Transmission processes in the ventrobasal complex of rat during the sleep-waking cycle

Brain Research Bulletin, Vol. 5, pp. 553-562. Printedin the U.S.A.

Transmission Processes in the Ventrobasal Complex of Rat During the Sleep-Waking Cycle G. GANDOLFO, C. ARNAUD AND C. GOTT’ESMANN L~borato~

of ~sychop~ysi~~o~y,

Facula

of Sciences,

06034 Nice Cedex, France

Received 15 August 1979 GANDGLFO, G., C. ARNAUD AND C. GOTTESMANN. Transmission processes in the venfrobasd complex ofraf during the sleep-waking cycfe. BRAIN RES. BULL. 5(S) 553-562, 1980.-The thalamocortical reactivity and the transmission processes in the thalamic ventrobasal complex were studied during the different stages of sleep and waking. The mass responses of somesthetic Sl cortex and diencephalic relay nucleus were elicited by stimulation of the medial lemniscus with two shocks of identical parameters. The thaiamic afferents were studied by the amplitude of the lemniscal response induced by antidromic stimulation. The thalamocortical population response (tested by the amplitude of the positive surface 4 component of evoked potential) and the thalamic one (quantified by the amplitude of the postsynaptic rl wave) varied in a parallel manner. During waking without theta activity, the thahunocortical and thalamic responses were maximal. They significantly decreased in the course of waking with theta (active and/or attentive) for a part, at Ieast, because of a presynaptic inhibition of lemniscal terminals. During the different stages of slow sleep, thalamic transmission d~~shed to its minimal value during the intermediate stage which preceded and followed rapid sleep. During rapid sleep, thalamic transmission and cortical excitability significantly increased when the eye movements occurred in bursts, and the thalamic and thalamocortical excitability fell in part because of a depolarization of Iemniscal tierents. The recovery cycle of the thalamocortical and thalamic responsiveness was long, reaching 500 msec. Its variations in the course of the different stages of sleep and waking give some complementary indications of the functional modulation of diencephalic and telencephalic levels. The results are interpreted with respect to data in the literature pertaining to sleep-waking mechanisms in the rat. Sleep

Waking

Thaiamic &ansmission

Cortical responsiveness

THE first experimental step in the electrophysiological study of the brain has dealt with the recording of s~n~eous global activities related to behaviour. This has been done in many species, including the rat. The next methodological approach consisted of the study of cerebral evoked potentials induced by peripheral and central stimulation. Indeed, the global evoked responses of the brain reflect both the transmission of tierent information and its processing by the central nervous system. These population waves are important since they are more informative about the brain functioning, particularly the central level of activation and inhibition. Moreover, they can be an indirect criterion of brain storage mechanisms since the event-related potentials are able to be “emitted” by the brain when a stimulus announced, in a constant paradigm, is omitted 1731. Up to now, the induced ~pulation waves of the brain were seldom studied in the rat in relation to behaviour. We therefore began the analysis of the fluctuation of the central responsiveness during the stages of sleep and waking. We first chose the somesthetic specific system for, in this rodent, precise histological, electrophysiological and somatotopic studies have been done at S 1 cortex [19,3 1,32, 33,39,74,761 and ventrobasal[7,8,14,17,42,43,56,61,72] levels. We previously studied [9,10] the global excitability of

Copyright

@ 1980 ANKHO

International

Rat

the Sl cortex; here we describe the ventrobasal of afferent messages.

modulation

METHOD

Rat Surgery The experiment was carried out on 29 male Wistar rats weighing between 200 and 300 g. Fifteen animals were used

for the thalamocortical responsiveness study and fourteen for the thalamic level alone; of the 14, eight were used for the ventrobasal postsynaptic response and six for the lemniscal presynaptic one. At first, the rats were anesthetized by means of an intraperitoneal administration of sodium pentobarbital (45 mg/kg). In order to determine the amplitude of th~~oco~c~ responses, a deep multipolar electrode was stereotaxically implanted in the medial lemniscal tract at: anterior 3.2; lateral 2; depth +3 [3]. For the thalamic population wave study one multipolar electrode was inserted in the ventrobasal complex (anterior 3.8; lateral 3; depth 0) and a second was placed into the medial lemniscus (anterior 1.4; lateral 1.2; depth -4.75) according to Pellegrino and Cushman 1511. These deep electrodes were made up of several insulated (except at the tip) stainless steel wires (81100

