Comparative thresholds of cortex, vestibular system and reticular formation in wakefulness, sleep and rapid eye movement periods

ELECTROENCEPHALOGRAPHY AND CLINICAL NEUROPHYSIOLOGY

COMPARATIVE SYSTEM AND

THRESHOLDS

RETICULAR

SLEEP AND

RAPID

239

OF CORTEX, VESTIBULAR

FORMATION

I N WAKEFULNESS,

EYE M O V E M E N T

P E R I O D S 1,~

ROBERT HODES, P H . D . AND JUN-IcHI SUZUKI, M . D . a Departments o f Pediatrics and Neurology, The Mount Sinai Hospital, New York, N. Y. (U.S.A.) (Accepted for publication: July 22, 1964)

INTRODUCTION

Within recent years it has been shown in man, as well as many laboratory animals, that the periods of slow wave EEG activity in sleep are cyclically interrupted by episodes, of variable number and duration, characterized by low voltage fast activity. At this time, there is great depression of skeletal muscle tone, sporadic twitching of face, neck and limbs, and bursts of rapid eye movement periods (REMPs) during which, in the human subject, dreams frequently occur (Aserinsky and Kleitman 1955; Dement and Kleitman 1957; Dement 1958; Jouvet el al. 1959; Berger 1961 ; Jouvet 1962; Schwartz 1962; Antrobus et al. 1964 ; Dement 1964; Hades 1964a; Hades and Dement 1964). Most workers consider that REMPs represent sleep of the most profound depth (see Hades and Dement 1964), primarily on the basis of the findings that threshold for arousal by stimulation of the mesencephalic reticular formation (RF) is considerably higher during this stage than during the period of synchronized brain potentials (Benoit and Bloch 1960; Horovitz and Chow 1961 ; Jouvet 1962). This high arousal threshold, however, might be due to a depressed R F rather thanto anoverall depression, including that of the cortex, such as one might expect in the deepest stage of sleep. Our experiments were therefore undertaken to t Aided, in part, by U.S.P.H.S. Grants NB 02796-04, 0.5, and NB 00294. A preliminary account of some of this work has been reported (Hades 1964b). a Fulbright Fellow from the Department of Otolaryngology, University of Tokyo Medical School. Present address: University of Tokyo, Motofuji-cho 1, BunkyoKu, Tokyo, Japan.

test the excitability of the cerebral cortex. METItODS

At preliminary operations performed under pentobarbital anesthesia on 5 adult cats, insulated phonograph needle stimulating electrodes were inserted into anterior sigmoid and coronal gyri through small burr holes in the skull. Placements were verified at sacriftce of the animal. Phonograph needles lot ECoG recording were placed bilaterally in the frontal, parietal, and occipital cortex. A pair of insulated stainless steel wires, 0.25 mm in diameter, cemented together, and with their 0.5 mm bare tips separated by 2 ram, were inserted by stereotaxy into the mesencephalic RF on one side. The middle ear was exposed by a retroauricular approach and malleus, incus, tensor tympani and tympanic membrane removed. The stapedius muscle was cut and removed with the upper portion of the stapes; the foot plate of the stapes was preserved. The facial canal was opened and the facial nerve removed. Small openings, made at each ampulla, permitted the insertion of double, enamel-covered, 40 # stainless steel wires between the bony wall and the endosteum of each semicircular canal. Electrodes were fixed in place with paraffin and acrylic resin cement. Two small semicircular surgical needles, stitched in place bilaterally into the neck muscles, were used to record the EMG. Tiny curved Ophthalmic needles, sewn in the subcutaneous tissue lateral to the outer canthus of each eye recorded the electro-oculogram (EOG). All lead wires, carried subcutaneously to the surface, were soldered to a 15 or 25-point miniature socket (affixed to the skull by dental acrylic) and led to a Grass Model 6 EEG instrument. E K G was Electroenceph. clin. Neurophysiol., 1965, 18:239-248

240

R. HODES AND J. 1. S U Z U K I

LAF - F RAF-F

B

C

4~V

soy

LF - P ,

RF-P

EMG

~ EKG

15:39

INS~

a

~

.

