Parietal focal spikes evoked by tactile somatotopic stimulation

312

Electroencephalography and Clinical Neurophysiology, 1977, 43:312--316

© Elsevier/North-Holland Scientific Publishers, Ltd.

P A R I E T A L F O C A L S P I K E S E V O K E D BY T A C T I L E S O M A T O T O P I C S T I M U L A T I O N IN SIXTY NON-EPILEPTIC CHILDREN: THE NOCTURNAL SLEEP AND CLINICAL AND EEG EVOLUTION P. NEGRIN and P. DE MARCO Clinica delle Malattie Nervose e Mentali dell Universitd di Padova, Padova and Ospedale Civile di Trento, Reparto di Nearopsichiatria Infantile, Trento (Italy)

(Accepted for publication: January 18, 1977)

In M a r c h 1 9 7 0 , while r e c o r d i n g t h e E E G o f a child w h o h a d b e h a v i o u r a l d i s t u r b a n c e s , we o b s e r v e d t h a t tactile s t i m u l a t i o n o f t h e f o o t determined the appearance of contralateral parietal spikes (De M a r c o 1 9 7 1 ; De M a r c o a n d Negrin 1 9 7 3 ) . S o m e t i m e s e a c h spike was foll o w e d b y a slow wave (Fig. 1). A f t e r this o b s e r v a t i o n , in o r d e r to e x p l o r e t h e i n c i d e n c e of this p h e n o m e n o n , we l o o k e d f o r it s y s t e m atically in all y o u n g subjects w h o s e E E G s w e r e r e c o r d e d in o u r I n s t i t u t e . I t s e e m e d v e r y i n t e r e s t i n g t o us t o f o l l o w t h e s e subjects a n d t o get an E E G r e c o r d o f

FpO - FsO

t h e i r n o c t u r n a l sleep. T h e p o i n t was w h e t h e r the appearance of 'parietal spikes' following tactile s t i m u l a t i o n was a t r a n s i e n t p h e n o m e n o n in the c o u r s e o f brain m a t u r a t i o n or an early sign o f a n o t - y e t - e v i d e n t f o c u s o f spikes.

Methods D u r i n g t h e last 4.5 y e a r s we h a v e t e s t e d , at the C h i l d r e n ' s N e u r o p s y c h i a t r i c Division o f T r e n t o H o s p i t a l , a b o u t 8 0 0 0 s u b j e c t s , ranging in age f r o m 2 m o n t h s t o 15 years. Tactile

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Fig. 1. Tactile stimulation of the right foot (left part of the picture), and of the left foot (right part). Fp, Frontopolar; Fs, Superior frontal; R, Central; P, Parietal; O, Occipital; Ta, Anterior temporal; Tin, mid-temporal; D, right; L, left. Tactile stimuli indicated by artefacts.

F O C A L SPIKES E V O K E D BY T A C T I L E S T I M U L A T I O N

stimulation was performed manually with a reflex h a m m e r during a standard EEG, before activation with hyperpnoea and photic stimulation. The electrode placements were those of the 10/20 system (for further technical details see De Marco and Negrin 1973). This specific area was limited to the contralateral f o o t (mainly to the external border of the heel), and stimulation of other parts of the body did n o t generally evoke such a phenomenon. The strength of the h a m m e r stroke was the same as t h a t for eliciting tendon reflexes. In 'positive' cases (60) the EEG was repeated about every 6 months. Meanwhile, no specific therapy was given to the children who presented this p h e n o m e n o n . T w e n t y epileptic subjects who presented this evoked response were n o t included in this investigation; 15 of them had an epileptic focus, while 5 others suffered from a primary generalized epilepsy with tonico-clonic seizures.

313

lastic proficiency. The EEGs were normal, photic stimulation was negative. In 32 cases the specific zone of the f o o t was bilateral but the evoked spikes always predominated on the side opposite to t h a t stimulated. The startle factor did n o t play any role, and the stimulus, either expected or not, always evoked the same spike pattern. In 9 cases we determined oscilloscopically the peak latency of the evoked response: it was fairly constant, varying between 45 and 55 msec (Fig. 2).

Nocturnal sleep In 12 cases a nocturnal sleep EEG was recorded to investigate the evoked phenomenon in these conditions. In these cases, stimulation performed in the above way caused no modification of the sleep level. During slow sleep the evoked spikes underwent contralateral increase of amplitude and

Results

In 60 cases tactile stimulation of the f o o t (or more rarely, other parts of the body) evoked focal spikes in the contralateral parietal region; none of these y o u n g subjects had ever presented epileptic seizures; however, 17 of them had previously had febrile convulsions.

Clinical features The ages of the tested children ranged between 3 and 10 years; the observed sensory evoked responses had their highest occurrence rate and largest amplitude between the age of 4 and 8 years; b e y o n d this age we noted a progressive decrease of these potentials. The neurological examinations were negative and p s y c h o m o t o r development was also altogether normal. EEG Generally the first EEG was performed for mild behavioural disturbances or poor scho-

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/ \, Fig. 2. Oscilloscopic records of the evoked responses. All potentials were taken f r o m the same patient, and their peak latency is c o n s t a n t at 50 msec. Each bar equals 10 msec. A r r o w indicates the stimulus triggering the scope sweep.

