966; Sakata et al. 1966; Schlag and Villablanca 1968; Uno et al. 1970). Thus, recurrent excitation and inhibition of thalamic VL neurons are assumed to be involved in the generation of sleep spindles. The presence of sleep spindle activity in VL, and not in the ventro-basal complex, suggests that VL spindle activity is induced by some active process related specifically to quiet sleep and to the VL or motor cortex areas or both. It is possible that neostriatal structures (Sterman and Clemente 1968) are involved in this process. EEG activity in CP was very similar to that in VL and motor cortex. The appearance of large

R. C. H O W E A N D M. B. S T E R M A N

amplitude EEG spindles in CP during quiet sleep suggests that the VL-motor cortex circuit burst activity is directly reflected in the output of cortical motor neurons. However, little or no spindle activity was observed here in the medullary PT, and Morrison and Pompeiano (1965) found no change in the activity of flexor reflex afferents in the spinal cord during pyramidal cell bursts associated with spindles. The output of the motor cortex during spindle activity is apparently not directed through the corticospinal pathway but may take an alternate course through internal capsule and CP via cortico-olivary or corticopontine pathways or both to the cerebellum. The possibility of a functionally active cortico-cerebello-cortical circuit during quiet sleep emerges from these considerations. Finally, EEG activity in CM was unusual in that it clearly reflected both SMR and sleep spindle activity. This is due probably to its known anatomical relationships with structures in both somatosensory (Nauta and Whitlock 1954; Totibadze and Moniava 1969) and motor systems (Rinvik 1968). It has been suggested that the generators for the SMR and sleep spindle phenomena are located at the thalamic level and involve a mechanism of recurrent neuronal inhibition. The development and maintenance of rhythmic cortical subcortical EEG activity over a sustained period of time appear to depend upon tonic reverberating thalamo-cortico-thalamic circuits. The dynamic occurrence of rhythmic EEG activity in sensory and motor systems as a function of physiological state serves not only to label these states but provides also important clues about their physiological basis. SUMMARY

During suppression of motor behavior in cats, a 12-16 c/sec EEG activity generally localized over the sensorimotor cortex has been described previously and termed the sensorimotor rhythm (SMR). It has recently been shown that SMR conditioning can alter EEG spindle activity of slow wave or quiet sleep. The SMR can also appear in non-phasic portions of rapid eye movement or active sleep. Therefore, the purpose of this study was to examine the SMR and sleep spindle phenomena in detail. Electroenceph. c/in. Neurophysiol., 1972, 32:681 695

EEG CORRELATES DURING SLEEP AND WAKING

Cortical and subcortical EEG data were recorded from the somatosensory, motor and visual systems during sleep and wakefulness. EEG tracings were examined for any EEG rhythms or activity characteristic of any behavioral state or location or both. These results were tabled according to location and state and were quantified. States were defined by using EEG from both the sensorimotor and visual cortex areas, electrooculogram and behavioral observations. The SMR was found primarily within the somatosensory system in nucleus ventralis posterior lateralis (VPL) and its primary cortical projection area, the postcruciate gyrus. It occurred in these structures during the absence of phasic motor activity in both the alert animal and in active sleep. Centrum medianum (CM) also possessed a low voltage SMR correlate in the alert animal. The subcortical correlates of the SMR were not present during quiet sleep. In this state, spindle bursts were located primarily within the motor system in ventralis lateralis (VL) and its cortical projection area, the precruciate gyrus. The cerebral peduncles and CM also displayed sleep spindle activity. The VL-motor cortex spindle bursts showed a marked increase in frequency of occurrence in the 1 min interval preceding active sleep. It was proposed that the generators for the SMR and sleep spindle phenomena are probably located at the thalamic level. Although their thalamocortical projections and correlated behavioral states are relatively discrete, their functional origins both appear to reside in a mechanism concerned with the specific suppression of phasic motor activity. RESUME CONTRIBUTIONS

EEG

CORT1CO-SOUS-CORTICALES

DU COMPORTEMENT DE SUPPRESSION MOTRICE AU COURS DU SOMMEIL ET DE EA VEII.LE CHEZ LE CHAT

Au cours de la suppression du comportement moteur chez des chats, une activit6 E E G de 12 fi 16 c/sec g6n6ralement localis6e au niveau du cortex sensori-moteur, a 6t6 ant6rieurement ddcrite, activit6 d6nomm6e rythme sensori-moteur (SMR). On a montr6 r6cemment que le conditionnement du S M R peut modifier l'activit6 de spindles E E G du sommeil fi ondes lentes ou

693 sommeil tranquille. Le S M R peut 6galement apparaitre dans des portions non phasiques de sommeil REM ou sommeil actif. Ainsi, le sujet de cette 6rude est d'examiner en d6tail les relations entre SMR et ph6nom6nes de spindles du sommeil. Les donn6es E E G corticales et sous-corticales sont enregistr6es au niveau des systbmes somatosensoriels, moteurs et visuels au cours du sommeil et de la veille. Les tracts E E G sont examines en tenant compte soit de tout rythme ou activit6 E E G caract6ristique d'un 6tat comportemental soit de leur localisation, soit des deux. Les r6sultats de ce classement en fonction de la localisation et de l'6tat comportemental sont quantifi6s. Les 6tats sont d6finis en utilisant I'EEG des aires corticales sensori-motrices et visuelles, I'EOG et les observations comportementales. Le S M R s'observe principalement ~t l'int~rieur du syst6me somato-sensoriel au niveau du VPL et de son aire de projection primaire corticale, le gyrus post-cruci6. I1 survient dans ces structures en Fabsence d'activit6 motrice phasique aussi bien chez l'animal alerte que dans le sommeil actif. La contribution du CM au SMR est de faible votage chez l'animal 6veill6. Les contributions sous-corticales du SMR n'existent pas au cours du sommeil tranquille. Dans cet 6tat, les bouff6es de spindles sont localis6es primairement, ~ l'int6rieur du systeme moteur, au niveau du VL et de son aire de projection corticale, le gyrus pr6cruci6. Les p6doncules c6r6braux et le cortex moteur montrent 6galement une activit6 de spindles de sommeil. Les bouff6es de spindles du VL et du cortex moteur surviennent avec une beaucoup plus grande t¥6quence au cours de la minute qui pr6c6de le sommeil actif. Les auteurs font l'hypoth6se que les g6n6rateurs du SMR et des ph6nom6nes de spindles de sommeil soient probablement localises au niveau thalamique. Bien que leur projection thalamo-corticale soient relativement lidblemerit associ6es aux 6tats comportementaux, leurs origines tbnctionnelles communes paraissent r6sider dans un m6canisme qui intervient dans la suppression sp6cifique de l'activit6 motrice phasique. Electroenceph. clin. Neurophysiol., 1972, 32:681 695

694 The authors wish to thank the staff of Neuropsychology Research section at Veterans Administration Hospital, Sepulveda, California, for their assistance in this investigation. REFERENCES

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R~Jerence: HOWE, R. C. and STERMAN, M. B. Cortical-subcortical EEG correlates of suppressed motor behavior during sleep and waking in the cat. Electroenceph. clin. Neurophysiol., 1972, 32:681 695.