~

~

....... I~ -

16:28'

'

~x~

I)

S2V

1

ON SIDE

HEAD LIP

t

~i ~

16:32

,

I

Fig. 1

Determination of thresholds for electrographic and behavioral arousal by stimulation of the mesencephalic RF in different states of consciousness. Records taken 2 sec after end of stimulation of RF with a single train of shocks (0.3 msec, 200/sec) lasting 500 msec. Cat drowsy before stimulation in A and in REMP in B and C. Electrographic change with incipient behavioral arousal in A, no effect in B, and neck muscle movement artifact in C, suggesting near-arousal. More intense stimulation (D) causes arousal which subsides within 2 min and animal then becomes drowsy (E) and goes to sleep (F). In this and following records abbreviations L, R, A, F, P, O, EOG, EMG and EKG are: left, right, anterior, frontal, parietal, occipital, electro-oculogram, electromyogram (left to right neck muscles), and electrocardiogram (left to right forelimbs), respectively. In most records inspiration and expiration may be observed in the EKG amplitude fluctuations. r e c o r d e d on the ink writer by conventional E E G disc or h u m a n ear-clip electrodes on each forelimb. A few days after recovery f r o m surgery the a n i m a l s w o u l d become a c c u s t o m e d to the labor a t o r y a n d fall asleep a n d go into R E M P s spontaneously. E a c h cat was o b s e r v e d t h r o u g h a o n e - w a y m i r r o r for m a n y hours on several different days for 1-3 months. Square wave pulses (0.5-1 msec) f r o m a G r a s s S-4 stimulator, passed t h r o u g h a n isolation unit, were used for b i p o l a r s t i m u l a t i o n o f the frontal cortex. W h e n a p p l i e d singly or at a rate o f 0.5-1/ sec t h r e s h o l d shocks p r o d u c e d a small twitch o f the c o n t r a l a t e r a l pinna, vibrissae, or eyelids ( G a r o l 1942). W i t h slightly stronger s t i m u l a t i o n

there was a brisk c o n t r a l a t e r a l m o v e m e n t o f head a n d neck, or c o n t r a l a t e r a l forelimb flexion ( G a rol 1942; H o d e s et al. 1951). Bipolar stimulation e m p l o y e d for vestibular nerves by single, or 0 . 5 l/sec volleys o f 0.05-3 msec pulses for 20 msec at 100-800/sec, e v o k e d m o v e m e n t s o f pinna, face, or vibrissae (Suzuki a n d C o h e n 1964), o r c o n t r a versive deviation o f head a n d eyes. The R F was s t i m u l a t e d b i p o l a r l y by a volley o f 0. I-0.5 msec square pulses for 20-500 msec, at 50-250/sec. Either single, or a few trains o f stimuli, repeated at 2 sec intervals, were given. A r o u s a l by R F s t i m u l a t i o n was d e t e r m i n e d by changes in E C o G a n d o t h e r indicators on the i n k - w r i t t e n r e c o r d ( F i g . 1, A), as well as by alterations in behavioral attitudes. D u r i n g the low Electroenceph. clin. Neurophysiol., 1965, 18:239-248

241

THRESHOLDS IN WAKEFULNESS, SLEEP AND REMP

B 12

RP-O

I~K~VSY

~K£

EMG

"n~E~O~D,CODEX 26v

3lv

•,'...-~..~_.r~;_,:~-:*.:::~-:~_-~-.~_~4_ - -:~-.:--..~--~--:~_¢~ ~ . ~ ' ; ¢ g ~ # , ~ EKG i

,I

I

i

C

t

•

i

,]

r

D

RAPID EYE-MOVEMENTS

T

40V

Fig. 2 Electrographic features of different states of consciousness, and rise in threshold for evoking movements by motor cortex stimulation (single shocks, 0.5 msec) from wakefulness (A) to drowsiness (B) and sleep (C). Reversal of trend of threshold increase in R E M P (D).