Inc .-0361-9230/80/050553-10$01.50/0

5.54

GANDOLFO,

mm) fixed in a guide tube (4110 mm exterior diameter). They extend beyond the tube a predeterminate length in order to explore an approximate 1 mm zone. The optimal localization of the lemniscal electrode was verified by mechanical stimulation of the contralateral whiskers; the induced spikes were observed on a scope and with the aid of a loud speaker, This electride, in the still anesthetized animal, then was used to determine the optimal position of the ventrobasal electrode and somesthetic cortex electrode; we retained the ventrobasal and somesthetic Sl recording site which showed the population wave of largest amplitude and shortest latency. A similar procedure was used to define the site of the implanted electrode to study the lemniscal antidromic population wave induced by ventrobasal stimulation. In the latter case, it was carefully examined to see if the stimulation induced a movement, to avoid any diffusion to motor neurons. It was also verified in the later chronic animal. Silver balls of one millimeter diameter were placed on the frontal, parietal (Sl) and occipital cortex. The cortical evoked potentials being recorded monopolarly, a reference electrode was implanted in the middle plane, in front of the olfactory bulb. Two ocular electrodes, made of silver balls, were placed on the horizontal plane on both sides of one orbit; two myo~aphic electrodes (thin twisted wires of stainless steel) were inserted in the dorsal neck muscles. Finally, all electrodes were coated with an acrylic resin fixed on the skull. After surgery the animals were housed in individual cages with natural lighting. After several days, habituation to the recording cable began. Stitnrdufion

Parameters

and Response

Measurement

The determination of population responsiveness was calculated by summation of 64 evoked potentials (or twice 32) in every behavioural stage. Stimuli were sub-maximal and separated by at least 2 sec. These were rectangular pulses of 40 to 100 psec, and a constant current intensity of about 50 KA, situated from 2.5to 30% above the response threshold in the state where the amplitude was lowest, to obtain a clear response in all stages. The thalamocortical population wave recorded monopolarly was quantified by the mean amplitude of component 4, induced in the somesthetic S1 cortex by temniscal stimufation (Fig. 11. The component was measured from inflection to peak 1201.The rl component (Fig. 1) of the response elicited in the ventrobasal complex by lemniscal stimulation was recorded mono and/or bipolarly and measured from peak to base. The thalamic input was tested by the antidromic lemniscal response evoked by ventrobasal stimulation. The recording was also done with mono and/or bipolar derivation. The response was quantified by the amplitude of the first component measured from the baseline to the peak (Fig. 2). The study of the recovery cycle of thalamocortical and thalamic responsiveness was done by utilizing the same stimulation parameters for conditional and test stimulus. ~e~uviot~rul

ARNAUD

AND GOTTESMANN

FIG. 1. Population response of the thalamic ventrobasal complex and of the somesthetic Sl cortex to electrical stimulation of the medial lemniscus. Top: the cortical evoked potential induced by the lemniscal stimulus is made of several components. Only the first four are represented. Bottom: the thalamic response consists of two components of which the first, tl, betrays the (presynaptic) response of lemniscai terminals. The second one, rl, (postsynaptic) testifies to thalamic output. Note that the peak of thalamic rl wave precedes that of the cortical spike-like deflection (wave 1). The two responses were recorded by monopolar derivation, the positivity being down. Vertical bars represent the criterion used for the quantification of the results. Ca~ibrat~oa: 2 msec; 100 pV.

