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Suppression of focal spikes by somato-sensory stimuli
574
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
SUPPRESSION OF FOCAL SPIKES BY SOMATO-SENSORY STIMULI C. A. TASSINARI, M . D . ~
lnstitut National de la Sant~ et de la Recherche Mddicale,
Marseille (l-¥ance)
(Accepted for publication: April 19, 1968)
I t is well known clinically that focal epileptic discharges may be suppressed by peripheral somato-sensory stimuli, such as rubbing, moving or compressing the segments initially involved by the seizure (Gowers 1881 ; Forster et al. 1949; Jackson 1958; Symonds 1959, 1961; Paulson 1963); E E G evidence of this type of inhibition is, however, scanty. The aim of this work is to describe E E G studies related to the nature of the lesion and the mechanisms responsible for the suppression of inter-ictal focal spike activity by specific somato-sensory stimuli with a strict somatotopic distribution. A study of the reactivity of the spikes and the distribution of the seizures during the different phases of sleep allows some comments on the factors facilitating nocturnal seizures. CASE REPORT The patient was an l l-year-old boy, with a right hemiparesis that followed a traumatic delivery with subarachnoid haemorrhage. From the age of 8 years onwards the patient had nocturnal attacks, described as a sudden and generalized muscular contraction, which recurred 2-4 times every week. Neurological examination showed a marked hemiatrophy of the right side of the body and face; there was slight spasticity and weakness with exaggerated tendon jerks and an extensor plantar response on the right side. Sensation was normal. A pneumoencephalogram was regarded as normal, as were other routine biological and radiographic examinations. METHOD The EEGs were recorded from bipolar and average reference montages. Surface electrodes were used to record the electrocardiogram, oculogram and the electromyograms of the deltoid, extensors and flexors of the wrist, quadriceps and gastrocnemius muscles, on both sides. Different types of stimulation were performed under polygraphic control, while the child was awake and during nocturnal spontaneous sleep. 1 Charg¢ de Recherche at INSERM, 300 Bvd. Ste. Marguerite, Marseille, France. Present address: University of Bologna, Italy.
RESU LTS Serial EEGs were taken from the age of 3 years, at intervals of 4-6 months. Between the ages of 3 and 5 years the records were characterized by intermittent, high voltage 1.5-3 c/sec waves over the frontal regions. In subsequent years the slow waves progressively decreased in persistence and amplitude and high voltage sharp waves appeared over the left fronto-central area. At the age of 8 years, when seizures first occurred, the records were characterized by frequent sharp waves intermixed with slow waves over the left fronto-parietal and over the midline regions. At times the sharp waves became rhythmic, at 2-4 c/sec, continuous and spread bilaterally over the anterior head regions. During subsequent years the slow waves disappeared and the sharp waves became of smaller amplitude, of shorter duration and restricted to the midline regions. At the time of our observation the E E G showed the following characteristics:
During wakefulness 1. The dominant rhythm over the occipital regions was at 10-11 c/sec, roughly symmetrical and blocked normally by visual attention. Bi- or triphasic spikes, with an amplitude of 100-150/~V, recurred rhythmically at 3-4 c/sec over the central and posterior midline regions. These were continual and were present in every record taken during a month in hospital. At times, spikes of smaller amplitude appeared over the left fronto-temporal area (Fig. l). 2. Reactivity of the spikes. (a) Effective stimuli: the continuous rhythmic spikes were suppressed by passive (Fig. 2,a) and voluntary (Fig. 2,b) movements of flexion or extension of the right foot; a similar effect was obtained by rubbing or stroking the sole of the right foot, such as during the Babinski manoeuvre (Fig. 2,e). Suppression of the spikes by such stimuli--which will be referred to as effective stimuli--was constant, reproducible at will, and persisted without habituation. The effective stimuli blocked the spikes regardless of anticipation. In all instances, the spikes reappeared immediately after the end of any form of stimulation. Contemplation of movement only did not suppress the spikes. (b) Ineffective stimuli: tactile stimuli and passive and voluntary movements involving regions other than the right foot did not modify the spike activity. Visual and acoustic stimuli, mental activity (calculation, reading) Electroenceph. elin. Neurophysiol., 1968, 25:574-578
SPIKE SUPPRESSION BY SENSORY STIMULI
MONOPOI.AR "AWAKE
575
BIPOLAR "AWAKE:
l: :
,_-,
Fig. 1 Subject awake. Left: common reference recording (eyes open); right: bipolar recording (eyes closed). Continuous inter-ictal spike activity over the central and posterior midline regions. Amplitude calibration: I00 #V. Q
EMG. R.LEG ~ -~...... -'<---~-~:i i,:v ~/
/,.; .......
