Selective regulation of thalamic sensory relay nuclei by nucleus reticularis thalami

476

Electroencephalography and Clinical Neurophysiology, 1976, 4 1 : 4 7 6 - - 4 8 2 © Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

SELECTIVE R E G U L A T I O N OF THALAMIC SENSORY R E L A Y NUCLEI BY NUCLEUS R E T I C U L A R I S THALAMI * CHARLES D. YINGLING ** and JAMES E. SKINNER

Biology Department, Rice University; Physiology Department, Baylor College of Medicine; and Neurophysiology Service, The Methodist Hospital, Houston, Texas 77025 (U.S.A.) (Accepted for publication: April 5, 1976)

Selective attention in human subjects results in the specific enhancement of cortical evoked responses to attended stimuli (Spong et al. 1965; Hillyard et al. 1973; also see Desmedt (Ed.) 1975), whereas arousal causes the enhancement of cortical responses to both relevant and irrelevant stimuli alike (Niititfinen 1970). Stimulation of the mesencephalic reticular formation enhances evoked potentials mainly by increasing thalamic transmission in the primary afferent p a t h w a y (Bartlett and D o t y 1974; Rapasardi et al. 1974}. This stimulation affects all sense modalities and is independent of the precise location of the stimulus in the mesencephalic reticular region (Bremer and Stoupel 1959; D u m o n t and Dell 1960), findings which suggest that the evoked potential enhancement is general, as in the process of arousal. Blockade in the mediothalamic-frontocortical system also enhances evoked potentials by increasing thalamic transmission, but, in contrast to the enhancement caused by the mesencephalic reticular stimulation, various sense modalities are affected selectively depending upon the precise location of the blockade and its extent (Skinner and Lindsley 1971). * This work was supported by Grants HL 05435 and HL 13837 from the National Heart and Lung Institute, NIH, U.S. Public Health Service. ** C.D. Yingling was the recipient of a predoctoral fellowship from the National Science Foundation. Present address: Langley Porter Neuropsychiatric Institute, University of California, San Francisco, Calif. 94143, U.S.A.

Evidence has been presented in two recent papers from our laboratory that the mesencephalic reticular formation and mediothalamic-frontocortical system both control nucleus reticularis thalami (R) and that R is inhibitory upon the thalamus (Yingling and Skinner 1975; Skinner and Yingling 1976). Stimulation of a particular region in the anterior portion of R was found to inhibit the transmission of visual impulses through the laterial geniculate b o d y (Skinner and Yingting 1976), a finding which demonstrates that R is the source of a powerful inhibitory influence on thalamic relay nuclei. In the present paper, we will examine the effects of stimulation in various regions of R on the amplitudes of cortical evoked potentials in the three major sense modalities. These results will suggest that the thalamic inhibition produced by such punctate stimulation of R is highly selective in its regulation o f sensory evoked potential amplitude. Methods

Experiments were performed successfully in eight cats at both the time of operation and later in a recovered chronic condition. Bipolar stainless-steel stimulating electrodes were implanted stereotaxicaUy in: (1) prethalamic sensory afferent channels Coptic tract, brachium of the inferior coUiculus); and (2) various locations within nucleus reticularis thalami (R). Monopolar, stainless-steel screw electrodes

NUCLEUS RETICULARIS THALAMI (referenced to frontal sinus septal bone) were placed on the dura above the surface of the primary sensory cortices (marginal gyms, middle ectosylvian gyms, lateroposterior anterior sigmoid gyms). A pair of stainlesssteel wires were sutured through the skin of the forelimbs in order to provide cutaneous stimuli. The subcortical electrodes were adjusted in unanesthetized animals immobilized with gallamine triethiodide (Flaxedil). This was done because it was f o u n d that barbiturate anesthesia produced a large variance in the amplitudes of each of the sensory cortex evoked potentials, a condition which made it difficult to assess the effect of R stimulation upon them. All surgery was performed rapidly under sodium pentothal anesthesia and all w o u n d edges were infiltrated with lidocaine. Following surgery the animals were immobilized and artificially ventilated. Respiratory rate was controlled to maintain blood PO:, PCO2 and PH within normal limits (a Coming blood gas analyzer was used). In accordance with the standards set b y the American Physiological Society, the conscious animals were kept free from pain. All electrode placements were later confirmed histologically using standard methods (Skinner 1971). Natural stimuli, as well as electric stimuli to the sensory channels, were paired with prior conditioning stimulation to the R electrodes. The interval between the conditioning stimulus and the test stimulus was varied systematically from 1 to 1000 msec until an o p t i m u m inhibitory effect was observed. When necessary two-tailed t tests were performed between the mean amplitude of 10 nonconditioned control evoked responses and 10 conditioned experimental ones. A control for the constancy of sensory input was made by the direct electric stimulation of the sensory pathways; therefore it was felt unnecessary to dilate the pupils or equip the animals with earphones in order to maximize the constancy of the natural sensory inputs. An a t t e m p t was made, however, to keep the natural stimuli as constant as