as sleep deepens (SP); (5) intermediate stage, characterized by frontal spindles of large amplitude and theta activity at the occipital level 1251; this stage precedes and follows rapid sleep (stages 3 to 5 are called slow sleep); (6) the rapid or paradoxical sleep without eye movements (Rl); (7) the rapid sleep with eye movement bursts (R2). Statistical

Analysis

It was first done by means of the analysis of variance (F-test). It was carried out on the mean interstate value of each rat (x/M). The F value was: (a) for the component 4 of the thalamocortical response: F=34.91,p<0.001; (b) for the thalamic rl component: F=19.05, p
Stages

The cortical and thalamic population waves were analyzed during the seven stages of the sleep-waking cycle distinguished in previous studies [25,28]: (1) waking with theta activity (5-9 cisec) at the occipital level; this stage is called active and/or attentive wakefulness (AW); (2) waking without theta (NA); (3) sleep with slow and large amplitude cortical waves which defined the fist stage of sleep (SW; (4) frontal spindles [67] with amplitude and duration increasing

Histology

At the end of the experiment and after pentobarbital overdose, a weak electrolytic lesion (1 mA during 5 set) was performed to visualize the deep electrode tip. The animal was then perfused with potassium ferrocyanide via an intracardiac cannula. The histological control of the deep electrodes was made on frozen brain slices mounted, unstained, in glycerin.

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SLEEP

FIG. 2. Lemniscal evoked potential to electrical stimulation of the ventrobasal complex. Top: the antidromic response was recorded by bipolar derivation. The vertical bar indicates the criterion used for the quantification of the results. Bottom: corresponding position of the stimulating (left) and recording (right) electrodes. Uncolored frozen slice. Calibration: 1 msec; 25 ).LV.

RESULTS THALAMOCORTICAL

RESPONSES

in the somesthetic Sl cortex by stimulation of the medial lemniscus consisted of three fast and early deflections of positive polarity; they were followed by two waves of large amplitude, the first being positive and the second negative. The spike-like component reflecting the level of thalamic output had a peak latency of 0.79 msec ? 0.14 (mean value and standard deviation). The peak of the intracortical late components 4 and 5 occurred with respective latencies of 5.45 msec * 0.47 and 9.80 msec + 1.15 (Fig. 1). The evoked

Variation

potential

of Wave 4 Amplitude

(Figs. 3 and 4); it notably increased in waking without theta during which this amplitude was the highest of all sleepwaking stages. Slow sleep. The amplitude of component 4 was low during the cortical slow waves. It decreased a little during spindles. The amplitude was lowest during the intermediate stage. Rapid sleep. The amplitude of wave 4 was larger than during the slow sleep stages. During the eye movement bursts of rapid sleep, the amplitude of wave 4 significantly decreased. Variability

A

induced

Waking. The amplitude was very low during theta rhythm

Intrastate

R/Y

(Fig. 4)

The superimposed five cortical responses recorded during the different behaviour stages show that the greatest varia-

1.

t

t

,.

lr RI

I)

FIG. 3. Quantitative analysis of the amplitude of the positive surface component 4 of the cortical evoked potential elicited on the somesthetic SI cortex by lemniscal stimulation. Mean amplitude and standard error of the mean @EM). x/M: amplitude relative to interstate mean (NS: not significant). Abbreviations: AW, waking with theta activity in dorsal hippocampus and visual cortex (active or attentive); NA, waking without theta; SW, sleep with slow cortical waves of increasing amplitude (stage which follows falling asleep); SP, frontal spindles which occur as sleep deepens; IS, intermediate stage which precedes and follows the rapid sleep (characterized by frontal high spindle bursts and a theta activity in the dorsal hippocampus and occipital cortex); Rl, rapid sleep without eye movements; R2, periods of rapid sleep with eye movement bursts.