b
c
Fig. 2 Subject awake. EMG. R. LEG: electromyogram of the right gastrocnemius recorded in a and b. The spikes are suppressed: by passive movements of the right foot (a); by plantar flexion (b) and by tactile stimuli to the sole of the right foot as in Babinski's manoeuvre (c, horizontal bars). and situations of emotional stress did not modify the spike activity. 3. Evoked potentials. During induced suppression of
spike activity, percussion of the right Achilles tendon or foot evoked high voltage potentials over the central midline region (Fig. 3). Evoked potentials were not observed
Electroenceph. clin. Neurophysiol., 1968, 25:574-578
576
¢. A. TASSINARI
E EG= I,oo~vlsec E M G : I ~oo~,v- -
51GNAL RIGHT LEG . . . . . ~ / ~ - - ~
" ~ - ~ - ~ r ~
Fig. 3 Subject awake. Potentials evoked in the midline region by percussion (R) of the right Achilles tendon. R I G H T LEG: E M G of the right gastrocnemius-soleus muscles. to follow percussion of regions other than the right foot or during acoustic stimulation, movements of the arms and of the left leg.
During sleep The frequency and morphology of the midline spikes were not significantly modified during all stages of sleep. - ~'~
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1. The reactivity of the spikes. The stimuli effective during wakefulness also suppressed the spike activity during rapid eye movement (REM) stages of sleep, but were ineffective during stages 2, 3 and 4. Other forms of stimulation were ineffective during all phases of sleep. 2. The seizures. (a) Seven electro-clinical seizures were recorded during 6 h and 20 rain of spontaneous nocturnal sleep: four seizures during stage 2, two during stage 4 and one after a movement at the end of an R E M stage, which passed into stage 2. The seizures (Fig. 4), which did not waken the child, were characterized by a sudden flexion of the trunk and rotation of the head to the right; the arms elevated and abducted, the forearm being flexed at the elbow; the legs were hyperextended in adduction, with the feet rotated inwards. The E E G discharge was a synchronous paroxysm of rhythmic activity at 6-8 c/sec, which increased progressively in amplitude from 50 to 250-350 #V. The discharge, which was of greater amplitude on the left, involved all regions of the scalp except the central andposterior midline areas, where the spike activity persisted unchanged. (b) Nineteen subclinical paroxysmal discharges were recorded during stages 2, 3 and 4, fifteen of them during stage 2. From the EEG point of view the morphology and topography of the discharges were similar to those described previously, but they were less persistent (4-6 sec).
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Fig. 4 Sleep, stage 2: Electro-clinical seizure. Electromyographic recordings from left deltoid (L.A.), right deltoid (R. A.) and right gastrocnemius (R. L.). The EEG paroxysm is generalized, but maximal over the anterior region. The spike activity continues unaltered throughout.
Electroenceph. clin~ Neurophysiol., 1968, 25 : 574-578
SPIKE SUPPRESSION BY SENSORY STIMULI DISCUSSION
1. Topography of the epileptogenic lesion A right hemiparesis with hemiatrophy indicates a lesion involving the left post-central cerebral cortex (Penfield and Robertson 1943). The topography of the spikes, and their suppression by sensory stimuli applied to the right foot, suggest that the lesion also involved the sensory projection area of the right foot. 2. Mechanisms o f suppression o.f the spike discharges The strict somatotopy and constant suppression of the spikes by the effective stimuli, without habituation, suggest that the desynchronization was mediated by the specific sensory projection system rather than by the diffuse reticulo-cortical system, since attentive, emotive factors or conditioning mechanisms, which may facilitate or suppress epileptic discharges (Lairy 1956; Goldie and Green 1959; Stevens 1959), had no such effects. Furthermore, the spikes were suppressed during wakefulness and during sleep, in R E M stages, without the awareness of the subject. 3. The spike "rhythm" as a result of a cortical lesion in the condition of partial deafferentation (isolated cortex) The spikes which appeared over the central and posterior midline regions may be considered as a "spike rhythm" characterized by its topography, continuity and periodicity, as well as by its specific reactivity to certain stimuli. This is a rare example of abnormal EEG activity, which can be defined by the same parameters as physiological rhythms. The reactivity of the physiological rhythms, however, is less specific and does not usually show as strict a somatotopy as the spikes recorded in this case. The electrical activity in chronic partially isolated somato-sensory cortex is characterized by: (a) the appearance of paroxysmal bursts of slow waves, which are progressively replaced by spike discharges (Grafstein and Sastry 1957; Echlin and Battista 1963); (b) by high voltage evoked potentials in response to local electrical stimulation or to afferent stimuli applied to peripheral nerves (Burns 1950; Echlin and Battista 1961); (c) by the occurrence of subclinical seizures, spontaneous or induced by repetitive stimulation of peripheral nerves (Echlin and Battista 1961). Similar features were also found in this case. The importance of the passage of time in determining the continuity and rhythmicity of the spikes is stressed since these patterns appeared 10 years after birth. The rhythmicity of the spikes could result from a progressive increase in the excitability of a partially isolated area, or from a change in the degree and quality of the afferent input "driving" the hyperexcitable neurones into rhythmic activity. It was found by Burns (1950) and by Echlin and Battista (1961 and 1963) that "the spontaneous" activity in the partially isolated cortex (somato-sensory area) was largely dependent on the afferent input to this area. That sensory afferents from the periphery could contribute to such triggering of the rhythmic spikes in our subject is suggested indirectly by the effectiveness of sensory stimulation of the right foot in modifying the focal epileptic activity, and by the high voltage potentials evoked in the central
577
midline region by synchronous afferent volleys evoked by percussing the right foot. Facilitation or suppression of focal epileptogenic activity, only and specifically by somato-sensory stimuli, is a rare event in human epilepsy (Vizioli 1962; Gastaut and Tassinari 1966). In the few reported cases (Forster et al. 1949; Turinese 1956; Tudor et al. 1966) it could be that the epileptogenic lesion in the somato-sensory area was in a state of partial deafferentation. If this hypothesis is correct, our observation indicates that an additional characteristic of the partially isolated sensory-motor cortex is suppression of the epileptic activity by an asynchronous sensory barrage, with a strict somatotopy.