477 possible by delivering them to the animals while they were sitting quietly in a restraining box, to which they were adapted, with their ears and eyes in alignment with the sources of auditory and visual stimuli. If the animal was agitated or showed EEG signs of drowsiness, then the experiment was postponed. The photic stimuli were delivered only when the animal's eyes were open and fixated in the horizontal plane, and the pupils were at a 4 mm horizontal diameter produced by adjusting the r o o m lights. The photopic energy of the flash was 170 lux-sec measured directly in front of the reflector unit at 10 cm (Fuller et al. 1975) and was from a 750,000 candle, 10/~sec Xenon discharge focused with a parabolic mirror (Grass photostimulator PS-2 at intensity 16). The source was located 2 ft. in front of the eyes and approximately 4 ft. from the sagittal plane of the head. The auditory stimuli were clicks from 8 ~ crystal earphones, located 4 in. from the ears, that were driven by 15 V, 0.5 msec duration pulses. The somatic stimuli were 20 V, 0.5 msec duration electric pulses delivered to the forearm electrodes.

Results Visual cortex evoked potentials were elicited in immobilized cats b y single optic tract stimuli (2--4 V, 0.5 msec duration) while a second stimulating electrode was progressively lowered through: (1) the optic radiations (OR); (2) nucleus reticularis thalami adjacent to the lateral geniculate ( R L 6 ) ; and (3) the lateral geniculate b o d y (LG). Brief stimulus trains were systematically delivered to this second electrode 1--1000 msec prior to the optic tract stimulus. As the electrode approached the thalamus, a region was found which highly attenuated all c o m p o n e n t s o f the visual evoked potential; when the electrode was lowered farther, the inhibitory effect disappeared. Histological examination later showed the zone of maximum inhibition to be RL6. The inhibitory effect was obtained

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w h e n Lhe interval b e t w e e n the end o f tim cond i t i o n i n g stimulus to RLc, and the test stimulus t o the o p t i c t r a c t was f r o m 1 t o 150 reset. T h e o p t i m a l i n t e r s t i m u l u s interval, utilizing t h e l o w e s t c o n d i t i o n i n g s t i m u l u s intensity, ranged b e t w e e n 50 a n d 100 m s e c f o r all o f the animals. T h e i n h i b i t o r y e f f e c t was generally so striking, w i t h no o v e r l a p in the d i s t r i b u t i o n o f the c o n t r o l and experim e n t a l a m p l i t u d e s , t h a t statistical tests w e r e n o t r e q u i r e d to d e m o n s t r a t e the effect. T h e localization o f the i n h i b i t o r y e f f e c t to RLG was r e p l i c a t e d in t h r e e c h r o n i c preparat i o n s i m p l a n t e d with six e l e c t r o d e s spaced 1 m m a p a r t and p l a c e d so t h a t t h e a r r a y s t r a d d l e d R~,G, with the higher tips in the O R and the l o w e r o n e s in t h e LG, as illustrated in Fig. 1. M a x i m a l inhibition o f t h e visual e v o k e d r e s p o n s e was o b t a i n e d by s t i m u l a t i o n

