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Rhythmic slow wave activity recorded in the ventral mesencephalic tegmentum in the rat
Electroencephalography and Clinical Neurophysiology, 1975, 38:139 -147 4 Elsevier Scientific Publishing Company, Amsterdam Printed in The Netherlands
139
R H Y T H M I C SLOW WAVE ACTIVITY R E C O R D E D IN THE V E N T R A L M E S E N C E P H A L I C T E G M E N T U M IN THE RAT M. LE MOAL AND B. CARD() Lahoratoire de Psvchophysiologie, University; de Bordeaux l. Avenue des Facultds, 33405 Talence (France)
(Accepted I\~r publication: August 18, 1974)
In recent years anatomical studies (Nauta 1958; Nauta and Kuypers 1958) have made it possible to link the limbic system with an important mesencephalic region including the ventral mesencephalic tegmentum (VMT), the nuclei of the anterior raphe, the nuclei of Gudden and the ventral part of the central grey matter. The functions of this "'limbic midbrain area" (Nauta 1958) are still relatively unknown. Some recent data, however, attribute to the VMT characteristics which are peculiar to the limbic system (Karli 1968); thus, after VMT lesions, hyperactivity, difficulty in inhibiting previously acquired behaviour and perseveration are observed (Le Moal et al. 1969, 1970). Furthema0re, no electrophysiological study of these structures has yet been made in the freely moving animal with chronically implanted electrodes. In order to improve our knowledge of these mesencephalic areas, we have carried out electroencephalographic recordings (EEG) from the VMT by means of large electrodes. These records were taken in the course of various behavioural sequences and during paradoxical sleep (PS).
METHOD AND MATERIAL
Animals and surgery
Thirty-four male rats of the Sprague-Dawley strain were used. The implantation of electrodes was done under deep Pentothal anaesthesia (80 mg/kg i.p.). After the operation the animals were housed in individual cages at constant temperature (22°C). Stereotaxic coordinates anddistribution of animals
Besides the VMT, cortical or subcortical electrodes were implanted in 2 or 3 of the following structures: medial septum (MS), dorsal hippocampus (Hpc), antero-ventral thalamus (TAV) and lateral hypothalamus (LH). Cortical electrodes made of chloride-plated silver wire 0.2 mm in diameter, insulated except for the end 0.3 ram, were placed in the bi-occipital (bi-occ) or occipitofrontal (occ-fr) cortex. In certain rats electrodes were inserted into the cortex in order to record by diffusion the activities of the dorsal hippocampus (Jouvet 1967 ; Parmeggiani 1967 ; Yamagushi et al. 1967). The bipolar subcortical elec-
]'ABLE I Stercotaxiccoordinates of implantations (ram) Structure
Antero-posterior*
Lateral*
Vertical**
Medial septum Antero-ventral thalamus Lateral hypothalamus Dorsal hippocampus Ventral tegmentum
A 2.0 P 0.6 P 0.6 P 2.4 P 4.3
0.0 1.8 1.7 2.7 0.5
6.2 6.5 8.5 3.0 8.6
* From bregma. ** Belowthe skull.
140
t iodcs ~\ crc nlack: of t\~istcd pallacliunl-tungstcn wirc~, 0.15 111111in dianlcler, insulated cxccpl for 111cend 0.3 n1111.Tho coordinates ol'inll-~lanlalion arc' lisicd in Table I. 7ix ral s iccoi~ cd a 111Ollopolar il>Uklted slainlcss-slccl electrode, dkuneior 0 2 ii111/ \~ith ~l 0.4 111111point, ill the MS. By 111CLIllSol'lhis clcctrodc. coagulation ol'lhis strucl ure \vould later be made. All the elcc/iodcs were soldered to a inicrominint tll't_" 5-pin tI'allSisloF socket and sterilized [)c.'t'OlC lhc opcrcltion. Thc \~hole impkll~t \~;is l]xcd to lhc skull \~ ith anchoring scIo\~ s and acrylic rosin. t{\01\' ral had an electrode in II~e V M T . 13 r:.ils had an clccilodc ill the L t l , 5 had o11c in the ltpc. 5 in ihe MS and tho TA\.;. 5 in the [ , , \ V and Iho t lpc. The f, rats having a coagulalion electrode in the M S also had recoMing electrodes in tile mcsenccphalon and the lhalalmis. The lesions oF tile MS were nlade rind,21 anaesthesia b,, ;i radiol'requcncy (500 kc sec CtlITC!]I t'd" 50 /~,.'\ xxhich klstcd I\)r .'2_sec.