4. The seizures The generalized tonic contractions did not suppress the spike activity but, since the seizures occurred during the slow wave stages of slcep, this could be the consequence of the same factors which rendered ineffective the tactile and proptioceptive stimuli applied to the right foot. Alternatively, during the seizures, mechanisms of occlusion may have been active at a subcortical level, or the epileptic discharge could have excited the cortical, cerebellar or reticular system whose stimulation could subsequently decrease the sensory afferent input at a spinal level (Hagbarth 1960). 5. Factors leading to seizures during sleep Since the somato-sensory afferents from the right foot suppressed the focal epileptic discharges, it is conceivable that the continuous sensory input resulting from daily activity (standing, walking, etc.) prevented the occurrence of diurnal seizures. This does not necessarily imply that the seizures which occurred during sleep did so merely because this is a state of rest with diminished somatosensory cortical inflow. The absence of seizures during the R E M stages of sleep is unlikely to be due to the shorter duration of these stages: 26 seizures occurred during 315 min of slow E E G sleep, while none occurred during 65 rain of R E M sleep. In an unselected population of epileptics, sleep does not facilitate but usually decreases the frequency of seizures (Gastaut et al. 1965). It may be that the slow stages of EEG sleep represent a state of further functional deafferentation, as compared to wakefulness I and to R E M sleep. This could result in the failure of sensory stimulation to suppress the spike activity. The slow stages would facilitate the seizures by reduction of somato-sensory input, having a suppressive effect on the epileptic discharges. Such factors could account for the frequent occurrence of nocturnal seizures in human subjects 1 It is known that even at rest there is a continuous sensory inflow from the periphery which participates in the control of the electrical activity of the somato-sensory areas. Decreased somato-sensorv input by posterior chordotomy facilitates the synchronization of the cortical activity in the corresponding regions of sensory projections (Anderson 1962), and may even produce frank epileptiform activity in the thalamic (VPL nuclei) and cortical (somatosensory) regions (Bava et al. 1966).
Electroenceph. clin. Neurophysiol., 1968, 25:574-578
578
c . A . TASSINARI
(Turinese 1956; Kaitor 1963; Tudor et al. 1966; ScolloLavizzari and Hess 1967) and in monkeys (Ward 1961), with a focal lesion in the somato-sensory region whose seizures are otherwise precipitated by somato-sensory stimuli. SUMMARY The EEG findings in a child with a right hemiparesis and hemiatrophy associated with nocturnal seizures are described. Rhythmic inter-ictal spike activity was present continuously over the central and post-central midline regions, and this could be selectively suppressed by tactile stimulation and voluntary or passive movements of the right foot. This effect was present during wakefulness and rapid eye movement sleep, but was abolished during the slow stage of sleep, during which all seizures occurred. These findings are discussed in the light of physiological studies on the experimental isolated cortex. It is concluded that the post-Rolandic lesion in this patient led to partial deafferentation, which was enhanced during the slow stage of sleep, thereby leading to clinical and subclinical seizures. RI~SUMI~ SUPPRESSION DE POINTES FOCALES PAR DES STIMULATIONS SOMATO-SENSORIELLES L'auteur presente l'6tude EEG d'un garqon avec h6mipar6sie et h6miatrophie droite, associ6es ~t des crises 6pileptiques nocturnes. Les trac6s se caract6risent par une activit6 de pointes, rythmiques et continues, localis6e dans la r6gion du vertex moyen et post6rieur, 61ectivement supprim6e par des stimulations tactiles et des mouvements passifs ou volontaires du pied droit. Cet effet peut 6tre observ6 pendant la veille et pendant la phase des mouvements oculaires du sommeil; par contre, au cours du sommeil lent, pendant lequel surviennent les crises 6pileptiques, les stimulations du pied droit ne parviennent plus fi bloquer les pointes. Ces donn6es sont discut6es ~ la lumi~re des 6tudes physiologiques sur le cortex isol6. L'auteur conclue que chez ce malade il y avait une 16sion post-Rolandique en 6tat de d6aff6rentation partielle; le sommeil lent augmenterait cet 6tat de d6aff6rentation, favorisant ainsi l'apparition de crises 6pileptiques cliniques et infra-cliniques. REFERENCES ANDERSON, S. A. Localised slow wave activity in the somato-sensory cortex. Med. exp. (Basel), 1962, 6: 21-24. BAVA, A., FADIGA, E. e MANZONI, T. Risposte convulsive in strutture sottocorticali di relais somatico e nella corteccia di preparati cronici parzialmente deafferentati. Boll. Soc. ital. Biol. sper., 1966, 42: 1-3. BURNS, B. D. Some properties of the cat's isolated cerebral cortex in the unanaesthesized cat. J. Physiol. (Lond.), 1950, 111: 50-68. ECHLIN, F. A. and BA'rXlSTA,A. Epileptic seizures originating in chronic partially isolated cortex following peripheral nerve stimulation. Trans. Amer. neurol. Ass., 1961, 86:209-211.