556

GANDOLFO,

AW

ARNAUD

AND GO~ES~ANN

NA

150ms

250ms

350ms

450ms

550ms

-$K&.+

FIG. 4. Variability in different stages ofsleep-wukefa~ness and recovery cycle of the evokedpotential indwed on the somesthetic Sl cortex by kmniscal stimulation. Response to the conditioning stimulus (top): it is during waking with theta and the di&!rent stages of slow sleep (SW, SP, IS) that the variability of component 4 is the most important. Response to the test stimulus at different latencies: the recovery cycle of component 4 is extremely long; it clearly begins at first during the slow sleep stages at 250 msec; for the rapid sleep, it is still uncomplete at 550 msec. For abbreviations, see Fig. 3. Cu~jbratio~: 10 msec, 500 *V.

4

bility occurred during the slow waves, spindles and the intermedite stage, thus during slow sleep. Recovery Cycle of Thalamocortical

Responses

(Fig. 4)

Up to 150 msec intershock interval, the test stimulus essentialiy induced the earliest components (1 and 2) of the cortical evoked potential, regardless of the behavioural stage. At 250 msec, a partial recovery appeared (in fact, principally of wave 5) during the different stages of slow sleep, The recovery of waking stages began at 350 msec and the rapid sleep stages were still far from total recovery at 550 msec.

M

t

t

0.

ts.

THALAMIC~NSMiSSI~N Postsynaptic Response The respective latencies of the two most rapid components of the thalamic evoked potential elicited by Iemniscal stimulation were 0.71 msec ? 0.08 (mean and standard deviation) for the peak of the presynaptic component tl and 1.30 msec 2 0.25 for that of the postsynaptic rl wave.

0

AW

NA

I SW

SP

w IS

Rl

A2

FIG, 5. Statistical analysis of amplitude variations of thalamic postsynaptic rl component induced by iemniscal srimulation, Mean amplitude and dispersion (SEM). x/M: amplitude related to the interstate mean value. For abbreviations, see Fig. 3.

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SLEEP

RECOVERY

150ms

250ms

350ms

450m

s

550ms

L

AW

NA

SW

SP

IS

RI

R2

FIG. 6. Study of the ~ntrustafe ~arjabiiity and recovery cycle of the post~yaaptic rl component induced in the ventrobasal complex by lemniscal stimulation. Response to the conditioning stimulus (top): the most important variability is observed during waking with theta, the different stages of slow sleep (SW, SP, IS) and the eye movement bursts of rapid sleep. Response to the test stimulus: the recovery cycle is extremely long since the rl wave is still diminished at 550 msec during rapid sleep. For abbreviations, see Fig. 3. Ca~ibrat~un: 2 msec, 100 pV.

Variation af the Amplitude of the rl Wave Only the thalamic responses where the peak of the component rl preceded that of the spike-like wave 1 of the evoked potentiai induced on the Sl cortex by the same lemniscal stimulations were taken into account (Fig. 1). Waking. During waking without theta (Figs. 5 and 6), the amplitude was larger than during other stages of the sleepwaking cycle. Slow sleep. During the slow wave phase, the amplitude of the rl component was low. It decreased during spindles and reached the lowest value during the intermediate stage. Rapid steep. The component rl markedly increased,

compared to the stages of slow sleep. During the short periods of eye movement bursts, the responsiveness significantly decreased. intrastate

Variability

As for the th~~oco~~c~ responses, the dispersion in amplitude of component rl was greatest during the different stages of slow sleep (Fig. 6). Recovery Cycle of rl Component A conditioning stimulus resulted in a long-lasting depression of the component rl to the test stimulus (Fig. 6). At 150

GANDOLFO,

55x

msec of interstimulus interval, no responses recovered. Later on, the responses occurring during slow sleep, waking with theta and eye movement bursts of rapid sleep, began to recover earlier than those of waking without theta and rapid sleep without eye movement bursts. At 550 msec interstimulus interval, all states recovered except the two stages of rapid sleep.