voltage fast E C o G of wakefulness and REMPs little electrocortical change could be observed on incipient arousal (Fig. 1, B and C). When behavioral arousal did take place during REMPs (Fig. 1, D), tone of the neck and facial muscles would increase sharply. If the stimulus were discontinued soon enough, the animal might then drowse and sleep again (Fig. 1, E and F). RESULTS

1. Thresholds for evoking cortico-spinal movement in different behavioral and ECoG stages As several investigators have shown, the cat, adjusted to the laboratory, presents the 4 behavioral stages and their correlated ECoG, EOG, and E M G recordings of Fig. 2. In the relaxed waking state, threshold for eliciting a particular movement was quite stable in the same animal. In one cat, e.g., the average thresholds (for movement of the right vibrissae when the left cortex was stimulated with a 0.5 msec pulse), tested several times on 6 different days over a period of

3 weeks, were: 30, 35, 30, 32, 32 and 30 V. On 4 of these days, when the cat was purposely excited from relaxed wakefulness, thresholds were: 26, 25, 28 and 23 V. Stimulation of the left cortex of the cat shown in Fig. 2 caused a tiny movement of the right pinna. Threshold for elicitation of this response changed from 26 to 32 to 40 V as the animal passed from relaxed wakefulness to drowsiness to sleep (Fig. 2, A, B, C). During the REMP, however, threshold declined, almost to the level of the waking animal (Fig. 2, D). The period of REMs is not a constant, nor a steady state (Antrobus et al. 1964; Hodes and Dement 1964). Fig. 3 shows an example of fluctuations in a single R E M P ; record B demonstrates greater ocular activity than A (2 min earlier). Also, movements of head and face (channels 6 and 7) are absent in A. Threshold for production of movement by cortical stimulation was lower during the phase of active eye movements (38 V) than during periods of ocular quiescence (43 V). This was true of all 12 obserEleetroeneeph.

clin. N e u r o p h y s i o l . ,

1965, 1 8 : 2 3 9 - 2 4 8

242

R.

HODES

AND

J, I. S U Z U K I

LAF -F

RAF -F

~-~

LF -P RF-P

c,,~ -RO

THRESHOLD. CORTEX=.3,'

EIOG

EMG EKG

13:10

INSp

EXp

..~---,-,...-..~.~, -..¢-~.,-~,¢ - ~ . , ~ . . ~

~ -

~

.

~

~.~ 7 , %

~

B

THRESHOLD, CORTEX=38V

,¢ 13:12

I 2uc !

f

Fig. 3 Higher threshold for cortically evoked movements in a single REMP when eyes are relatively quiet (A) than in the burst of ocular jerking (B). Note irregularity of cardiac rhythm, especially in B. vations in which such comparative thresholds were studied. Changes in threshold with variations in E C o G and behavior are shown for another experiment in Fig. 4. Threshold is lowest in wakefulness (average, 42 V), and rises in drowsiness and sleep. Average threshold in the 3 sleep phases (48.5 V) is higher than the average level during the 2 REMPs (44.5 V). The gradual threshold changes in the first 2 periods of sleep in this experiment were not seen in all animals, nor in all experiments on this same animal; abrupt threshold alterations occurred often at the transition from sleep to REMPs, and vice-versa (right part of Fig. 4 and Fig. 7).

2. Thresholds for eliciting vestibular reflexes in different ECoG stages Threshold for producing movement by stimulation of the vestibular nerves during REMPs,

in contrast to the case for cortically evoked movements, was higher than during sleep (Fig. 5). The abrupt rise and fall in threshold from sleep to R E M P and vice-versa was a typical finding in all experiments, but the magnitude of the changes usually was not so great as in the first transition of Fig. 5. Also in contradistinction to cortical stimulation, threshold for vestibular reflexes was higher when the eyes were actively moving than when they were relatively quiet, in any given R E M P (Fig. 6).