ECHLIN, 17. A. and BATTISTA,A. Epileptiform seizures from chronic isolated cortex. Arch. Neurol. (Chic.), 1963, 2:154-170. FORSTER, F. M., PENEIELD, W., JASPER, H. and MADOW, L. Focal epilepsy, sensory precipitation and evoked potentials. Electroenceph. clin. Neurophysiol., 1949, 1 : 349-356. GASTAUT, H., BATINI, C., FRESSY, J., BROUGHTON, R. et TASSINARI,C. A. l~tude 61ectroenc6phalographique des ph6nom~nes 6pisodiques 6pileptiques au cours du sommeil. In: Le sommeil de nuit normal et pathologique, Masson, Paris, 1965: 239-254. GASTAUT, H. and TASSINARI,C. A. Triggering mechanisms in epilepsy. The electroclinical point of view. Epilepsia (Amst.), 1966, 7: 85-138. GOLDIE, L. and GREEN, J. M. A study of the psychological factors in a case of sensory reflex epilepsy (psychological factors in reflex epilepsy). Brain, 1959, 4: 505-524. GOWERS, W. R. Epilepsy and other chronic convulsive diseases. Their causes, symptoms and treatment. Churchill, London, 1881. GRAFSTEIN, B. and SASTRY, P. B. Some preliminary electrophysiological studies in chronic neuronally isolated cerebral cortex. Electroenceph. clin. Neurophysiol., 1957, 9: 723-725. HAGBARTH, K. E. Centrifugal mechanisms of sensory control. Ergebn. Biol., 1960, 22: 47-66. JACKSON,J. H. From "Selected writings o f John Hughlings Jackson". Basic Books, New York, 1958, Vol. 1. KAITOR, F. The influence of sleep and wakefulness in the epileptic activity of different cerebral structures. In Z. SERViT (Ed.), Reflex mechanisms in the genesis o f epilepsy. Elsevier, Amsterdam, 1963: 66-71. LAmv, G. C. D6clenchement r6flexe de l'activit6 convulsive. Electroenceph. clin. Neurophysiol., 1956, 8: 73-85. PAULSON, G. W. Inhibition of seizures. Dis. nerv. S.vst., 1963, 24: 657-664. PENFIELD, W. and ROBERTSON, J. S. M, Growth asymmetry due to lesion of the post-central cerebral cortex. Arch. Neurol. Psychiat. (Chic.), 1943, 50: 405430. SCOLLO-LAvlZZARL G. and HEss, R. Sensory precipitation of epileptic seizures. Fpilepsia (Amst.), 1967, 8: 157- 161. SXEVENS, J. R. Emotional activation of the electroencephalogram in patients with convulsive disorders. J. nerv. ment. Dis., 1959, 4: 339-351. SY~tONDS, C. Excitation and inhibition in epilepsy. Brain, 1959, 82: 133-146. SVMONDS,C. Some observations on the facilitation or arrest of epileptic seizures. In H. GARLAND (Ed.), Scientific aspects o f neurology. Livingstone, Edinburgh, 1961: 142-152. TUDOR, I., DANAILA, L. e PATRICHI-MACOVEI, M. Crize comitiale induse de miscare. Stud. Cercet. Neurol., 1966, I1: 127-138. TURINESE, A. Suite crisi epilettiche riflesse. Riv. Pat. herr. ment., 1956, 77: 788-814. V1ZIOLI, R. The problem of human epilepsy and the possible role of marked epileptogenic factors. Epilepsia ( A rest.), 1962, 3: 229-302. WARDJR., A. A. Epilepsy. b;t. Ret. Neurobiol.,1961,3:137.
Reference: TASSINARI,C. A. Suppression of focal spikes by somato-sensory stimuli. Electroenceph. clin. Neurophysiol., 1968, 25:574 578.