ARNAUD

AND GOTTESMANN

t

Presynaptic Response

The lemniscal population wave induced by ventrobasal antidromic stimulation is made up of two components; their respective peak latency was 0.28 msec ? 0.10 (mean and standard variation) and 0.61 msec -e 0.12. During the sleep-waking cycle, two stages showed significantly higher amplitudes: waking with theta and periods of eye movement bursts of rapid sleep. These two behavioural stages are thus characterized by a thalamic presynaptic inhibition (Fig. 7). The intrastate variability of this presynaptic component was also the highest during these two stages (Fig. 8). DISCUSSION Methodological

Comments

To study the thalamocortical global responsiveness, we chose to quantify the amplitude of the fourth component of the population wave induced by lemniscal stimulation. We previously used the same criteria to test the Sl cortex excitability after the stimulation of the somesthetic radiations; indeed, this positive-surface wave reflects intracortical postsynaptic events as shown by slow potential variations and the firing of cortical neurons [lo, 32, 331. As Evarts did [20], its amplitude was measured from inflection to peak. This method does not quantify the entire postsynaptic events of positive-surface polarity as would be the case by measuring the amplitude between the inflection of wave 3 and the peak

AW

NA

SW

SP

of the ventrobasal

variability of the lemniscal response elicited by stimucomplex. During waking with theta and periods of eye

movement bursts of rapid sleep, the amplitude and the dispersion of the presynaptic component are most important. For abbreviations, see Fig. 3. Calibration: 1 msec, 25 GLV.

Rl

R2

of wave 4. Nevertheless, we selected this postsynaptic unquestionable criterion since the inflection of wave 3, essentially during waking with theta, was often more positive or less negative than the inflection of wave 4. This could be the consequence of a negative shift of cortex polarization during this behaviorally active stage [77]. The rl ventrobasal component reflects the output of the somesthetic relay nucleus [ 11,641. We verified this by means of a repetitive lemniscal stimulation at high frequency (615 c/set); it abolished or markedly attenuated this component without changing the amplitude of the presynaptic t 1 component. The r 1 wave was measured from peak to base; indeed, the variation in size of the peak was very low whereas the amplitude of the base of the population wave was highly reactive during the different sleep-waking stages. Moreover, it varied in exactly the same way as the peak amplitude. Similar observations were made in cats: Allison [4] also quantified the rl component from

FIG. 8. Study of the intrastate lation

IS

FIG. 7. Statistical analysis of the thalamic presynaptic component amplitude. Mean amplitude and dispersion @EM). x/M: amplitude related to the interstate mean value. For abbreviations, see Fig. 3.

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SLEEP

peak to base. Howe and Sterman [34] dissociated on the one hand, a wave “two” corresponding to the peak amplitude referred to baseline and on the other hand, a wave “three” corresponding to the base also referred to baseline. They showed that these two waves present similar variations in size during all phases of the sleep-waking cycle. Finally, Steriade used the same criterion to quantify this thalamic postsynaptic component (personal communication). The thalamic input was tested by the lemniscal mass response induced by ventrobasal stimulation. This antidromic population wave is built up of two components and several arguments suggested that they correspond to different fiber velocity: the stimulation never induced motor activities and the latency of the two components was too short to support mediation of the neocortex. Finally, the acute and chronic homolateral decortication did not affect the response shape in spite of important changes during the sleep-waking cycle (in preparation). As in the cat [ 161, we used the amplitude of the first peak, from base to peak, to measure the polarization state of lemniscal afferents. Result Comments

The comparison of evoked responses induced on the somesthetic Sl cortex by electrical stimulation of radiations [9,10], and of medial lemniscus, often allows the differentiation of influences originating from cortical and thalamic levels. Nevertheless, only a specific analysis of the ventrobasal complex transmission detects the neurophysiological origin of the modulation of the thalamocortical massresponses. In other respects, only intracellular recording gives satisfactory information for neurophysiological interpretation; but this technique is difficult in the free moving animal [24,49]. Consequently, the reasoning in this discussion will necessarily rely on indirect arguments. Waking