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Fig. 1. R e d u c e d transmission o f a f f e r e n t signals li~rough the lateral genieulate b o d y (LG) following a e o n d i l i o n i n g stimulus to the adjacent part o f nucleus reticularis thalami (R). The trace marked C O N T R O l , was r e c o r d e d in p r i m a r y visual c o r t e x and elicited by a single i l 5 msee sfinmlus (,o the ot)lie ltact. The lraces marked 1 --.~ were eliciled and r e c o r d e d in this same m a n n e r , excep) l h a i t h e y were preceded l()0 msec earlier hy a negative c o n d i t i o n i n g stimulus (250 c/see, 30 reset) lo t.he e l e c t r o d e sites illustrated to the right (diagram is from the atlas of Jasper and A j m o n e Marsan 1954). S t i m u l a t i o n outside o f R, in LG or the optic radiations, had n o significant e f f e c t , whereas s t i m u l a t i o n within RI, G significantly r e d u c e d b o t h early and late c o m p o n e n t s o f t h e r e s p o n s e ( P ~ 0.()I),

o f tile central e l e c t r o d e s o f the array, in or just a d j a c e n t to RL(~ : the e f f e c t was a b s e n t or m u c h w e a k e r w h e n s t i m u l a t i n g on either side o f RL~;, i.e.. in the OR or LG. Tests of m e a n d i f f e r e n c e s (t Lest) of 10 responses each s h o w e d t h a t s t i m u l a t i o n outside o f R, i.e., in LG or OR,, had no significant e f f e c t o n the s e n s o r y e v o k e d potentials, w h e n c o m p a r e d to t h e n o n c o n d i t i o n e d c o n t r o l responses, whereas s t i m u l a t i o n o f RL~, significantly r e d u c e d h o t h early and late c o m p o n e n t s o f the s e n s o r y responses (P < 0.011. E v o k e d p o t e n t i a l s elicited by p h o t i c stimuli were also s h o w n in c h r o n i c p r e p a r a t i o n s to be inhibited b y p r i o r s t i m u l a t i o n o f RL6, b u t o n l y if the flash stimulus was localized in the visual hemifield contralatcral to the site o f l~Lt; s t i m u l a t i o n , as illustrated by Fig. 2. This p r o c e d u r e isolated the e v o k e d activity t o the side o f t h e t h a l a m u s being s t i m u l a t e d , t h u s p r e v e n t i n g e v o k e d cortical a c t i v i t y via a callosal p r o j e c t i o n f r o m t h e o p p o s i t e hemisphere. T h e o b t a i n e d result s h o w s t h a t t h e i n h i b i t o r y e f f e c t o f RL~ s t i m u l a t i o n is limited ~o the ipsilateral t h a l a m u s . T h e e f f e c t of RLG s t i m u l a t i o n was f o u n d to be specific to the visual m o d a l i t y , as it did n o t a f f e c t a u d i t o r y or s o m a t o s e n s o r y e v o k e d p o t e n t i a l s ; stimu l a t i o n o f RL(; was also w i t h o u t effect on n o n p r i m a r y e v o k e d responses to o p t i c t r a c t stimuli r e c o r d e d in a u d i t o r y cortex. T h e i n h i b i t o r y e f f e c t was next t e s t e d m the a u d i t o r y m o d a l i t y by s t i m u l a t i n g various r e g m n s o f R, especially t h o s e lateral to t h e medial geniculate (RM~). T h e bilateral rep r e s e n t a t i o n o f a u d i t o r y i n f o r m a t i o n in the t h a l a m u s p r e v e n t s the unilateral isolation o f ew)ked activity m a m a n n e r a n a l o g o u s to the visual syst, em: hence, mlilateral R M (; ~timulal.l(m was ineffecl,iw t~ reducing a u d i t o r y cort, ex e v o k e d l.)olenttats to binaural ()r m o n a u r a l click stimuti~ th)wever, when ~tm activity was r e s t r i c t e d zo one side b y elecm c a l l y s t i m u l a t i n g the b r a c h i u m of the inferior collieulus (BIC) just p o s t e r i o r to the MG, a c o n d i t i o n armlogous ~o o p t i c tract s t i m u l a t i o n m the visual s y s t e m , a parallel result was o b t a i n e d as illustrated in Fig. 3.