Electroencephalography and Clinical Neurophysiology Elsevier Publishing Company, Amsterdam - Printed in The Netherlands
SUPPRESSION OF FOCAL SPIKES BY SOMATO-SENSORY STIMULI C. A. TASSINARI, M . D . ~
lnstitut National de la Sant~ et de la Recherche Mddicale,
Marseille (l-¥ance)
(Accepted for publication: April 19, 1968)
I t is well known clinically that focal epileptic discharges may be suppressed by peripheral somato-sensory stimuli, such as rubbing, moving or compressing the segments initially involved by the seizure (Gowers 1881 ; Forster et al. 1949; Jackson 1958; Symonds 1959, 1961; Paulson 1963); E E G evidence of this type of inhibition is, however, scanty. The aim of this work is to describe E E G studies related to the nature of the lesion and the mechanisms responsible for the suppression of inter-ictal focal spike activity by specific somato-sensory stimuli with a strict somatotopic distribution. A study of the reactivity of the spikes and the distribution of the seizures during the different phases of sleep allows some comments on the factors facilitating nocturnal seizures. CASE REPORT The patient was an l l-year-old boy, with a right hemiparesis that followed a traumatic delivery with subarachnoid haemorrhage. From the age of 8 years onwards the patient had nocturnal attacks, described as a sudden and generalized muscular contraction, which recurred 2-4 times every week. Neurological examination showed a marked hemiatrophy of the right side of the body and face; there was slight spasticity and weakness with exaggerated tendon jerks and an extensor plantar response on the right side. Sensation was normal. A pneumoencephalogram was regarded as normal, as were other routine biological and radiographic examinations. METHOD The EEGs were recorded from bipolar and average reference montages. Surface electrodes were used to record the electrocardiogram, oculogram and the electromyograms of the deltoid, extensors and flexors of the wrist, quadriceps and gastrocnemius muscles, on both sides. Different types of stimulation were performed under polygraphic control, while the child was awake and during nocturnal spontaneous sleep. 1 Charg¢ de Recherche at INSERM, 300 Bvd. Ste. Marguerite, Marseille, France. Present address: University of Bologna, Italy.
RESU LTS Serial EEGs were taken from the age of 3 years, at intervals of 4-6 months. Between the ages of 3 and 5 years the records were characterized by intermittent, high voltage 1.5-3 c/sec waves over the frontal regions. In subsequent years the slow waves progressively decreased in persistence and amplitude and high voltage sharp waves appeared over the left fronto-central area. At the age of 8 years, when seizures first occurred, the records were characterized by frequent sharp waves intermixed with slow waves over the left fronto-parietal and over the midline regions. At times the sharp waves became rhythmic, at 2-4 c/sec, continuous and spread bilaterally over the anterior head regions. During subsequent years the slow waves disappeared and the sharp waves became of smaller amplitude, of shorter duration and restricted to the midline regions. At the time of our observation the E E G showed the following characteristics:
During wakefulness 1. The dominant rhythm over the occipital regions was at 10-11 c/sec, roughly symmetrical and blocked normally by visual attention. Bi- or triphasic spikes, with an amplitude of 100-150/~V, recurred rhythmically at 3-4 c/sec over the central and posterior midline regions. These were continual and were present in every record taken during a month in hospital. At times, spikes of smaller amplitude appeared over the left fronto-temporal area (Fig. l). 2. Reactivity of the spikes. (a) Effective stimuli: the continuous rhythmic spikes were suppressed by passive (Fig. 2,a) and voluntary (Fig. 2,b) movements of flexion or extension of the right foot; a similar effect was obtained by rubbing or stroking the sole of the right foot, such as during the Babinski manoeuvre (Fig. 2,e). Suppression of the spikes by such stimuli--which will be referred to as effective stimuli--was constant, reproducible at will, and persisted without habituation. The effective stimuli blocked the spikes regardless of anticipation. In all instances, the spikes reappeared immediately after the end of any form of stimulation. Contemplation of movement only did not suppress the spikes. (b) Ineffective stimuli: tactile stimuli and passive and voluntary movements involving regions other than the right foot did not modify the spike activity. Visual and acoustic stimuli, mental activity (calculation, reading) Electroenceph. elin. Neurophysiol., 1968, 25:574-578
SPIKE SUPPRESSION BY SENSORY STIMULI
MONOPOI.AR "AWAKE
575
BIPOLAR "AWAKE:
l: :
,_-,
Fig. 1 Subject awake. Left: common reference recording (eyes open); right: bipolar recording (eyes closed). Continuous inter-ictal spike activity over the central and posterior midline regions. Amplitude calibration: I00 #V. Q
EMG. R.LEG ~ -~...... -'<---~-~:i i,:v ~/
/,.; .......