3. ThresholdsJor arousal by stimulation of the RF during different ECoG phases Our results are in agreement with those of Benoit and Bloch (1960), Horovitz and Chow (196]) and Jouvet (1962), who have shown a marked rise for arousal threshold during REMPs, as compared with sleep (Fig. 7). Electroenceph. clin. Neurophysiol., 1965, 18:239-248

THRESHOLDS IN WAKEFULNESS, SLEEP AND*REMP I

~

I

'

I

-

~

I

[ CORTICO- SPINAL]

d

!ii!!!iii! ~i!!il

!iii!i:ii!;!ii!

iiiiiii!iii~i!ii! 5i iii~il~iii:

iiil;ii~iiiii!i ii!~~ ii~i~i

~ii! +~!~h ~i ¸~?:!i .............

i iii iii!iiiiill ;i~ ili~i~i¸ Si:ii:i;:!

AWAKE m "1" DROWSy

"~

ASLEEP

o~

REM

. . . . . . . . .

I 73:ao

J

14:00

. . . . . . . . . . . . . .

I

I

14:30

. . . . . . . . . . . . .

i

I

|5:00

l1 ,

I

15:30

TIME

Fig. 4 Threshold changes for evoking movement by cortical stimulation in different states of consciousness. ECoG recorded continuously during 2 h session. Stippling denotes REMPs.

lated activity, whereas, for vestibular and R F stimulation, the rise from sleep to R E M P s is considerably greater. The distinction between vestibular and R F stimulation on the one hand and cortical stimulation thresholds on the other, as the cat changes from sleep to REMPs, is clearly shown by their opposite slopes at this transition. In the experiment in Fig. 8, stimulation thresholds (in multiples of threshold (T) during relaxed wakefulness) for the drowsy and sleeping states were: cortical, 1.3 and 1.4 T; vestibular, 1.1 and 1.4 T; reticular, 1.1 and 2.0 T, respectively. In R E M P s thresholds rose to 4.7 T for vestibular and to 5.1 T for reticular stimulation. On the other hand, the ratio of threshold for cortical stimulation in R E M P s compared with relaxed wakefulness was only 1.1. I f threshold in R E M P s is compared with that in sleep, it is 3.4 times greater for evoking vestibular movements, and 2.6 times as high for producing R F arousal. However, the ratio of thresholds for cortico-spinal movement in these two states is less than unity (0.76). t

4. Concurrent studies of threshold changes during various ECoG stages In some cases we examined thresholds for two, or all three types of stimulation in the same experiment. In this way we could avoid the complication of, e.g., variations in the states of consciousness, reactivity, or health of the animal from day to day, possible variations due to time of day, or other fortuitous changes. One such experiment is illustrated in Fig. 7, where thresholds for both cortico-spinal movement and for arousal by RF stimulation were carried out in the same, 21 h session. The data confirm the results presented earlier-- fall in thresh old for corticallyevoked movement from sleep to R E M P , and the opposite change for R F arousal thresholds. All three thresholds were studied in another, 6 h experiment (Fig. 8), during which the animal was in relaxed wakefulness twice, drowsy twice, and in sleep and R E M P s on 5 separate occasions. Each threshold obtained during the various stages was plotted against the appropriate behavioral and E C o G condition, marked on the abscissa. The increase in threshold from wakefulness to sleep is rather small for all 3 types of stimu-

243

~

J

'

1

loc t~

80

~ ~, ~

60

I.--

20

i'=

VESTIBULO-SPfNAL REFLEX

,0

o ...:.:...,

•

,, ,w,~E o ~.~~,,,s~ ~ ,,~f t~ ~ ,t~ i |5:30

I 16:00

15145

I 16:15

16:30

TIME

Fig. 5 Threshold changes for eliciting vestibulo-spinal neck movement in different behavioral and ECoG stages. Same cat as in Fig. 4, but on a different day. ECoG recording was continuous for the period plotted. Note contrast with cortical stimulation (Fig. 4) in direction of threshold change from sleep to REMPs.

Electroenceph. olin. Neurophysiol., 1965, 18:239-248

244

R. HODES AND J. I. SUZUKI

LF-O RF-P

A

LF RP - O

Thresh. Vestib.- Sp.= 30 V

EKG

13:58 I

r

,

i

,

INSR EXP.

B

Thresh. Vestib.- Sp.= 25 V

14'01

2 ~

11~'

Fig. 6 Higher threshold for vestibulo-spinal neck reflexes in a single REMP during bursts of eye movements (A) than in ocular quiescence (B). Contrast with Fig. 3.