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P. NEGRIN, P. DE MARCO

diffusion; the cutaneous involved area also increased in extent, to include the knee and hip (where stimulation was completely ineffective during the waking state). In 10 cases the record during slow sleep displayed 'spontaneous' focal spikes (i.e. in the absence of any stimulation); these were mostly parietal, always localized to the hemisphere on which the evoked spikes predominated or manifested themselves; 4 of this group of cases had previously suffered from febrile convulsions (Figs. 3 and 4). The reverse occurred during REM sleep: the evoked spikes diminished greatly in amplitude and diffusion, finally to appear clearly focal in the parietal region. The cutaneous involved area was also restricted to the foot, and it was n o t possible to observe 'spontaneous' spikes (Fig. 5). In other words, the

EEG during REM sleep was similar to that of the waking condition, regarding both the evoked p h e n o m e n o n and 'spontaneous' focal spikes. E vo lu t i o n

In 20 of the 60 cases studied a spontaneous focal spike appeared in the waking condition, after a variable delay from 9 months up to 4 years and in some cases the focus displayed discharges of spikes and waves in the following EEGs. These focal spontaneous spikes were always localized to the hemisphere where they had been predominant during stimulation and were parietal or central. In 8 of these 20 cases, night sleep EEGs showed a focus of spikes during slow sleep, 4 to 12 months before its appearance during the waking state. In at least 5 of the 20 cases

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Fig. 3. Slow sleep record. Notice evoked and spontaneous parieto-occipital spikes. Va, anterior vertex; Vm, midvertex.

FOCAL SPIKES EVOKED BY TACTILE STIMULATION

315

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Fig. 4. Deep stage of slow sleep. Notice spontaneous left parieto-occipital focus of spikes in addition to the evoked response.

which presented a spontaneous focus of spikes during waking, one or more tonicclonic seizures occurred which were generalized or hemi-generalized; they followed the appearance of the first evoked parietal spikes after 4 years.

Discussion Despite the increased number of available cases since our previous paper on this topic {De Marco and Negrin 1973), we are n o t able to propose a valid hypothesis regarding the genesis of the described p h e n o m e n o n . The absence of cerebral lesions, demonstrated neurologically and through the EEG, allows us to reject the hypothesis of a partial deafferentation of the somatosensory area,

which could be responsible for a focal facilitation (Echlin and Battista 1961; Tassinari 1968); this hypothesis might also be contradicted by the fact t h a t in several of our subjects the spikes could be evoked by bilateral stimulation of the foot. As already mentioned, the startle effect does n o t play any role in these subjects, as it did in the case of Alajouanine and Gastaut (1955), in which tactile stimulation evoked a cortical response only if it was n o t expected. The reason for the large amplitude of this evoked response and the way by which the stimulus travels are still u n k n o w n . However the evolution of these cases may give the key for a valid interpretation. At present, we think t h a t at least some of our subjects show this p h e n o m e n o n as a result of a particular cortical excitability preceeding the appear-

316 ance of a focus of spikes. The electro-clinical evolution o f these particular subjects suggests the hypothesis th at there could be a sequence of 4 stages in the following years: (1) evoked parietal spikes in a normal EEG; (2) appearance of a s p o n tan eous focus o f spikes during sleep; (3) appearance o f a s pont a ne ous focus of spikes during waking and (4) clinical phase, is represented by generalized or hemigeneralized tonic-clonic seizures.

Summary Tactile stimulation o f the f o o t evoked contralateral parietal spikes in the EEG of young, non-epileptic, subjects. After this initial finding, the authors systematically tested a b o u t 8000 patients, aged f r om 2 m o n t h s to 15 years. The p h e n o m e n o n was evoked in 80 cases, of which 60 had never presented epileptic seizures. Slow sleep markedly facilitated this phen o m e n o n ; on the c o n t r a r y paradoxical sleep reduced it. In 20 o f t he 60 nonepileptic subjects a s p o n tan eo u s focus o f spikes appeared after a variable delay; in some o f these cases tonic-clonic seizures developped in the following years.

R6sum6

Pointes focales pari$tales ~voqu~es par la stimulation tactile somatotopique contralat~rale chez 60 sujets non-dpileptiques: sommeil nocturne et l'dvolution clinique et EEGraphique. Apr~s avoir observ~ que la stimulation tactile du pied ~voquait 'coup p o u r c o u p ' des

P. NEGRIN, P. DE MARCO pointes pari~tales contralat~rales sur I'EEG de quelques jeurnes sujets les auteurs ont recherch~ de fa~on syst~matique ce curieux ph~nom~ne ~voqu~ sur environ 8000 sujets, d o n t l'~ge variait de 2 mois ~ 15 ans. Le ph~nom~ne ~voqu~ fut present dans 80 cas, d o n t 60 n'avaient jamais pr~sent~ de ('.rises ~pileptiques. Le sommeil lent a facilit~ le ph~nom~ne d'une fa~on remarquable, tandis que le sommeil rapide l'a r6duit. Dans 20 des 60 sujets non-~pileptiques un f o y e r irritatif spontan~ est apparu apr~s un d~lai variable; dans quelques cas des crises tonico-cloniques se sont d6velopp6s dans les ann~es suivantes.

References Alajouanine, TH. et Gastaut, H. La syncin~siesursaut et l'dpilepsie-sursaut ~ d~clenchment sensoriel ou sensitif inopinC Les faits anatomocliniques (15 observations). Rev. neurol., 1955, 93: 29--41. De Marco, P. Su un particolare aspetto dei potenziali evocati mediante stimoli sensitivi. Nota preliminare. Riv. Neurobiol., 1971, 17: 177--183. De Marco, P. and Negrin, P. Parietal focal spikes evoked by contralateral tactile somatotopic stimulation in four non-epileptic subjects. Electroenceph, clin. Neurophysiol., 1973, 34,308--312. Echlin, F.A. and Battista, A. Epileptic seizures originating in chronic partially isolated cortex following peripheral nerve stimulation. Trans. Amer. neurol. Ass., 1961, 86: 209--211. Tassinari, C.A. Suppression of focal spikes by somatosensory stimuli. Electroenceph. clin. Neurophysiol., 1968, 25: 574--578.