NUCLEUS RETICULARIS THALAMI

CONTRALATERAL FLASH Control

479

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1: I; Fig. 2. Effects on photic evoked potentials recorded in visual cortex (V CX) of unilateral stimulation of nucleus reticularis thalami adjacent to the lateral geniculate body (RLG). Photic stimuli were presented in the visual fields contralateral and ipsilateral to the stimulating electrode in RLG and the recording electrode in V CX. Responses to contralateral flashes, which project through the side of the thalamus containing the RLG electrode, are abolished by prior stimulation of RLG (30 msec, 250 c/sec train delivered 50 msec preceding the test flash). The same RLG stimulus does not abolish the responses to ipsilateral flashes, which are relayed through the other side of the thalamus. Calibrations: 200 pV, 100 msec.

RMG s t i m u l a t i o n d u r i n g t h e o p t i m u m 5 0 - 1 0 0 m s e c p r e c e d i n g t h e s t i m u l u s t o BIC h i g h l y a t t e n u a t e d all c o m p o n e n t s o f t h e a u d i t o r y e v o k e d p o t e n t i a l (P < 0 . 0 1 ) . Simil a r l y , s t i m u l a t i o n o n e i t h e r side o f RMG , i.e., in t h e a u d i t o r y r a d i a t i o n s o r t h e MG, h a d l i t t l e o r n o e f f e c t ; RMG s t i m u l a t i o n h a d n o effect on visual or s o m a t o s e n s o r y ev o k ed potentials. In o r d e r t o t e s t t h e i n h i b i t o r y e f f e c t o n cutaneous evoked responses, stimulation of R adjacent to the ventrobasal complex (RvBc), was p r o d u c e d p r i o r t o a t e s t s h o c k d e l i v e r e d t o wires s u t u r e d t h r o u g h t h e s k i n on t h e contralateral forelimb. The somatosensory e v o k e d p o t e n t i a l was c o m p l e t e l y b l o c k e d b y RvBc stimulation within the optimum 50--100 msec interval prior to the skin shock (Fig. 3). As w o u l d be e x p e c t e d , R v B c s t i m u l a t i o n h a d n o e f f e c t on v i s u a l o r a u d i t o r y evoked potentials.

Fig. 3. Reduction of evoked potentials in three major sense modalities by stimulation of various regions of nucleus reticularis thalami (R) adjacent to different thalamic relay nuclei. Visual evoked potentials (VEPs) were elicited by optic tract (ot) stimulation and recorded in primary visual cortex (V CX); auditory evoked potentials (AEPs) were elicited by stimulation of the brachium of the inferior colliculus (bic) and recorded in primary auditory cortex (A CX); somatosensory evoked potentials (SEPs) were elicited by stimulation of stainless-steel wires sutured through the skin of the hind leg and recorded in the contralateral somatosensory cortex (far lateral anterior sigmoid gyrus, AS). Conditioning stimuli of 250 c/sec, 20 msec trains were delivered to either RLG , RMG or RVBC 50 msec prior to the test stimulus. Stimulation of RLG attenuates the VEP but has no effect on the AEP or SEP; similarly, RMG stimulation affects only the AEP and stimulation of RVB c affects only the SEP. Stimulation 1 mm on either side of these various regions of R had no effect on reducing the primary sensory evoked potentials. Calibrations: 200 pV; 4 msec (VEPs), 10 msec (AEPs and SEPs).

Discussion The results show that stimulation of various p a r t s o f t h e t h a l a m i c r e t i c u l a r n u c l e u s ( R ) will i n h i b i t s p e c i f i c a l l y t h e c o r t i c a l e v o k e d responses m e d i a t e d through the adjacent thalamic relay nucleus. S t i m u l a t i o n on either the t h a l a m i c o r t h a l a m o c o r t i c a l r a d i a t i o n side o f t h e e f f e c t i v e r e g i o n o f R has n o e f f e c t on t h e s e n s o r y e v o k e d r e s p o n s e s . T h i s f i n d i n g indic a t e s t h a t t h e i n h i b i t o r y e f f e c t is m e d i a t e d b y f i b e r s a r i s i n g in RLG a n d is n o t d u e t o s t i m ulation of fibers traversing R or to activation of inhibitory interneurons within the thalamus itself. T h i s s t i m u l a t i o n a r o u n d R serves as a