Rccom/illg.v All file recoldillgs \~ele made 111a soundprool" cabin, ol'x~ hich c)ne side was transpalcnt It) nllo\~ obscr\'alioll of the aninlal. The 11oo1 o1" the recoMing ccitt consisted in a hydraulic lnattress which /iansn]itlcd c\or\.' nlO\'enlcnt of 111c ral as a pressure \ a r i a l i o n to a lransduccr and I'roni there to one of the a11~plil]ers of the electroencephalograph. The serisii ivity was increascd \~ hen lhc ailimal ~as asleep, in order to record its smallest inovenlents, especially during F'S. The clectrodcs \\erc electrically connected to the rccordhlg a p p a r a t u s , b y a nlobilc mercury con-nector. The records were made with a differential clccl roon copha logra p h. Iirst. the anilnals x~ere recorded during the I\~llm\ing acti~hies: eating, snifl]ng, exploring. cleaning and licking, a\takening caused bv the cxpcrilnenter or by' central electrical stimulalion. Tllcn. various recordings were perfornlcd during bolh sl;./los of slcep. Finally the EEO activit'ios v, erc cOillparcd befoFe and after sepial coagulation. AI the end of ihc experiment the aninlals \x ere anaesthetized \~ith Pentothal and killed by' transcardiac per fusion o f a 10 o <,formol solution. Then the brain \x as renloved and the histological cont l'OiSwere nladc (N issl-stain ). The electrode phice-
xI. i i M ( i A I
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IllClIIs arc indicated in the di',tgrilms placed at lllc beginlling of tr:.lcing>, these cli:.lgr',in> ;.11-c_' lakcn l'ronl KGnig ;.llltt Klippcl (1%31 (scc Results). R I M I IV;
1. I@corditlg /)~,l~ rlw J.AI7 dminft r~,lot~ ~w/iril h c mtchlgs \\crc c]lalacieri/cd b\ lhc appeara l l o t LIIIdcI CC1!aill bcJ1~1\ iOLll"al CiICHI11S|~IIICCS c)[
1hvthmic sire\ acfi,~il\ (RSA)',1i fl X c scc ofthe lhcb:l type. l'ig. I ~ho\\~ ~o111c cXaml~Ics, lu i the rat is iImoduccd into lhc cage and cxph)rcs: at the same lime P,SA appears in the \ r M T x~h i l t
the cortex and the h>pothahmlu,~ ~,ho\x small amplitude irregular activi/\ (SIAL t11 B l b o d is introduced inlo the cage of an animal depJivcd ol'[k~od [br 24 h: at first Ihc l'~|! looks 1i~1lhc l'ood \x hich it snilT~ ;,li: RSA appccu>, hi the VMF, the \xa\cs 'arc large, a[ 7 c see: then the anhn',ll disco\ ors the food and c:lrlics it: the V M I cledricai actixitx seems nlorc hlcgular 'and lastcr and the alnplitudc is smaller. Nel, icc in the occipital deri\ ation rhythmic slov, x,,a yes x~hose amplitudc and l'rcquclacy are identical to lhc V M T Fhvllma. I:ig. 2 shows dill>re111 cases ol'a\\ akcning from slmx \~ave slccp (SWS). 111 .1. natur~ll ttwakuni,lg : the \ ; M ] rl-kkth111svary \\il h the different pCl iOdS of \~aking,, In a first period oF 5 6 sou lhc ral doe'~ not illO\C the tracing sho\~.,> rapid >mall anlpliludc irreeular a c t i \ i l ) ; in ;.i second period oI" 25 27 soc lhc ani111ul Stletches: lhc X~a\rCSarc slo~er and their alnplitude hugcr; finally, in a lhird period, the animal stands up and \talks arOtllld exploring; ;.it the same lhnc that largo a c i i \ i b ;.ippcai'>, in lllc ;.iclogranL 14SA appeal,4 in Ihc V M I . In B the same scqucncu'.s apr~c,ai bul faster, d uring an :.lV~;.iken ing pro\ okcd b\ a knock on the \xiildo\~ oF the cclbin. The I';A{ d o e s 11Oi raise its head until 3 or 4 scc after lhc disappearance o1" file slow sloop \\gives: ITS.,\ is r0cordcct fronl this nlOlllenl on. In tile cor/cx and hypothalamus, small anlplit ude rupid irregular activity apl)cars. In ('awakellhlg is provoked by electrical stilmlhltion oF\he ipsihitcral Lt| (100 c sec sine \',a\es at 30 HA l'or 4 see). Tile stinlulus c~.itlSCS
disappearance o1" the slo\~ sleep Xxa\rcs flonl lhc cortex and V M T : lhe anilnal does nol illC)vc. Then. xvhcn tile anhnal has oriented ilscll" and
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Fig. 2 shox~s that during SWS lhe V M T rhythms arc similar to the cortical and ILvpothalamic rhythms and appear as large slo~ irregular waves. Recordings arc performed in the VMT. in ncighbouring structures and in lhc lclcnccplmlic limbic structures during P%. "]hc clclograph records the muscular twitching tinct the smnll lno~,.omcnts of lhc limbs, back. head ;.ind ~ibrissac which appear phasicully during PS. a. Recording l)'om Hw I ' M T i Fig..7) Dr mean.~
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012 hil)ohu" elecll'ode,x .vimaled oil eidwr ,,idc +!1 []H.' iIllWY/?CChIII¢'IIi{.H" tlIIUIWII.'~. It can be seen thcli the passage from SWS to PS coincides \~ ith the appearance o f RSA in this region. This rhythna is not regular during PS: bursts appear in ~ hich the x~'avcs arc larger, slo\~er and more regular: it seems that these bursts happen at the same time that m o x c m e n t is recorded by lhc aclograph.
142
M. LE MOAL AND B. CARI)O
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B_ LIFTING OF HEAD C ORIENTATION REARING Fig. 2. EEG recording from VMT during awakening in three different animals (A, B, C). A: Spontaneous awakening• B: Awakening provoked by a tap. C: Awakening provoked bystimulation of lateral hyl~othalamus (stim). Calibration: 100 l~V and 2 sec.
b. Recording from the VMT, from the L H andJrom various limbic structures. Theta rhythm is not recorded in the L H during PS (Fig. 4). A slow rhythm which seems very similar to RSA is recorded from the occipital cortex. It can be seen that the mesencephalic and hippocampal
rhythms are at 6-8 c/sec. The tracings show the same variations of amplitude and frequency. In Fig. 5, in which the septum, the anterior thalamus, the V M T and the cortex are recorded, theta rhythms which seem to undergo the same modulations are observed in all the derivations. The
143
THETA RHYTHM IN ]'HE VENTRAL TEGMENTUM
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© Fig. 3. EEG recordings from deepoccipital cortex and neighbouring dorsal hippocampus (hpc) and VMT during sleep: the two bipolar electrodes are situated on either side of the interpeduncular nucleus (IP). A: Slow sleep (SWS). B-C: Paradoxical sleep (PS). Notice variations of actogram (Act) during PS. Calibration: 100 #V and 2 sec. Scheme on first recording, left: position of the electrodes in the deep occipital cortex; bottom scheme: frontal section (from K6nig and K lippel 1963) with position of the tip of the two bipolar electrodes in VMT (IP: nucleus interpeduncularis; LM: lemniscus medians. Black circles: tip of the electrode). VMT-r and VMT-I: right and left electrode according to the scheme. OCC-(hpc)CX. ~
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® Fig. 4. EEG recordings from VMT, from deep occipital cortex and neighbouring dorsal hippocampus (hcp) and from lateral hypothalamus (hypo) during sleep. A: SWS. B: PS. Calibration: 100 #V and 1 sec. Top scheme: position of electrodes in the deep occipital cortex; second scheme: VMT area on frontal section (IP: nucleus interpeduncularis; LM: lemniscus me~lialis; NR: nucleus ruber): bottom scheme: hypothalamus (FMP: fasciculus medialis prosencephalii; HM: medial hypothalamus; Fx: fornix). Black circles: tip of the electrodes. (Frontal section: according to K6nig and Klippel 1963.)
cortical tracings shows mixed fast and slow waves, the hippocampal rhythms being sometimes picked up. It can be seen that the RSA follows the same modulations in the first three structures.