Electroenceph. clin. Neurophysiol., 1965, 18:239-248

THRESHOLDS IN WAKEFULNESS, SLEEP AND REMP

60 -

I

'

I

,

I

'

I

'

I

'

J

I

•

~

so

"

,o

,/

/

X/ ~

-

:~'~

a0 "

ORT~CO s~,~l -

I11 ~ i

qb

i'~{I;-;~,,: ,~,, /-

~i

o-o

i!!

""%

°

......

~

~.SLEEP

~

REM

-

\

.

.

.

.

.

.

.

.

.

.

.

.

-

.

.

.

.

--

I

,

12:00

I

,

I

12:30

~

I

13:00

I

I

13:30

I

14:00

14:30

TIME

Fig. 7 Concurrent thresholds for cortical and R F stimulation. Overt arousal at asterisk. I

"

50

9

I

I

I

II

e

-

/ J ~

.

I

I e°CORTICAL

I o-VEST~aAR I I e-RETIC. FORM.]

40

30 G

-r

,

"*'

20

s

lO . . . . . . . . .o o .

,1 AWAKE

~

I

I

1

DROWSY

ASLEEP

REM

STAGES

OF ECoG AND

BEHAVIOR

Fig. 8 Concurrent thresholds for all 3 types ofstimulationin one observation and recording session lasting for 6 h. Details in text. DISCUSSION

The most important result presented in this paper is the fact that the neo¢ortical cells which initiate cortico-spinal movement have a lower stimulation threshold in REMPs than during

245

sleep. When eye movements are prominent, the heightened excitability of the motor cortex is especially striking and is only slightly less than that of quiet wakefulness. Even this somewhat lower excitability may be more apparent than real; for thresholds were judged on the basis of induced movements-- i.e., of the strength required not only to stimulate cortical cells but also to pass across the synapses of the spinal motoneurons whose excitability may actually be depressed (Hodes and Dement 1964). Our finding of an increased excitability of the neocortex in REMPs, compared with sleep, are indirectly supported by previous data. Although there is not necessarily a simple correlation between augmented spontaneous unit firing rate of visual and sensorimotor cortical units, which Evarts (1962, 1964), demonstrated during RE M Ps, and diminished threshold to electrical stimulation reported in the present paper, concordance of these indicators of neuronal function in the situation under consideration appears to be nearly complete. The work of Okuma and Fujimori (1963) and of Allison (1964) on cortical evoked potentials following stimulation of nuclei of the specific thalamocortical system also provide evidence of increased neocortical excitability during REMPs. Since motor threshold, spontaneous visual and sensorimotor cortical firing, and sensorimotor evoked activity all appear to be affected in an analogous fashion, the heightened excitability of the motor cortex in REMPs, compared with sleep, may be general for the entire neocortex. Hyperexcitability of the cortex which might lead to, or at least be concomitant with, "spontaneous" depolarization of its cells could account for the increased discharge over the pyramidal tract during REMPs (Arduini et al. 1963). The fact that sporadic, often uncoordinated, and apparently purposeless jerks of head, face and limbs occur at all in this state bears remarkable testimony to the exaggerated responsiveness of the cortical centers; for the final motor neurons which mediate such muscular contractions are depressed (Hodes and Dement 1964), and must only be capable of excitation by an overwhelming volley from above. Cortical mechanisms could also play some part in initiating the striking eye movements in the presumed orteiric (REM) phase. Electroenceph. clin. Neurophysiol., 1965, 18:239-248