b
c
Fig. 2 Subject awake. EMG. R. LEG: electromyogram of the right gastrocnemius recorded in a and b. The spikes are suppressed: by passive movements of the right foot (a); by plantar flexion (b) and by tactile stimuli to the sole of the right foot as in Babinski's manoeuvre (c, horizontal bars). and situations of emotional stress did not modify the spike activity. 3. Evoked potentials. During induced suppression of
spike activity, percussion of the right Achilles tendon or foot evoked high voltage potentials over the central midline region (Fig. 3). Evoked potentials were not observed
Electroenceph. clin. Neurophysiol., 1968, 25:574-578
576
¢. A. TASSINARI
E EG= I,oo~vlsec E M G : I ~oo~,v- -
51GNAL RIGHT LEG . . . . . ~ / ~ - - ~
" ~ - ~ - ~ r ~
Fig. 3 Subject awake. Potentials evoked in the midline region by percussion (R) of the right Achilles tendon. R I G H T LEG: E M G of the right gastrocnemius-soleus muscles. to follow percussion of regions other than the right foot or during acoustic stimulation, movements of the arms and of the left leg.
During sleep The frequency and morphology of the midline spikes were not significantly modified during all stages of sleep. - ~'~
v
%"a'~'~'% "~
1. The reactivity of the spikes. The stimuli effective during wakefulness also suppressed the spike activity during rapid eye movement (REM) stages of sleep, but were ineffective during stages 2, 3 and 4. Other forms of stimulation were ineffective during all phases of sleep. 2. The seizures. (a) Seven electro-clinical seizures were recorded during 6 h and 20 rain of spontaneous nocturnal sleep: four seizures during stage 2, two during stage 4 and one after a movement at the end of an R E M stage, which passed into stage 2. The seizures (Fig. 4), which did not waken the child, were characterized by a sudden flexion of the trunk and rotation of the head to the right; the arms elevated and abducted, the forearm being flexed at the elbow; the legs were hyperextended in adduction, with the feet rotated inwards. The E E G discharge was a synchronous paroxysm of rhythmic activity at 6-8 c/sec, which increased progressively in amplitude from 50 to 250-350 #V. The discharge, which was of greater amplitude on the left, involved all regions of the scalp except the central andposterior midline areas, where the spike activity persisted unchanged. (b) Nineteen subclinical paroxysmal discharges were recorded during stages 2, 3 and 4, fifteen of them during stage 2. From the EEG point of view the morphology and topography of the discharges were similar to those described previously, but they were less persistent (4-6 sec).
' ~ . ~ ' 5 " ~ ' ~ " ¢ ~ ' ~ ' ~ t 1 ' ~ ^ ~ , ~ ~'.'% . . . . ! '
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Fig. 4 Sleep, stage 2: Electro-clinical seizure. Electromyographic recordings from left deltoid (L.A.), right deltoid (R. A.) and right gastrocnemius (R. L.). The EEG paroxysm is generalized, but maximal over the anterior region. The spike activity continues unaltered throughout.
Electroenceph. clin~ Neurophysiol., 1968, 25 : 574-578
SPIKE SUPPRESSION BY SENSORY STIMULI DISCUSSION
1. Topography of the epileptogenic lesion A right hemiparesis with hemiatrophy indicates a lesion involving the left post-central cerebral cortex (Penfield and Robertson 1943). The topography of the spikes, and their suppression by sensory stimuli applied to the right foot, suggest that the lesion also involved the sensory projection area of the right foot. 2. Mechanisms o f suppression o.f the spike discharges The strict somatotopy and constant suppression of the spikes by the effective stimuli, without habituation, suggest that the desynchronization was mediated by the specific sensory projection system rather than by the diffuse reticulo-cortical system, since attentive, emotive factors or conditioning mechanisms, which may facilitate or suppress epileptic discharges (Lairy 1956; Goldie and Green 1959; Stevens 1959), had no such effects. Furthermore, the spikes were suppressed during wakefulness and during sleep, in R E M stages, without the awareness of the subject. 3. The spike "rhythm" as a result of a cortical lesion in the condition of partial deafferentation (isolated cortex) The spikes which appeared over the central and posterior midline regions may be considered as a "spike rhythm" characterized by its topography, continuity and periodicity, as well as by its specific reactivity to certain stimuli. This is a rare example of abnormal EEG activity, which can be defined by the same parameters as physiological rhythms. The reactivity of the physiological rhythms, however, is less specific and does not usually show as strict a somatotopy as the spikes recorded in this case. The electrical activity in chronic partially isolated somato-sensory cortex is characterized by: (a) the appearance of paroxysmal bursts of slow waves, which are progressively replaced by spike discharges (Grafstein and Sastry 1957; Echlin and Battista 1963); (b) by high voltage evoked potentials in response to local electrical stimulation or to afferent stimuli applied to peripheral nerves (Burns 1950; Echlin and Battista 1961); (c) by the occurrence of subclinical seizures, spontaneous or induced by repetitive stimulation of peripheral nerves (Echlin and Battista 1961). Similar features were also found in this case. The importance of the passage of time in determining the continuity and rhythmicity of the spikes is stressed since these patterns appeared 10 years after birth. The rhythmicity of the spikes could result from a progressive increase in the excitability of a partially isolated area, or from a change in the degree and quality of the afferent input "driving" the hyperexcitable neurones into rhythmic activity. It was found by Burns (1950) and by Echlin and Battista (1961 and 1963) that "the spontaneous" activity in the partially isolated cortex (somato-sensory area) was largely dependent on the afferent input to this area. That sensory afferents from the periphery could contribute to such triggering of the rhythmic spikes in our subject is suggested indirectly by the effectiveness of sensory stimulation of the right foot in modifying the focal epileptic activity, and by the high voltage potentials evoked in the central
577
midline region by synchronous afferent volleys evoked by percussing the right foot. Facilitation or suppression of focal epileptogenic activity, only and specifically by somato-sensory stimuli, is a rare event in human epilepsy (Vizioli 1962; Gastaut and Tassinari 1966). In the few reported cases (Forster et al. 1949; Turinese 1956; Tudor et al. 1966) it could be that the epileptogenic lesion in the somato-sensory area was in a state of partial deafferentation. If this hypothesis is correct, our observation indicates that an additional characteristic of the partially isolated sensory-motor cortex is suppression of the epileptic activity by an asynchronous sensory barrage, with a strict somatotopy.