3. Influence of septal lesions on V M T rhythm The pre- and post-lesional records were corn-
pared for the 6 rats carrying a monopolar electrode in the MS. Recording was started 15 days after the septal lesions; a record from one of the 6 rats is shown in Fig. 6. The histological control of the septal lesion is schematized in a diagram representing the septum. The lesion is cenfred in the medial septum ;
144
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tig. 5. E[{(I recordings fronl corle'x. ['ronl \ M I and l'ronl limhic slrtl¢ltlrcs: medial septtilll (SM) rind Liillc.'ro-\eiltrLl] thalcinlus ( I \ V ) during sleep in one animal, t : S\\"%. B: PS. ('alibrcition: 100HV and 2 scc. rop',chcmc: position o f electrodes m deep occipital and fronlal cortex aboxc the dor,,41 hippocampu,, (hpc); second scheme: thalmnu~, on I'tontcil section ( \ l : nucleus ,,'entrails tlmlcuni: V \ : imclcus \enlralis thalmyli pciis anlcrior: M I : IraCttl~, mamilh+Ihalanlicus); third schclnc: re+ca tognlcnti '~cntralis on l'rontcll ,,cction ( + \ \ 1 ) : t\+tulh :,chcmc: scptum on frontal ,,ection (SI.: nucic,'u,4 httcrcilis scpti: SM: nucleus mcdialis scpti). Black cir¢lc~,; tip oI" cloth'odes. (l'ronta] soulhms: according Io KSnig and Klippcl 1963.)
he\ ertheless, tile necrotic zone reaches tile h/teral septunl. The records are from SWS arid fi-om PS. Comparing tile pre- and post-lesional tracings (Fig. 6), it can be seen that the RSA has practically disappeared in tile VMT region and in the limbic slructure (TAV) Lind the slow waves are replaced by I~lst rhythms (20 30 c,'sec). Tile effects of the septal lesion are made obvious by high-speed recording (Fig. 6. (" and C'). Besides the modification of frequency, the post-lesional tracings undergo an amplitude reduction of 50 70",,. The rhythms of SWS are not modified nor are the cortical records during PS changed in amplitude and frequency.
I. Et:'G characlcri,sti,w,v in llw 1"317
t{{-](] recording l'rom the VMT region by inacroelecirodes gave the follo~ving data" (a) 1)uring some behaviour and dtiring PS, rhylhnlic s l o ~ a c t i v i t y ( R S A ) a t 6 8c sec appears. (b) This VMT rhythm seems to have tile same characteristics as the theta rhythnl recorded during the waking period alld during PS in ihe hippocampus a n d a s s o c i a t e d s t r u c t t l r e s . (c) The Icsions of the scptum have similar effects in lhe limbic structures and in tile VMT. During PS, tile RSA is replaced in ihc lnesenccphalon by l'asl \X,Ll\'es of small amplitude. (d)Other hippocampal activities (GI'LlStyaI~I Ct u/. 1959: Whishax~ ',lnd V L m d e r wolf 1973) are also l'ound in tile V M T : small amplitude irregulLu activity (SIA) silnuhaneous ~ith cortical desynchronization durmg automatic behaviour and tile nori-orienlcd waking state, or RSA overcharged with l'asl v, aves, large irregular slo\x activity during SWS and spindles at tile beginning of PS. RSA seems to be concentrated in tile VMT. file existence of RSA in other nlesencephalic structures, however, has been pointed out by some authors. Iil the reticular l'ormation these rhythms have been recorded in the ia[. ;.ind n]ole rarely in the cat, during the attentive ~\aking slale alld during PS (Anokhin 1960: Bergnlali <'I al. 1963 : Brooksand Bizzi 1963 ;,louver 1965 :Stunlpf 1965). Parineggiani and ZLInOCCO (1961)recorded rhythnlic slow wa\es in ihc vicinity of tile substantiLi nigra (neLu tile V M T ) during PS. /\ synchronous rhythm has occasionally been nolicod in tile ventral l . e g m e n t u n l ( ( ] o t t e s n l a n i 1 1967 ). Thus il appears thai. apLU't t'ronl a fc;~, relicular points, tile theta rhythn~ is essentially recorded tit tile mesencephalic level in tile ventral teglnental a re,:.l. 2. Padm'avs h w o h c d in the in'Ol~mSalion
145
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Fig. 6. Influence of seplal lesions on VMT and thalamic rhythms during sleep in one animal. A B: SWS and PS be(ore septal lesion. A' B': After lesion. C C': PS before and after lesion on high speed recordings. Histological control shows that the lesion is centred in medial septum. Calibration : A B, A' -B': 100 FtV and 2 sec: C C': 100 I~V and I sec. Top scheme : position of the electrode in occipito-frontal cortex: second scheme: antero-ventral thalamus and frontal section (AM: nucleus anteromedialis thalami: AV: nucleus antero-ventralis thalami; VA: nucleus ventralis thalami pars anterior): third scheme: V MT area (NR: nucleus ruber; IP: nucleus interpeduncularisL Scheme in section B': diagram of lesion in nucleus medialis septi (LS: nucleus lateralis septi, ret;er to Fig. 5).
searches have shown the role of the septum and of the diagonal band of Broca in the genesis and transmission of hippocampal theta rhythm (Green and Arduini 1954: Petsche and Stumpf 1960: Petsche et al. 1962: Stumpf 1965: Gray 1971). Furthermore, as the records reveal the similarity of the limbic and mesencephalic rhythms, and as the septal lesions suppress in the same way the RSA recorded at these two levels, it is possible to assume that this RSA comes from a single septo-hippocampal pacemaker. Among the numerous bundles which pass through the
VMT, the descending fibres of the medial forebrain bundle (MFB) do not appear to be involved in the propagation of the theta rhythm, since this rhythm has not been recorded in the lateral hypothalamus. On the other hand, it would seem reasonable to consider the possible role of the post-commissural fornix, numerous fibres of which terminate in the thalamus and in the "limbic midbrain area", particularly in the VMT (Valenstein and Nauta 1959; Nauta and Haymaker 1969; Livingston and Escobar 1971).