246

R. HODES AND J. I. SUZUKI

Although Jouvet (1962) has shown that the cerebral cortex is not essential for eye movements in the phase rhombencdphalique du sommeil, the vigor of the movements is less in his decorticate, than intact, cats. From Jouvet's (1962) important contribution, we may suppose that certain pontile nuclei lay the basis for an excited cortex either by positive activation, by inhibition of mechanisms which inhibit cortical responsiveness in sleep, or both. Because REMPs are slightly reduced in the decorticate cat, it is probable that the activated cortex feeds back on the pontile RF to further enhance the latter's action. The reduction of cortical threshold in the R E M P is all the more impressive when viewed against the fact that, in the same animal and in the same stage, threshold for electrographic and behavioral arousal by RF stimulation is greatly increased. This result, which confirms earlier work, had been one of the main reasons for the belief that REMPs represent deepest sleep. The rise in threshold for evoking reflex movements of vestibular origin in oneirosis parallels that for arousal by RF stimulation. Increased threshold is not due to reduction of the afferent input to the vestibular nuclei, since the sensory input does not change from the waking state to sleep and the period of REMs (Huttenlocher 1960). The present results with polysynaptic vestibular reflexes are similar to the observations of Hodes and Dement (1964) on the human monosynaptic, electrically induced reflex (EIR), or "H-reflex". A single explanation would suffice to explain the increased thresholds for reticular and vestibular effects during REMPs. Direct stimulation of the R F shows that its excitability is depressed; the inference is strong that this is also true for the brain-stem mediators of the vestibular response. Huttenlocher's report (1960) that click-evoked potentials recorded from the mesencephalic reticulum are greatly reduced or abolished in the oneiric state would support the idea of depression of these regions at this stage of the cycle of consciousness. Although Okuma and Fujimori (1963) consider that activity of cutaneous origin is enhanced in the mesencephalic site, their results, nevertheless, appear to be in agreement with the earlier work if the late waves of the corn-

plex are used as an index of reticulai" responsiveness. The data of Okuma and Fujimori (1963) leave no doubt of the depression of the bulbar RF in the stage of REMs, since all components of the evoked response are less than at any other phase. We propose tl~t the active neocortex is responsible, in some measure, for the depressed excitability of brain-stem structures. Such a hypothesis is consistent with the concept expressed by Hugelin and Bonvallet (1957) and by Dell et al. (1961) of an inhibitory cortico-reticular loop for "reticular deactivation". Brain-stem depression would explain many features of the REMP. Reduction, or abolition, of reticular tacilitatory influence on the spinal motoneuron (Magoun and Rhines 1947; Peacock and Hodes 1951; Jung and Hassler 1960) would account for skeletomotor atony, and suppression of the ErR in the normal subject. If, at the same time, the brain-stem inhibitory influence on anterior horn cells (Magoun and Rhines 1947; Hodes et al. 1951 ; Jung and Hassler 1960; Jouvet 1962) were enhanced, depression of muscle tone and stretch reflexes would be still more profound. On the basis of reticular depression we may also appreciate why bodily movements in general are less in REMPs than in any other stage (Dement and Kleitman 1957), and also why RF stimulation during oneirosis reduces sporadic limb movements and eye and facial muscle twitches (Okuma and Fujimori 1963). The present work, together with some of tile evidence cited above, should help clarify the point raised by Moruzzi (1964): "To say that sleep becomes deeper during episodes of low voltage fast activity is an important conclusion, particularly in view of the fact that the E E G of the cerveau isold.., or of the cat during Nembutal anesthesia is exclusively dominated by classical patterns of cortical synchronization. Shall we conclude that the episodes of sleep with low voltage fast activity occurring in the normal cat are related to a depression of the cerebrum which is never attained during the coma produced by a midbrain transection or following injections of surgical doses of Nembutal? Common sense would lead us to reject such a conclusion, ..." Perhaps the difficulty with the prevailing concept on "depth of sleep" (see Hodes and Electroenceph. clin. Neurophysiol., 1965, 18:239-248

THRESHOLDS IN WAKEFULNESS~ SLEEP AND REMP

Dement 1964) which have prompted Moruzzi's comments is due to the failure to appreciate the essential distinction between the nature of sleep and oneirosis. For, we believe that oneirosis is not sleep of a different depth from that seen when the corticogram, e.g., is synchronous and slow, but is a process different in k i n d from sleep. The idea that sleep and dreaming are qualitatively distinctive processes may be supported by the contrasts in : ECoG, ocular and somatic muscle jerks, skeletal muscle tone, EIRs, spontaneous and evoked unit discharge, evoked potentials, arousal and movement thresholds, etc. In addition, dissimilarities have also been found between the two states in the following indicators of autonomic function: size of the pupil and retraction of the nictitating membrane (Berlucchi et al. 1964: Hodes 1964a); dilatation of the blood vessels supplying the cerebral cortex (Kanzow et al. 1962): and degree of fluctuation in heart rate, blood pressure, and respiratory rate and depth (Candia et al. 1962; Jouvet 1962; Snyder et al. 1963: Hodes 1964a). SUMMARY