4. The seizures The generalized tonic contractions did not suppress the spike activity but, since the seizures occurred during the slow wave stages of slcep, this could be the consequence of the same factors which rendered ineffective the tactile and proptioceptive stimuli applied to the right foot. Alternatively, during the seizures, mechanisms of occlusion may have been active at a subcortical level, or the epileptic discharge could have excited the cortical, cerebellar or reticular system whose stimulation could subsequently decrease the sensory afferent input at a spinal level (Hagbarth 1960). 5. Factors leading to seizures during sleep Since the somato-sensory afferents from the right foot suppressed the focal epileptic discharges, it is conceivable that the continuous sensory input resulting from daily activity (standing, walking, etc.) prevented the occurrence of diurnal seizures. This does not necessarily imply that the seizures which occurred during sleep did so merely because this is a state of rest with diminished somatosensory cortical inflow. The absence of seizures during the R E M stages of sleep is unlikely to be due to the shorter duration of these stages: 26 seizures occurred during 315 min of slow E E G sleep, while none occurred during 65 rain of R E M sleep. In an unselected population of epileptics, sleep does not facilitate but usually decreases the frequency of seizures (Gastaut et al. 1965). It may be that the slow stages of EEG sleep represent a state of further functional deafferentation, as compared to wakefulness I and to R E M sleep. This could result in the failure of sensory stimulation to suppress the spike activity. The slow stages would facilitate the seizures by reduction of somato-sensory input, having a suppressive effect on the epileptic discharges. Such factors could account for the frequent occurrence of nocturnal seizures in human subjects 1 It is known that even at rest there is a continuous sensory inflow from the periphery which participates in the control of the electrical activity of the somato-sensory areas. Decreased somato-sensorv input by posterior chordotomy facilitates the synchronization of the cortical activity in the corresponding regions of sensory projections (Anderson 1962), and may even produce frank epileptiform activity in the thalamic (VPL nuclei) and cortical (somatosensory) regions (Bava et al. 1966).
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(Turinese 1956; Kaitor 1963; Tudor et al. 1966; ScolloLavizzari and Hess 1967) and in monkeys (Ward 1961), with a focal lesion in the somato-sensory region whose seizures are otherwise precipitated by somato-sensory stimuli. SUMMARY The EEG findings in a child with a right hemiparesis and hemiatrophy associated with nocturnal seizures are described. Rhythmic inter-ictal spike activity was present continuously over the central and post-central midline regions, and this could be selectively suppressed by tactile stimulation and voluntary or passive movements of the right foot. This effect was present during wakefulness and rapid eye movement sleep, but was abolished during the slow stage of sleep, during which all seizures occurred. These findings are discussed in the light of physiological studies on the experimental isolated cortex. It is concluded that the post-Rolandic lesion in this patient led to partial deafferentation, which was enhanced during the slow stage of sleep, thereby leading to clinical and subclinical seizures. RI~SUMI~ SUPPRESSION DE POINTES FOCALES PAR DES STIMULATIONS SOMATO-SENSORIELLES L'auteur presente l'6tude EEG d'un garqon avec h6mipar6sie et h6miatrophie droite, associ6es ~t des crises 6pileptiques nocturnes. Les trac6s se caract6risent par une activit6 de pointes, rythmiques et continues, localis6e dans la r6gion du vertex moyen et post6rieur, 61ectivement supprim6e par des stimulations tactiles et des mouvements passifs ou volontaires du pied droit. Cet effet peut 6tre observ6 pendant la veille et pendant la phase des mouvements oculaires du sommeil; par contre, au cours du sommeil lent, pendant lequel surviennent les crises 6pileptiques, les stimulations du pied droit ne parviennent plus fi bloquer les pointes. Ces donn6es sont discut6es ~ la lumi~re des 6tudes physiologiques sur le cortex isol6. L'auteur conclue que chez ce malade il y avait une 16sion post-Rolandique en 6tat de d6aff6rentation partielle; le sommeil lent augmenterait cet 6tat de d6aff6rentation, favorisant ainsi l'apparition de crises 6pileptiques cliniques et infra-cliniques. REFERENCES ANDERSON, S. A. Localised slow wave activity in the somato-sensory cortex. Med. exp. (Basel), 1962, 6: 21-24. BAVA, A., FADIGA, E. e MANZONI, T. Risposte convulsive in strutture sottocorticali di relais somatico e nella corteccia di preparati cronici parzialmente deafferentati. Boll. Soc. ital. Biol. sper., 1966, 42: 1-3. BURNS, B. D. Some properties of the cat's isolated cerebral cortex in the unanaesthesized cat. J. Physiol. (Lond.), 1950, 111: 50-68. ECHLIN, F. A. and BA'rXlSTA,A. Epileptic seizures originating in chronic partially isolated cortex following peripheral nerve stimulation. Trans. Amer. neurol. Ass., 1961, 86:209-211.