480 control for the possibility of the effect being due to cortical recovery cycles (Allison 1962); such a control is necessary since any stimulus to R inevitably excites the thalamocortical fibers of passage, thus giving rise to a cortical evoked response, Stimulation on either side of R also excites these same fibers, b u t has no inhibitory effect on the test evoked response amphtude. Therefore, the dramatic inhibitory effects observed following R stimulation must be due to inhibitory projections arising from cells in R. T w o previous papers from our laboratory showed that both the mesencephalic reticular formation (MRF) and the mediothalamicfrontocortical (MTFC) systems regulate unit activities and concomitant slow potential shifts in R (Yingting and Skinner 1975; Skinner and Yingling 1976). The present results illustrate the specificity of the inhibitory influence that R has on the control of input to the cortex in three different sense modalities. Thus, the pattern of regulation of R b y the M R F and MTFC systems determines the pattern of regulation of cortical sensory evoked potentials. Bremer and Stoupel (1959) and D u m o n t and Dell (1960) first demonstrated that stimulation of the M R F produces a dramatic general facilitation of both early and late components of all sensory evoked potentials. These initial observations have been extended to show that the enhancement effect of MRF stimulation, at least in the visual system, is exerted primarily at the thalamic level (Bartlett and D o t y 1974; Rapasardi et al. 1974). The enhancement effect was found b y Bremer and Stoupel (1959) t o last for 20 sec or more following a brief stimulus to the MRF. We have shown that units in R are themselves inhibited for 20 sec or more by a brief M R F stimulus (Yingling and Skinner 1975). Thus it appears that a similar time course exists for both the R unit inhibition and the sensory evoked potential facilitation that occur following M R F activation. Therefore, we suggest that the enhancement of evoked potential amplitude produced b y

C.D. YINGLING, J.E. SKINNER MRF activation is the result of the general inhibition of R cells that, in turn, releases the thalamic relay nuclei from inhibition. The MTFC system, in contrast to the MRF, seems to be more selective in its regulation of sensory evoked potentials. Skinner and Lindsley (1971) showed that partial blockade of the MTFC system by cooling the inferior thatamic penduncle to 15°C enhanced visual evoked potentials, but had no effect on auditory evoked potentials. Increasing the size of the blockade by further cooling to 10°C, thus involving more fibers in the inferior thalamm peduncle, resulted in enhancement of evoked potentials in both auditory and visual modalities. The descending influence on R units from the frontal granular cortex appears to be excitatory because it is abolished following blockade in the inferior thalamic peduncle, as discussed previously (Yingling and Skinner 1975; Skinner and Yingling 1976). Removal of such descending excitation on a thalamic structure that has inhibitory control over the sensory relay nuclei would have the net effect of disinhibiting them and increasing sensory evoked potentials, either selectively or generally, depending upon the pattern of excitation that remained. In this study we have shown that sensory evoked potentials can be selectively abolished b y stimulation of highly specific points in R. A similar selective, modality-specific organization is found in the inferior thalamic peduncle, a pathway which appears to mediate the excitation of R by the frontal cortex. Therefore, the selective regulation of evoked potentials appears to arise from the frontal cortex. This frontocortico-R system, b y regulating patterns of thalamic inhibition, could thus control the selective ascent of sensory information to widespread regions of cortex. This function is similar to that of the selective filter postulated in psychological theories of attention (James 1890; Broadbent 1958; Moray 1970). The override of this selective pattern o f inhibition by activation of the M R F could underlie the general and reflexive arousal that typifies the orienting response.

NUCLEUS RETICULARIS THALAMI

Summary Stimulation in the segment of nucleus reticularis thalami adjacent to the lateral geniculate body (RLG), abolished visual evoked potentials for up to 150 msec. Both photic stimulation in the contralateral visual field and electric stimulation in the ipsflateral optic tract elicited primary cortical responses that were markedly reduced or abolished by prior conditioning stimulation in RLO. Stimulation of the segments of nucleus reticularis thalami adjacent to the medial geniculate ( R M G ) o r the ventrobasal complex (RvBc) had the effect of markedly reducing or abolishing unilaterally projected primary evoked responses in the auditory and cutaneous systems, respectively. Only the sensory evoked potentials mediated by the relay nucleus adjacent to the region of R stimulated were affected. The reduction of the cortical evoked potentials was not due to the processes underlying the cortical recovery cycle, because conditioning stimulation on either side of RLG stimulated the primary geniculocortical fibers, but had a minimal or no effect on the visual test evoked response. These results suggest that R functions as a topographically organized inhibitory gate which can regulate the patterns of sensory input from the thalamus to the cortex. The regulatory effects on R by the mesencephalic reticular formation and the mediothalamic-frontocortical system may mediate both generalized and selective control of cortical sensory evoked potentials.