146 3. R S A a m l h e h a t ' i o u r
This electrophysiological research was motivated by certain behavioural data. We have shown that alesion o f the V M T c a u s e s a s y n d r o m e revealing a deficiency in behavioural control and in the processes of selective attention (Le Moal et el. 1969, 1970). The "'VMT s y n d r o m e " displays the general characteristics of limbic deficits. This c o m p a r i s o n is strengthened by the discovery o f theta-type rhythms in this structure. The functional significance o f these rhythms varies according to the authors because the correlated behaviours considered have been differently defined. It seems that the RSA of the V M T changes according to the nature o f the m o v e m e n t and to its way o f execution and occurs when behavioural control and attentive vigilance are pred o m i n a n t (Douglas 1967; Kimble 1968: Bennet and Gottfried 1970: K l e m m 1972). However, all these data are still controversial and it is therefore difficult to relate the effects o f V M T lesions to the significance o f the RSA. In any case the discovery o f theta r h y t h m in the V M T adds electrophysiological data to the anatomical and behavioural information which tends to relate this structure to the limbic systems.
~a. LE MOAL AND B. ('ARI)O RESUME ACTIVITES LENTES RYTHMIQUES RECUEILLIES AU NIVEAU I)U TEGMENTUM MESEN('EPHALIQUEVENTRAL CttEZ LE RAT 1. Des ondes lentes rythmiques de type theta ont ate enregistrdes chez le rat dans la rdgion tegmento-mdsencaphalique ventrale sus-interpddonculaire, un des elements de la " / i m h i c m i d b r a i n a r e a " . Ces ondes sont enregistrdes durant certains 6veils attentifs, durant l'execution de m o u v e m e n t s volontaires et durant le sommeil paradoxal. 2. Ces ondes lentes rythmiques T M V semblent de meme nature que le rythme theta enregistre darts les structures limbiques. La lesi(m du septurn supprime les ondes lentes rythmiques au niveau mesencdphalique c o m m e au niveau telencdphalique. 3. Si les ondes lentes rythmiques mesencephaliques ont un gendrateur unique, les voies qui transmettent le rythme theta jusqu'fi la region T M V sont mal connues. Toutefois ilest raisonnable d ' a d m e t t r e que des fibres du fornix postcommissural sont impliquees dans cette transmission.
SUMMARY 1. Slow rhythmic theta-type waves were recorded in the sub-interpeduncular ventral mesencephalic tegmentum (VMT) in the rat. This region is one o f the parts o f the "limbic midbrain area". These waves are recorded during certain attentive waking states, during the executmn ot" voluntary m o v e m e n t s and during paradoxical sleep. 2. These rhythmic V M T waves seem to be o f the same nature as the theta r h y t h m recorded in the limbic structures. A lesion o f the septum suppresses the slow rhythmic waves at the mesencephalic level as well as at the telencephalic level. 3. A l t h o u g h we have n o w shown that the mesencephalic and telencephalic slow rhythmic waves have the same pacemaker, the pathways which transmit the theta r h y t h m to the V M T are not well known. However, it is reasonable to suppose that the fibres o f the post-commissural fornix are involved in this transmission.
We would like to thank Mrs A. M. Perret and Mrs M. Mallet for their technical assistance.
REFERENCES ANCHEL, H. and LINDSLEY,D. B. Differentiation of two reticulo-hypothalamic systems regulating hippocampal activity. Electroenceph. c/in. Neurophysiol., 1972, 32: 209 226. ANOKHIN.P. On the specific action of the reticular formation on the cerebral cortex. Electroenceph. olin. Neurophysiol., 1960, 13:257 270. BENNETT,T. L. and GOTTFRmD,J. Hippocampal theta activity and response inhibition. Electroeneeph. olin. Neurophysiol.. 1970, 29 : 196-200. BERGMAN,F.. COSTIN,A. and GUTMAN,J. A low threshold convulsive area in the rabbit's mesencephalon. Electroenceph, olin. Neurophysiol., 1963, 15: 683-690. BROOKS, D. C. and BIzzl, E. Brain stem electrical activity during deep sleep. Arch. ital. Biol., 1963, 101:648 665. DOUGLAS,R. J. The hippocampus and behavior. Psychol. Bull., 1967, 67: 416-442. OOTTESMANN. C. Recherche sur la psychophysiologie du sommeil chez le rat. Presses du Palais Royal, Paris, 1967, 156 p.
" I I t F F A RHYTHM IN I-HE VENTRAL TEGMENTUM
(iRASI 5 AN, l£.. IASSAI,;.,K.. MAI)ARASZ. 1 and l)o?