From waking without theta to waking with theta, the component 4 of the cortical evoked potential elicited by stimulation of the radiations [9,10] or the lemniscus decreased. The analysis of the thalamic transmission, tested by the orthodromic and antidromic method, indicates that this parallel evolution depends on both cortical and thalamic processes. The cortical ones are most likely postsynaptic because of the amplitude stability of the evoked spike-like component 1 induced by the stimulation of the radiations [9,10]. The lowered amplitude of wave 4 during waking with theta is probably the result of the activation of cortical inhibitory intemeurons [40, 41, 52, 651. The reduction of ventrobasal transmission during theta could result from surrounding inhibition [36,37] arising, for example, from kinesthetic afferents [69] or from thalamic integrative regions [ 1,38,55]. Of course, thalamic transmission could also be modulated by corticofugal inhibitory influences [S, 6, 7, 81 coming from pyramidal fibers 162,701 originating partly from somesthetic Sl cortex (1501 for the cat, [751 for the rat). The important point is that, as shown by our results, at least one part of this restraining process is the consequence of an inhibition of presynaptic nature (remember that in the rat both ascending and descending fibers entering the ventrobasal complex show axo-axonic terminals [611). In our experiment the cortical control of ventrobasal transmission also appeared in the recovery cycle analysis. Indeed, the thalamic values are of longer duration than those obtained at cortical level [9, lo]. A possible function of this twofold intracortical and thalamic

control of somesthetic atferents could be to focus the perceptive field on other sensory modalities, [30] possibly the kinesthetic [69] or the olfactory ones, the rat being a macrosmatic. To our knowledge, no work has been done in the chronic cat on the central excitability with and without theta activity (Tokizane’s group only compared the variation in amplitude of the thalamocortical responses related to hippocampal electrophysiologic patterns of different frequency in the acute animal [68]). Nevertheless, cortical [15] and thalamocortical [18] reactivity, in the visual modality, decrease when the cat comes from “arousal” to a stage of lasting, oriented waking which is generally concomitant with theta activity in the rat. Slow Sleep

The thalamocortical and thalamic postsynaptic reactivity observed in the rat is weak; this is probably related to a diminution of ascending facilitatory influences originating from the brainstem [48] which in the rat is correlated to a lowering of cellular activity in that part of the brain [45]. This lowering in the rat probably leads to the suppression of disinhibitory influences identified at the cat ventrobasal [551 and lateral geniculate [63] levels. The reactivity is minimal during the intermediate stage, as compared to all other sleep-waking phases. This result is in favour of a neurophysiological similarity between the acute “cerveau isole” [12] and the intermediate stage of sleep [25,27]: in these two states, frontal spindles of large amplitude and duration coexist with theta rhythm in the dorsal hippocampus and occipital cortex [23,29]. The thalamocortical recovery cycle shows that the response to lemniscal test stimulus first appears during the slow sleep stages; this seems more precisely to be the case for the component 5, negative surface. In cats 1401 and rats [9,101, the rate of true cortical recovery is an inverse function of the response amplitude to the conditioning stimulus. Consequently, we suggest that from the moment the ventrobasal gate is “half opened” to the test stimulus, the cortical response level may make the differences since during slow sleep stages the lemniscal conditioning stimulus only induces at the cortical level a very low amplitude response, and the ability of Sl area to respond to the test stimulus is still high. In the rodent studied here the inhibition certainly acts at thalamic postsynaptic level, since we were unable to detect any significant presynaptic inhibition during these behavioural stages. Rapid Sleep The increase in the thalamocortical reactivity during rapid sleep, also noted in the cat 12, 21, 571, as compared to the different stages of slow sleep, is consecutive to thalamic processes as shown by the increased amplitude of the postsynaptic rl component. This is a process limited to the diencephalon since the cortical responsiveness does not vary throughout rapid sleep at the level of the somesthetic Sl area [9,101 nor at the visual primary area (unpublished data). In the cat, the rising amplitude of the cortical evoked potentials during the eye movements of rapid sleep ([21, 34, 591 for vision), is concurrent with electrophysiological phasic activities, i.e., with ponto-geniculo-occipital spikes or eye movement potentials (113,601 for vision). Since the rat does not display cortical spikes during rapid sleep [25, 26, 661 our previous result appeared logical. Now at the thalamic level, our data were unexpected for the same reason: it is well known that in the cat, the thalamic transmission is most