481

du champ visuel controlat~ral et la stimulation 61ectrique du tractus optique ipsilat6ral font apparaftre des feponses corticales primaires qui sont nettement rdduites ou abolies par conditionnement prdalable par stimulation du RLG. La stimulation des segments du noyau r6ticulaire thalamique adjacents au g6nicul~ m6dian (RMG) OU au complexe ventrobasal ( R v s c ) a pour effet de r~duire de faqon marqude ou d'abolir les r6ponses 6voqu6es primaires projetdes unilat6ralement dans le syst6me auditif et cutan6, respectivement. Seuls les potentials 6voqu6s sensoriels m6diatis6s par les noyaux de relai adjacents ~ la r6gion du R stimul6e sont affectds. La r6duction des potentiels dvoqu6s corticaux n'est pas dfie au processus qui soutend le cycle cortical de rdcupdration, car la stimulation de conditionnement de chaque c6t6 du RLG stimule les fibres g6niculo-corticales primaires, mais a un effet minime ou nul sur les r6ponses 6voqu6es au test visuet. Ces rdsultats sugg6rent que le R fonctionne comme une fen~tre inhibitrice topographiquement organis6e, qui peut r6guler les patterns d'affdrences sensorielles allant du thalamus au cortex. Les effets r~gulateurs de R par la formation rdticulaire mdsencephalique et le systhme mediothalamique-frontocortical peuvent m6diatiser ~ la fois le contrSle g6n6ralis6 et s61ectif des potentiels dvoquds corticaux sensoriels.

The authors wish to thank Gregory L. King for his invaluable assistance.

R6sum6

References

Rdgulation sdlective des noyaux de relai sensitif thalamiques par le noyau rdticulaire du thalamus

Allison, T. Recovery function of somatosensory evoked responses in man. Electroenceph. clin. Neurophysiol., 1962, 14: 331--343. Bartlett, J.R. and Doty Sr., R.W. Influence of mesencephalic stimulation on unit activity in the striate cortex of squirrel monkeys. J. Neurophysiol., 1974, 37: 642--652. Bremer, F. et Stoupel, N. Facilitation et inhibition des potentials 6voqu6s corticaux dans l'6veil c6r6bral. Arch. int. Physiol. Biochim., 1959, 67: 240--275.

La stimulation du segment du noyau r6ticulaire du thalamus adjacent au corps g6nicul6 lateral (RL6) abolit les potentiels ~voqu6s visuels pendant une pdriode pouvant atteindre 150 msec. La stimulation photique

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C.D. YINGLING, J.E. SKINNER Scheibel, M.E. and Scheibel, A.B. The organization of the nucleus reticularis thalami: a Golgi study. Brain Res., 1966, 1: 43--62. Scheibel, M.E. and Scheibel, A.B. Structural organization of nonspecific thalamic nuclei and their projection toward cortex. Brain Res.. 1967, 6: 60--94. Skinner, J.E. Neuroscmnce: a laboratory manual. W.B. Saunders, Philadelphia, Pa., 1971. Skinner, J.E. and Lindsley, D.B. Enhancement of visual and auditory evoked potentials during blockade of the nonspecific thalamo-cortical system. Electroenceph. c]in. Neurophysiol., 1971, 31 : 1--6 Skinner, J.E. and Yingling, C.D. Regulation of slow potential shifts in nucleus reticularis thalami by the mesencephalic reticular formation and the frontal granular cortex. Electroenceph. clin. Neurophysiol., 1976, 4 0 : 2 8 8 296. Spong, P., Haider, M and Lindsley, D.B. Selective attentiveness and cortical evoked responses to visual and auditory stimuli. Science, 1965, I48: 395--397. Yingling, C.D. and Skinner, J.E. Regulation of unit activity in nucleus reticularis thalami by mesencephalic reticular formation and the frontal granular cortex. Electroenceph. clin. Neurophysiol., 1975, 39: 635--642.