147 and fiber connections. In W. HA'~MAK|R ('I tl/. (l'tts.). The hvpothalamtcs, Thomas. Springfield. I11.. 1969: 136 209. NAt 1:,. W. J. H. and Kt'vpt RS, H. (;. J. M. Sore,: ascending pathv, ays in the brain stem reticular formation. In t lI l ] JASPER Ct ~/]. (Eds.). R c l i c u k t r /i)17~talioH O/ lh¢ ]wUl/h Liule, Brown, Boston, Mass., 1958:3 30. P*RME(;(;IANI. P. L. On the functional significance of the hippocampal ~I-rhythm. ha W. R. ADtc~ and T. "I'oKIZANI (Eds.). Prow. Brain Rc.s.. 1967. 27:413 441. PARMI¢;(ilANI. P. L. and ZANO('UO. (}. Cortical and sub cortical recordings during low voltage lkist E t G phase in sleep in cat. ttc/r, ph.vsiol, p/utr/mwo/. Act,. 1961, 10: 97 99. F'vls(ln. t1. and Sqt:Mpl. C. Topographic and toposcopic study of the origin and spread of the regular synchronized arousal pattern in the rabbit. Electroem'cplI. olin :\curold~wio/., 1960. 12:589 600. Pl.71S('ln!. tt.. STUMPI. C. and GO(;OI.AK. (]. The significance of the rabbit's septum as a relay stalion between the midbrain and hippocalnpus. 1. The control of hippocampal arousal activity by the septum cells. Eh'ctr,cnceph, c/in. Ncuropky,sioL. 1962, 14:202 221. ROUI TI!NI'UiR(;.a . [ t i p p o c a l n p a l correlates OI consnnqnlalory and observed behavior. PkrvioL Behar.. 1968, 3:533 535. STUMI'I. C. The fast component in the electrical activity of the rabbit's hippocampus. Elcclrocnc'7d~. ¢/in. ,Vcm',ldU'viol.. 1965, l?.': 477 486. gALl NSTI!IN, 1~. S. and NM:T~,, W..I. H A comparison of lhc distribution of the fornix system in the rat. guinea pig. cat and monkey. J. comp. neuro/.. 1959, /13:337 363. WmSHAW. I. Q. and VAXDtiRWOLI.C. 11. ]lippocampal I . t ( i and behavior: changes in amplitude and frequent) of RSA (theta rhythm) associated with spontaneous and learned movement patterns m rats and cats. Bck,~. 13:,/.. 1973, S: 461 484. YAblA(ilr('lll. Y.. VcJsIIII. N.. MIYAMOI(L K. and [IOIGAW\. N. 4 S[lldl' Otl Ill!' illl'(I.Sil'{' hJp/)oCtlDl/~H/ [h{,[tl i1¢11c~ 1o l/w corW.v. In W. R. AI)iv and T. "I'~I/A~,~ (1 ds.I. Prow. Bra#1 Res.. 1967, 27:281 292.
139
R H Y T H M I C SLOW WAVE ACTIVITY R E C O R D E D IN THE V E N T R A L M E S E N C E P H A L I C T E G M E N T U M IN THE RAT M. LE MOAL AND B. CARD() Lahoratoire de Psvchophysiologie, University; de Bordeaux l. Avenue des Facultds, 33405 Talence (France)
(Accepted I\~r publication: August 18, 1974)
In recent years anatomical studies (Nauta 1958; Nauta and Kuypers 1958) have made it possible to link the limbic system with an important mesencephalic region including the ventral mesencephalic tegmentum (VMT), the nuclei of the anterior raphe, the nuclei of Gudden and the ventral part of the central grey matter. The functions of this "'limbic midbrain area" (Nauta 1958) are still relatively unknown. Some recent data, however, attribute to the VMT characteristics which are peculiar to the limbic system (Karli 1968); thus, after VMT lesions, hyperactivity, difficulty in inhibiting previously acquired behaviour and perseveration are observed (Le Moal et al. 1969, 1970). Furthema0re, no electrophysiological study of these structures has yet been made in the freely moving animal with chronically implanted electrodes. In order to improve our knowledge of these mesencephalic areas, we have carried out electroencephalographic recordings (EEG) from the VMT by means of large electrodes. These records were taken in the course of various behavioural sequences and during paradoxical sleep (PS).
METHOD AND MATERIAL
Animals and surgery
Thirty-four male rats of the Sprague-Dawley strain were used. The implantation of electrodes was done under deep Pentothal anaesthesia (80 mg/kg i.p.). After the operation the animals were housed in individual cages at constant temperature (22°C). Stereotaxic coordinates anddistribution of animals
Besides the VMT, cortical or subcortical electrodes were implanted in 2 or 3 of the following structures: medial septum (MS), dorsal hippocampus (Hpc), antero-ventral thalamus (TAV) and lateral hypothalamus (LH). Cortical electrodes made of chloride-plated silver wire 0.2 mm in diameter, insulated except for the end 0.3 ram, were placed in the bi-occipital (bi-occ) or occipitofrontal (occ-fr) cortex. In certain rats electrodes were inserted into the cortex in order to record by diffusion the activities of the dorsal hippocampus (Jouvet 1967 ; Parmeggiani 1967 ; Yamagushi et al. 1967). The bipolar subcortical elec-
]'ABLE I Stercotaxiccoordinates of implantations (ram) Structure
Antero-posterior*
Lateral*
Vertical**
Medial septum Antero-ventral thalamus Lateral hypothalamus Dorsal hippocampus Ventral tegmentum
A 2.0 P 0.6 P 0.6 P 2.4 P 4.3
0.0 1.8 1.7 2.7 0.5
6.2 6.5 8.5 3.0 8.6
* From bregma. ** Belowthe skull.
140
t iodcs ~\ crc nlack: of t\~istcd pallacliunl-tungstcn wirc~, 0.15 111111in dianlcler, insulated cxccpl for 111cend 0.3 n1111.Tho coordinates ol'inll-~lanlalion arc' lisicd in Table I. 7ix ral s iccoi~ cd a 111Ollopolar il>Uklted slainlcss-slccl electrode, dkuneior 0 2 ii111/ \~ith ~l 0.4 111111point, ill the MS. By 111CLIllSol'lhis clcctrodc. coagulation ol'lhis strucl ure \vould later be made. All the elcc/iodcs were soldered to a inicrominint tll't_" 5-pin tI'allSisloF socket and sterilized [)c.'t'OlC lhc opcrcltion. Thc \~hole impkll~t \~;is l]xcd to lhc skull \~ ith anchoring scIo\~ s and acrylic rosin. t{\01\' ral had an electrode in II~e V M T . 13 r:.ils had an clccilodc ill the L t l , 5 had o11c in the ltpc. 5 in ihe MS and tho TA\.;. 5 in the [ , , \ V and Iho t lpc. The f, rats having a coagulalion electrode in the M S also had recoMing electrodes in tile mcsenccphalon and the lhalalmis. The lesions oF tile MS were nlade rind,21 anaesthesia b,, ;i radiol'requcncy (500 kc sec CtlITC!]I t'd" 50 /~,.'\ xxhich klstcd I\)r .'2_sec.