560

often facilited during the eye movement bursts of rapid sleep (211 and correlated with spikes in the lateral geniculate nucfeus [35,58]. This facilitation is the consequence of an increase in the postsynaptic neuron excitability [l&22] which masks a presynaptic inhibition ([ 16,22,35] and [58] for visual system). Since the rat does not display thalamic spikes during rapid sleep [25, 26,661, we expected no change in transmission level throughout this phase of sleep whereas lowering was observed during the eye movement bursts. This diminution also appears at the lateral geniculate nucleus (unpublished data). We have already noted that the increase of thalamic transmission during rapid sleep (particularly with regard to the intermediate stage) is also related to the tonic activation of the dorsal parasagittal pons [25,26,46,71]; the eye movement bursts of rapid sleep being consecutive to and accompanied by a transient pontine ove~~tivation [25,26], the correlative decrease of the thalamic transmission can with difficulty result in a reduced postsynaptic facilitation. In all likelihood it should only be the consequence of the presynaptic inhibition, identified by the antidromic stimulation of lemniscal terminals. The precise central origin of the presynaptic moduIation is still unknown. Nevertheless, in the cat, the eye movement bursts of rapid sleep, and the correlative spikes in the thalamic relay of vision are under control of the vestibular complex [47,53]. It is worthwhile to mention that the cellular activation which occurs there during these phasic motor activities is also responsible for a presynaptic inhibition of the spinal proprioceptive afferents 1541; hence as postulated by Marchiafava and Pompeiano 1441 for the visual system in the cat, it seems to us that the thalamic presynaptic depolarization might be of pontine origin in the rat. Perhaps, instead of a true vestibular source, it could be the direct or indirect consequence of the cellular

1. Albe-Fessard, D. and A. Fessard. Thalamic integrations and their consequences at the telencephalic level. In: Brain Mechanisms, Progress in Brain Research, Vol. I, edited by G. Moruzzi, A. Fessard and H. H. Jasper. Amsterdam: Elsevier Publ. Co., 1%3, pp. 114-148. 2 Albe-Fessard, D., J. Massion, R. Hall et W. Rosenblith. Modifications au tours de la veille et du sommeil des valeurs moyennes de reponses nerveuses centrales induites par des stimulations somatiques chez le Chat libre. C. R. hebd. sPanc. Acad. Sci, Paris 258: 353-356, 19&l. 3. Albe-Fessard, D., F. Stutinsky et S. Libouban. Atlas St&iotaxique du Dienckphale du Rat Blanc. Ed. CNRS, 1966. 4. Allison, T. Cortical and subcortical evoked responses to central stimuli during wakefulness and sleep. Eiectroenceph. clin. Ne~rop~ysio~. 18: 131-139, 1965. 5. Andersen, P., C. Brooks, J. C. Eccies and T. A. Sears. The ventrobasal nucleus of the thalamus: potential fields, synaptic transmission and excitability of both presynaptic and postsynaptic components. J. Physiol., Lond. 174: 348-369, 1964. 6. Andersen, P., J. C. Eccles and T. A. Sears. The ventro-basal complex of the thalamus: types of cells, their responses and their functional organization. J. Physiot. Lond. 174: 370-399, 1964. 7. Angel, A. Evidence for cortical inhibition of transmission at the thalamic sensorv relay nucleus in the rat. J. Physiol., Land. 169: 108-109, 1963. _ 8. Angel, A. and K. A. Clarke. An analysis of the representation of the forelimb in the ventrobasal thalamic complex of the albino rat. J. Phy~~ial., Land. 249: 399-423, 1975.