1. Thresholds for evoking movement by stimulating cortex and vestibular nerves, and for behavioral and electrographic arousal by mesencephalic RF stimulation have been studied in 5 cats bearing implanted electrodes. These thresholds were recorded as the animals passed spontaneously from wakefulness into drowsiness, sleep, and low voltage fast E C o G and rapid eye movement periods (REM Ps). 2. Threshold for evoking cortico-spinal movement is lowest in the waking animal, increases in drowsiness, and becomes still higher in sleep. During REMPs threshold is lower than in sleep and is nearly as low as in relaxed wakefulness. 3. In a single episode of low voltage ECoG, threshold for cortico-spinal movement is lower during bursts of REM than in the periods of ocular quiescence. 4. Vestibular and RF stimulation thresholds increase from wakefulness to sleep similarly to cortical thresholds. By contrast, however, vestibular and RF thresholds are higher in REMPs than in sleep, and vestibular threshold is higher during REMs than in the lulls between bursts of ocular activity.

247

5. We conclude that the neocortex is activated during REMPs, compared with sleep. 6. Our findings, and other data suggest that sleep and REMPs represent qualitatively different processes rather than quantitatively different aspects (lightness or depth) of a single state of sleep. REFERENCES ALLISON, T. Cortical and subcortical evoked responses to central stimuli during wakefulness and sleep. Electroenceph, olin. Neurophysiol., 1965, 18: 131-139. ANTROBUS, J., DEMENT, W. and FISHER, C. Patterns of

dreaming and dream recall : an EEG study. J. abnorm. soc. Psychol., 1964, in press. ARDUINI, A., BERLUCCHI,G. and STRATA,P. Pyramidal activity during sleep and wakefulness. Arch. ital. Biol., 1963, 101: 530-544. ASERINSKY, E. and KLEITMAN,N. Two types of ocular motility occurring in sleep. J. appl. Physiol., 1955, 8: 1-10. BENOIT,O. et BLOCH,V. Seuil d'excitabilit6 reticulaire et sommeil profond chez le chat. J. Physiol. (Paris), 1960, 52: 17-18. BERGER, R. Tonus of extrinsic laryngeal muscles during sleep and dreaming. Science, 1961, 134: 840. BERLUCCHI, G., MORUZZI, G., SALVA, G. and STRATA, P. Pupil behavior and ocular movements during synchronized and desynchronized sleep. Arch. ital. Biol., 1964, 102:230 244. CANDIA, O., FAVALE, E., GIUSSANI, A. and Rossl, G. G. Blood pressure during natural sleep and during sleep induced by electrical stimulation of the brain stem reticular formation. Arch. ital. Biol., 1962, 100:216 233. DELL, P., BONVALLET, M. and HUGELIN, A. Mechanisms of reticular deactivation. In G. E. W. WOLSTENHOLME and M. O'CONNOR (Eds.), The nature o f sleep. Churchill, London, 1 % 1 : 8 6 107.

DEMENT, W. The occurrence of low voltage fast electro-

encephalogram patterns during behavioral sleep in the cat. Electroenceph. clin. Neurophysiol., 1958, 10: 291 296. DEMENT,W. An essay on dreams: The role of physiology in understanding their nature. In T. NEWCO~tB(Ed.) New directions in psychology, Vol. 11. Holt, Rhinehart and Winston, New York, 1964, in press. DEMENT,W. and KLEITMAN,M. Cyclic variations in LEG during sleep and their relation to cyemovements, body motility and dreaming. Electroenceph. olin. Neurophysiol., 1957, 9 : 673-690. EVARTS, E. V. Activity of neurons in visual cortex of thc cat during sleep with low voltage fast EEG activity. J. Neurophysiol., 1962, 25 : 812-816. EVARTS, E. V. Temporal patterns of discharge of pyramidal tract neurons during sleep and waking in the monkey. J. Neuroph3siol., 1964, 27: 152-171. GAROL, H. W. The "'motor" cortex of the cat.. J. Neuropath. exp. Neurol., 1942, 1: 139-145. Electroenceph. clin. Neurophysiol., 1965, 18:239 248