Rccom/illg.v All file recoldillgs \~ele made 111a soundprool" cabin, ol'x~ hich c)ne side was transpalcnt It) nllo\~ obscr\'alioll of the aninlal. The 11oo1 o1" the recoMing ccitt consisted in a hydraulic lnattress which /iansn]itlcd c\or\.' nlO\'enlcnt of 111c ral as a pressure \ a r i a l i o n to a lransduccr and I'roni there to one of the a11~plil]ers of the electroencephalograph. The serisii ivity was increascd \~ hen lhc ailimal ~as asleep, in order to record its smallest inovenlents, especially during F'S. The clectrodcs \\erc electrically connected to the rccordhlg a p p a r a t u s , b y a nlobilc mercury con-nector. The records were made with a differential clccl roon copha logra p h. Iirst. the anilnals x~ere recorded during the I\~llm\ing acti~hies: eating, snifl]ng, exploring. cleaning and licking, a\takening caused bv the cxpcrilnenter or by' central electrical stimulalion. Tllcn. various recordings were perfornlcd during bolh sl;./los of slcep. Finally the EEO activit'ios v, erc cOillparcd befoFe and after sepial coagulation. AI the end of ihc experiment the aninlals \x ere anaesthetized \~ith Pentothal and killed by' transcardiac per fusion o f a 10 o <,formol solution. Then the brain \x as renloved and the histological cont l'OiSwere nladc (N issl-stain ). The electrode phice-
xI. i i M ( i A I
\HI> B ('ARI)()
IllClIIs arc indicated in the di',tgrilms placed at lllc beginlling of tr:.lcing>, these cli:.lgr',in> ;.11-c_' lakcn l'ronl KGnig ;.llltt Klippcl (1%31 (scc Results). R I M I IV;
1. I@corditlg /)~,l~ rlw J.AI7 dminft r~,lot~ ~w/iril h c mtchlgs \\crc c]lalacieri/cd b\ lhc appeara l l o t LIIIdcI CC1!aill bcJ1~1\ iOLll"al CiICHI11S|~IIICCS c)[
1hvthmic sire\ acfi,~il\ (RSA)',1i fl X c scc ofthe lhcb:l type. l'ig. I ~ho\\~ ~o111c cXaml~Ics, lu i the rat is iImoduccd into lhc cage and cxph)rcs: at the same lime P,SA appears in the \ r M T x~h i l t
the cortex and the h>pothahmlu,~ ~,ho\x small amplitude irregular activi/\ (SIAL t11 B l b o d is introduced inlo the cage of an animal depJivcd ol'[k~od [br 24 h: at first Ihc l'~|! looks 1i~1lhc l'ood \x hich it snilT~ ;,li: RSA appccu>, hi the VMF, the \xa\cs 'arc large, a[ 7 c see: then the anhn',ll disco\ ors the food and c:lrlics it: the V M I cledricai actixitx seems nlorc hlcgular 'and lastcr and the alnplitudc is smaller. Nel, icc in the occipital deri\ ation rhythmic slov, x,,a yes x~hose amplitudc and l'rcquclacy are identical to lhc V M T Fhvllma. I:ig. 2 shows dill>re111 cases ol'a\\ akcning from slmx \~ave slccp (SWS). 111 .1. natur~ll ttwakuni,lg : the \ ; M ] rl-kkth111svary \\il h the different pCl iOdS of \~aking,, In a first period oF 5 6 sou lhc ral doe'~ not illO\C the tracing sho\~.,> rapid >mall anlpliludc irreeular a c t i \ i l ) ; in ;.i second period oI" 25 27 soc lhc ani111ul Stletches: lhc X~a\rCSarc slo~er and their alnplitude hugcr; finally, in a lhird period, the animal stands up and \talks arOtllld exploring; ;.it the same lhnc that largo a c i i \ i b ;.ippcai'>, in lllc ;.iclogranL 14SA appeal,4 in Ihc V M I . In B the same scqucncu'.s apr~c,ai bul faster, d uring an :.lV~;.iken ing pro\ okcd b\ a knock on the \xiildo\~ oF the cclbin. The I';A{ d o e s 11Oi raise its head until 3 or 4 scc after lhc disappearance o1" file slow sloop \\gives: ITS.,\ is r0cordcct fronl this nlOlllenl on. In tile cor/cx and hypothalamus, small anlplit ude rupid irregular activity apl)cars. In ('awakellhlg is provoked by electrical stilmlhltion oF\he ipsihitcral Lt| (100 c sec sine \',a\es at 30 HA l'or 4 see). Tile stinlulus c~.itlSCS
disappearance o1" the slo\~ sleep Xxa\rcs flonl lhc cortex and V M T : lhe anilnal does nol illC)vc. Then. xvhcn tile anhnal has oriented ilscll" and
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141
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Fig. 2 shox~s that during SWS lhe V M T rhythms arc similar to the cortical and ILvpothalamic rhythms and appear as large slo~ irregular waves. Recordings arc performed in the VMT. in ncighbouring structures and in lhc lclcnccplmlic limbic structures during P%. "]hc clclograph records the muscular twitching tinct the smnll lno~,.omcnts of lhc limbs, back. head ;.ind ~ibrissac which appear phasicully during PS. a. Recording l)'om Hw I ' M T i Fig..7) Dr mean.~
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012 hil)ohu" elecll'ode,x .vimaled oil eidwr ,,idc +!1 []H.' iIllWY/?CChIII¢'IIi{.H" tlIIUIWII.'~. It can be seen thcli the passage from SWS to PS coincides \~ ith the appearance o f RSA in this region. This rhythna is not regular during PS: bursts appear in ~ hich the x~'avcs arc larger, slo\~er and more regular: it seems that these bursts happen at the same time that m o x c m e n t is recorded by lhc aclograph.