ECHLIN, 17. A. and BATTISTA,A. Epileptiform seizures from chronic isolated cortex. Arch. Neurol. (Chic.), 1963, 2:154-170. FORSTER, F. M., PENEIELD, W., JASPER, H. and MADOW, L. Focal epilepsy, sensory precipitation and evoked potentials. Electroenceph. clin. Neurophysiol., 1949, 1 : 349-356. GASTAUT, H., BATINI, C., FRESSY, J., BROUGHTON, R. et TASSINARI,C. A. l~tude 61ectroenc6phalographique des ph6nom~nes 6pisodiques 6pileptiques au cours du sommeil. In: Le sommeil de nuit normal et pathologique, Masson, Paris, 1965: 239-254. GASTAUT, H. and TASSINARI,C. A. Triggering mechanisms in epilepsy. The electroclinical point of view. Epilepsia (Amst.), 1966, 7: 85-138. GOLDIE, L. and GREEN, J. M. A study of the psychological factors in a case of sensory reflex epilepsy (psychological factors in reflex epilepsy). Brain, 1959, 4: 505-524. GOWERS, W. R. Epilepsy and other chronic convulsive diseases. Their causes, symptoms and treatment. Churchill, London, 1881. GRAFSTEIN, B. and SASTRY, P. B. Some preliminary electrophysiological studies in chronic neuronally isolated cerebral cortex. Electroenceph. clin. Neurophysiol., 1957, 9: 723-725. HAGBARTH, K. E. Centrifugal mechanisms of sensory control. Ergebn. Biol., 1960, 22: 47-66. JACKSON,J. H. From "Selected writings o f John Hughlings Jackson". Basic Books, New York, 1958, Vol. 1. KAITOR, F. The influence of sleep and wakefulness in the epileptic activity of different cerebral structures. In Z. SERViT (Ed.), Reflex mechanisms in the genesis o f epilepsy. Elsevier, Amsterdam, 1963: 66-71. LAmv, G. C. D6clenchement r6flexe de l'activit6 convulsive. Electroenceph. clin. Neurophysiol., 1956, 8: 73-85. PAULSON, G. W. Inhibition of seizures. Dis. nerv. S.vst., 1963, 24: 657-664. PENFIELD, W. and ROBERTSON, J. S. M, Growth asymmetry due to lesion of the post-central cerebral cortex. Arch. Neurol. Psychiat. (Chic.), 1943, 50: 405430. SCOLLO-LAvlZZARL G. and HEss, R. Sensory precipitation of epileptic seizures. Fpilepsia (Amst.), 1967, 8: 157- 161. SXEVENS, J. R. Emotional activation of the electroencephalogram in patients with convulsive disorders. J. nerv. ment. Dis., 1959, 4: 339-351. SY~tONDS, C. Excitation and inhibition in epilepsy. Brain, 1959, 82: 133-146. SVMONDS,C. Some observations on the facilitation or arrest of epileptic seizures. In H. GARLAND (Ed.), Scientific aspects o f neurology. Livingstone, Edinburgh, 1961: 142-152. TUDOR, I., DANAILA, L. e PATRICHI-MACOVEI, M. Crize comitiale induse de miscare. Stud. Cercet. Neurol., 1966, I1: 127-138. TURINESE, A. Suite crisi epilettiche riflesse. Riv. Pat. herr. ment., 1956, 77: 788-814. V1ZIOLI, R. The problem of human epilepsy and the possible role of marked epileptogenic factors. Epilepsia ( A rest.), 1962, 3: 229-302. WARDJR., A. A. Epilepsy. b;t. Ret. Neurobiol.,1961,3:137.
Reference: TASSINARI,C. A. Suppression of focal spikes by somato-sensory stimuli. Electroenceph. clin. Neurophysiol., 1968, 25:574 578.