GANDOLFO,

ARNAUD

AND GOTTESMANN

overactivation of the dorsal parasagittal pons, since barbiturates at low doses suppress for a while this pontine activation and the eye movement bursts. The pontine ascending influences of rapid sleep could end in the lemniscal terminals after going all along the longitudinal posterior fasciculus which passes close to the third and sixth nucleus and there induces the spikes correlated with eye movements [25,26]. In any case, these influences do not ascend in a diffuse way into the lateral reticular formation: indeed, a massive bilateral electrolytic lesion of this structure suppresses the frontal cortex desynchronization of rapid sleep for several days, but spares the eye movements of this sleep stage (251. A pontine origin of the thalamic presynaptic inhibition, also invoked by Sakakura and Iwama [SS] for visual modality is then possible. However, nothing allows us to exclude the possibility of a cortical origin [22]. The recovery cycle of the thalamic postsynaptic response induced by lemniscal stimulation is very long during rapid sleep. It is during the eye movement bursts, so during the presynaptic inhibitory process, that the recuperation first appears. This result is also available for waking, during which the recovery occurs at first in the presence of theta, thus again, during a presynaptic inhibition; it suggests that the presynaptic inhibition issued from the pons could spare some ventrobasal neurons from activation. Yet, a subliminar facilitation induced by the conditioning stimulus would increase their probability of activation by the test stimulus. However, a cortico-thalamic positive feedback released by the conditioning stimulus [62] can not be excluded.

ACKNOWLEDGEMENTS I wish to express my thanks to Professor M. Steriade for his helpful criticism on the previous manuscript. C.G.

9. Amaud, C. and C. Gottesmann. Somesthetic cortex reactivity during sleenina and waking in the rat. Experientia 34: 15!341585,_1978._ 10 Amaud, C., G. Gandolfo and C. Gottesmamr. The reactivity of the somesthetic SI cortex during sleep and waking in the rat. Brain Res. Balk 4: 735-740, 1979. 11. Bishop, P. 0. and J. G. McLeod. Nature of potentials associated with synaptic transmission in lateral geniculate of cat. J. Neurophysiol. 17: 387-414, 1954. 12. Bremer, F. “Cerveau isole” et physiologic du sommeil. C. r. h&d. Siam. Sot. Biol. Paris 118: 1235-1241, 1935. 13. Calvet, J., M. C. Calvet and J. M. Langlois. Diffuse cortical activation waves during so-called desynchronised EEG patterns. J. Nearophysiol. 28: 893-907, I%5 14. Clark, W. E. Le Gros. An experimental Study of the Thalamic Connections in the Rat. Philos. Trans. B222: l-28, 1932. 15. Cordeau, P., J. Walsh and H. Mahut. Variations dans la transmission des messages sensoriels en fonction des differents &tats d’bveil et de sommeil. In: Neurophysiologie des Hats de Sommeil, CNRS Edit., Lyon: CNRS, 1965, pp. 477-507. 16. Dagnino, N., E. Favale, C. Loeb, M. Manfredi and A. Seitun. Presynaptic and postsynaptic changes in specific thalamic nuclei during deep sleep. Archs ital. Biol. 107: 668-684, 1%9. 17. Davidson, N. The projection of afferent pathways on the thalamus of the rat. J. camp. Neurol. 124: 377-390, 1%5. 18. Dumont, S. and P. Dell. Facilitations specitiques et non spdcifiques des responses visuelles corticales. J. Physiol., Paris SO: 261-264, 1958. 19. Emmers, R. Organization of the first and second somesthetic regions (SI and SII) in the rat thalamus. J. camp. Neurof. 124: 215-228. 1965.

SOMESTHETIC

RESPONSIVENESS

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