142
M. LE MOAL AND B. CARI)O
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B_ LIFTING OF HEAD C ORIENTATION REARING Fig. 2. EEG recording from VMT during awakening in three different animals (A, B, C). A: Spontaneous awakening• B: Awakening provoked by a tap. C: Awakening provoked bystimulation of lateral hyl~othalamus (stim). Calibration: 100 l~V and 2 sec.
b. Recording from the VMT, from the L H andJrom various limbic structures. Theta rhythm is not recorded in the L H during PS (Fig. 4). A slow rhythm which seems very similar to RSA is recorded from the occipital cortex. It can be seen that the mesencephalic and hippocampal
rhythms are at 6-8 c/sec. The tracings show the same variations of amplitude and frequency. In Fig. 5, in which the septum, the anterior thalamus, the V M T and the cortex are recorded, theta rhythms which seem to undergo the same modulations are observed in all the derivations. The
143
THETA RHYTHM IN ]'HE VENTRAL TEGMENTUM
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© Fig. 3. EEG recordings from deepoccipital cortex and neighbouring dorsal hippocampus (hpc) and VMT during sleep: the two bipolar electrodes are situated on either side of the interpeduncular nucleus (IP). A: Slow sleep (SWS). B-C: Paradoxical sleep (PS). Notice variations of actogram (Act) during PS. Calibration: 100 #V and 2 sec. Scheme on first recording, left: position of the electrodes in the deep occipital cortex; bottom scheme: frontal section (from K6nig and K lippel 1963) with position of the tip of the two bipolar electrodes in VMT (IP: nucleus interpeduncularis; LM: lemniscus medians. Black circles: tip of the electrode). VMT-r and VMT-I: right and left electrode according to the scheme. OCC-(hpc)CX. ~
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® Fig. 4. EEG recordings from VMT, from deep occipital cortex and neighbouring dorsal hippocampus (hcp) and from lateral hypothalamus (hypo) during sleep. A: SWS. B: PS. Calibration: 100 #V and 1 sec. Top scheme: position of electrodes in the deep occipital cortex; second scheme: VMT area on frontal section (IP: nucleus interpeduncularis; LM: lemniscus me~lialis; NR: nucleus ruber): bottom scheme: hypothalamus (FMP: fasciculus medialis prosencephalii; HM: medial hypothalamus; Fx: fornix). Black circles: tip of the electrodes. (Frontal section: according to K6nig and Klippel 1963.)
cortical tracings shows mixed fast and slow waves, the hippocampal rhythms being sometimes picked up. It can be seen that the RSA follows the same modulations in the first three structures.
3. Influence of septal lesions on V M T rhythm The pre- and post-lesional records were corn-
pared for the 6 rats carrying a monopolar electrode in the MS. Recording was started 15 days after the septal lesions; a record from one of the 6 rats is shown in Fig. 6. The histological control of the septal lesion is schematized in a diagram representing the septum. The lesion is cenfred in the medial septum ;
144
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tig. 5. E[{(I recordings fronl corle'x. ['ronl \ M I and l'ronl limhic slrtl¢ltlrcs: medial septtilll (SM) rind Liillc.'ro-\eiltrLl] thalcinlus ( I \ V ) during sleep in one animal, t : S\\"%. B: PS. ('alibrcition: 100HV and 2 scc. rop',chcmc: position o f electrodes m deep occipital and fronlal cortex aboxc the dor,,41 hippocampu,, (hpc); second scheme: thalmnu~, on I'tontcil section ( \ l : nucleus ,,'entrails tlmlcuni: V \ : imclcus \enlralis thalmyli pciis anlcrior: M I : IraCttl~, mamilh+Ihalanlicus); third schclnc: re+ca tognlcnti '~cntralis on l'rontcll ,,cction ( + \ \ 1 ) : t\+tulh :,chcmc: scptum on frontal ,,ection (SI.: nucic,'u,4 httcrcilis scpti: SM: nucleus mcdialis scpti). Black cir¢lc~,; tip oI" cloth'odes. (l'ronta] soulhms: according Io KSnig and Klippcl 1963.)
he\ ertheless, tile necrotic zone reaches tile h/teral septunl. The records are from SWS arid fi-om PS. Comparing tile pre- and post-lesional tracings (Fig. 6), it can be seen that the RSA has practically disappeared in tile VMT region and in the limbic slructure (TAV) Lind the slow waves are replaced by I~lst rhythms (20 30 c,'sec). Tile effects of the septal lesion are made obvious by high-speed recording (Fig. 6. (" and C'). Besides the modification of frequency, the post-lesional tracings undergo an amplitude reduction of 50 70",,. The rhythms of SWS are not modified nor are the cortical records during PS changed in amplitude and frequency.
I. Et:'G characlcri,sti,w,v in llw 1"317
t{{-](] recording l'rom the VMT region by inacroelecirodes gave the follo~ving data" (a) 1)uring some behaviour and dtiring PS, rhylhnlic s l o ~ a c t i v i t y ( R S A ) a t 6 8c sec appears. (b) This VMT rhythm seems to have tile same characteristics as the theta rhythnl recorded during the waking period alld during PS in ihe hippocampus a n d a s s o c i a t e d s t r u c t t l r e s . (c) The Icsions of the scptum have similar effects in lhe limbic structures and in tile VMT. During PS, tile RSA is replaced in ihc lnesenccphalon by l'asl \X,Ll\'es of small amplitude. (d)Other hippocampal activities (GI'LlStyaI~I Ct u/. 1959: Whishax~ ',lnd V L m d e r wolf 1973) are also l'ound in tile V M T : small amplitude irregulLu activity (SIA) silnuhaneous ~ith cortical desynchronization durmg automatic behaviour and tile nori-orienlcd waking state, or RSA overcharged with l'asl v, aves, large irregular slo\x activity during SWS and spindles at tile beginning of PS. RSA seems to be concentrated in tile VMT. file existence of RSA in other nlesencephalic structures, however, has been pointed out by some authors. Iil the reticular l'ormation these rhythms have been recorded in the ia[. ;.ind n]ole rarely in the cat, during the attentive ~\aking slale alld during PS (Anokhin 1960: Bergnlali <'I al. 1963 : Brooksand Bizzi 1963 ;,louver 1965 :Stunlpf 1965). Parineggiani and ZLInOCCO (1961)recorded rhythnlic slow wa\es in ihc vicinity of tile substantiLi nigra (neLu tile V M T ) during PS. /\ synchronous rhythm has occasionally been nolicod in tile ventral l . e g m e n t u n l ( ( ] o t t e s n l a n i 1 1967 ). Thus il appears thai. apLU't t'ronl a fc;~, relicular points, tile theta rhythn~ is essentially recorded tit tile mesencephalic level in tile ventral teglnental a re,:.l. 2. Padm'avs h w o h c d in the in'Ol~mSalion
145
I-ttliTA RIIYTtlM IN THE VENTRAI~ TEGMENTI M occ. FR. Cx.