248

R. HODES AND J. I. SUZUKI

HODES, R. Ocular phenomena in the two stages of sleep in the cat. Exp. Neurol., 1964a, 9: 36-42. HODES, R. LOW~ cortical threshold in rapid eye movement periods than during sleep. Fed. Proc., 1964b, 23 : 208. HODES, R. and DEMENT, W. C. Depression of electrically induced reflexes (H-reflexes) in man during low voltage EEG "sleep". Electroenceph. clin. Neurophysiol., 1964, 17: 617-629. HOOES, R., PEACOCK JR., S. M., and HEATH, R. G. Influence of the forebrain on somato-motor activity. I. Inhibition. J. comp. Neurol., 1951, 94: 381-408. HOROVITZ, Z. P. and CHow, M. 1. Desynchronized electroencephalogram in the deeply sleeping cat. Science, 1961, 134: 945. HUGELIN, A. et BONVALLET, M. l~tude exp&imentale des interrelations r6ticulo-corticales. Proposition d'une th6orie de l'asservissement r6ticulaire ~ un syst6me diffus cortical. J. Physiol. (Paris), 1957, 49: 12011223. HUTTENLOCHER, P. R. Effects of state of arousal on click responses in the mesencephalic reticular formation. Electroenceph. clin. Neurophysiol., 1960, 12: 819-827. JOUVET, MR Recherches SUE les structures nerveuses et les m6canismes responsables des diff6rentes phases du sommeil physiologique. Arch. ital. Biol., 1962, 100: 125-206. JouvE7, M., MICHEL, T. et COURJON, J. Sur un stade d'activit6 61ectrique c6r6brale rapide au cours du sommeil physiologique. C. R. Soc. Biol. (Paris), 1959,

133: 1024-1028. JUNG, R. and HASSLER, R. The extrapyramidal motor system. In J. FIELD et al. (Eds.), Handbook of physiology, Sect. 1. Am. Physiol. Soc., Washington, 1960, 2: 863-927. KANZOW, E., KRAUSE, D., und KUHNEL, H. Die Vasomotorik der Hirnrinde in den Phasen desynchronisierter EEG-Aktivit~.t in natiJrlichen Schlaf der Katze. Arch. ges. Physiol., 1962, 274: 593-607. MAGOUN, H. W. and RHINES, R. Spastic#y: the stretch reflex and extrapyramMal systems. Thomas, Springfield, 1947, 59 p. MoRuzzt, G. Reticular influences on the EEG, Electro enceph, clin. Neurophysiol., 1964, 16:2-17. OKUMA, T. and FUJIMORI, M. Electrographic and evoked potential studies during sleep in the cat. Folia psychiat. neurol.jap., 1963, 17: 25-50. PEACOCK JR., S. M. and HODES, R. Influence of the forebrain on somato-motor activity. I1. Facilitation. J. comp. Neurol., 1951, 94: 409426. SCHWARTZ,B. EEG et mouvements oculaires dans le sommeil de nuit. Electroenceph. clin. Neurophysiol., 1962, 14: 126-218. SNVDER, F., HOBSON, J. A., and GOLDFRANK, F. Blood pressure changes during human sleep. Science, 1963, 142: 1313-1314. SUZUKI, J. and ConEy, B. Head, eye, body, and limb movements from semicircular canal nerves. Exp. Neurol., 1964, in press.

Reference: HODES, R. and SUZUKI, J, I. Comparative thresholds of cortex, vestibular system and reticular formation in wakefulness, sleep and rapid eye movement periods. Electroenceph. clin. Neurophysiol., 1965, 18: 239-248.