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Fig. 6. Influence of seplal lesions on VMT and thalamic rhythms during sleep in one animal. A B: SWS and PS be(ore septal lesion. A' B': After lesion. C C': PS before and after lesion on high speed recordings. Histological control shows that the lesion is centred in medial septum. Calibration : A B, A' -B': 100 FtV and 2 sec: C C': 100 I~V and I sec. Top scheme : position of the electrode in occipito-frontal cortex: second scheme: antero-ventral thalamus and frontal section (AM: nucleus anteromedialis thalami: AV: nucleus antero-ventralis thalami; VA: nucleus ventralis thalami pars anterior): third scheme: V MT area (NR: nucleus ruber; IP: nucleus interpeduncularisL Scheme in section B': diagram of lesion in nucleus medialis septi (LS: nucleus lateralis septi, ret;er to Fig. 5).
searches have shown the role of the septum and of the diagonal band of Broca in the genesis and transmission of hippocampal theta rhythm (Green and Arduini 1954: Petsche and Stumpf 1960: Petsche et al. 1962: Stumpf 1965: Gray 1971). Furthermore, as the records reveal the similarity of the limbic and mesencephalic rhythms, and as the septal lesions suppress in the same way the RSA recorded at these two levels, it is possible to assume that this RSA comes from a single septo-hippocampal pacemaker. Among the numerous bundles which pass through the
VMT, the descending fibres of the medial forebrain bundle (MFB) do not appear to be involved in the propagation of the theta rhythm, since this rhythm has not been recorded in the lateral hypothalamus. On the other hand, it would seem reasonable to consider the possible role of the post-commissural fornix, numerous fibres of which terminate in the thalamus and in the "limbic midbrain area", particularly in the VMT (Valenstein and Nauta 1959; Nauta and Haymaker 1969; Livingston and Escobar 1971).
146 3. R S A a m l h e h a t ' i o u r
This electrophysiological research was motivated by certain behavioural data. We have shown that alesion o f the V M T c a u s e s a s y n d r o m e revealing a deficiency in behavioural control and in the processes of selective attention (Le Moal et el. 1969, 1970). The "'VMT s y n d r o m e " displays the general characteristics of limbic deficits. This c o m p a r i s o n is strengthened by the discovery o f theta-type rhythms in this structure. The functional significance o f these rhythms varies according to the authors because the correlated behaviours considered have been differently defined. It seems that the RSA of the V M T changes according to the nature o f the m o v e m e n t and to its way o f execution and occurs when behavioural control and attentive vigilance are pred o m i n a n t (Douglas 1967; Kimble 1968: Bennet and Gottfried 1970: K l e m m 1972). However, all these data are still controversial and it is therefore difficult to relate the effects o f V M T lesions to the significance o f the RSA. In any case the discovery o f theta r h y t h m in the V M T adds electrophysiological data to the anatomical and behavioural information which tends to relate this structure to the limbic systems.
~a. LE MOAL AND B. ('ARI)O RESUME ACTIVITES LENTES RYTHMIQUES RECUEILLIES AU NIVEAU I)U TEGMENTUM MESEN('EPHALIQUEVENTRAL CttEZ LE RAT 1. Des ondes lentes rythmiques de type theta ont ate enregistrdes chez le rat dans la rdgion tegmento-mdsencaphalique ventrale sus-interpddonculaire, un des elements de la " / i m h i c m i d b r a i n a r e a " . Ces ondes sont enregistrdes durant certains 6veils attentifs, durant l'execution de m o u v e m e n t s volontaires et durant le sommeil paradoxal. 2. Ces ondes lentes rythmiques T M V semblent de meme nature que le rythme theta enregistre darts les structures limbiques. La lesi(m du septurn supprime les ondes lentes rythmiques au niveau mesencdphalique c o m m e au niveau telencdphalique. 3. Si les ondes lentes rythmiques mesencephaliques ont un gendrateur unique, les voies qui transmettent le rythme theta jusqu'fi la region T M V sont mal connues. Toutefois ilest raisonnable d ' a d m e t t r e que des fibres du fornix postcommissural sont impliquees dans cette transmission.
SUMMARY 1. Slow rhythmic theta-type waves were recorded in the sub-interpeduncular ventral mesencephalic tegmentum (VMT) in the rat. This region is one o f the parts o f the "limbic midbrain area". These waves are recorded during certain attentive waking states, during the executmn ot" voluntary m o v e m e n t s and during paradoxical sleep. 2. These rhythmic V M T waves seem to be o f the same nature as the theta r h y t h m recorded in the limbic structures. A lesion o f the septum suppresses the slow rhythmic waves at the mesencephalic level as well as at the telencephalic level. 3. A l t h o u g h we have n o w shown that the mesencephalic and telencephalic slow rhythmic waves have the same pacemaker, the pathways which transmit the theta r h y t h m to the V M T are not well known. However, it is reasonable to suppose that the fibres o f the post-commissural fornix are involved in this transmission.
We would like to thank Mrs A. M. Perret and Mrs M. Mallet for their technical assistance.
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