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Speech Findings in Epilepsy and Electro-Cortical Stimulation: An Overview
SPEECH FINDINGS IN EPILEPSY AND ELECTRO-CORTICAL STIMULATION: AN OVERVIEW· E. A. Serafetinides2 (Guy's Maudsley Neurosurgical Unit, Maudsley Hospital, London)
This review will inevitably start with definitions. These are pever satisfying but serve at least the purpose of delineating the areas of our ignorance. The next step will be to tackle speech symptoms as part of epileptic symptomatology and to see if any useful differentiation can be made among such symptoms - especially in relation to the type of epilepsy and localization of the discharges associated with them. Lastly cortical stimulation observations will be brought in and compared with the clinical data. Since jackson's original report in 1898 it has been accepted that ictal aphasia often occurs in focal epileptic seizures originating in the dominant cerebral hemisphere. In addition speech automatisms have also been described as occurring during epileptic seizures. But what do we mean by ictal aphasia or speech automatisms? Most authors prefer to use these terms without precise definition thus suggesting universal agreement on their significance. This, to a certain extent and within certain time and space limits, may be so, but makes communication and research extremely difficult. Others prefer to paraphrase or use as operational a clinical definition as possible, but even in operational definitions of this kind, unless the terms of reference are themselves sub-defined, as it were, and kept constant, the tacit assumption of universal argreement, characterizing the non-definition school, is still present. In an already published paper (Serafetinides and Falconer, 1963) the following definitions were given: • Based on an invited talk given at the 1965 annual meeting of the Academy of Aphasia (U.S.A.). 2 Now at the University of Oklahoma Medical Center.
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A. Paroxysmal Dysphasia is an inability on the part of the patient to express himself by the correct words while he is still conscious and without obvious impairment of articulation or of hearing. The patient mayor may not comprehend fully what is said to him, but his replies are such as to rule out confusion with disorientation or mere speech arrest. On recovery from an attack the patient remembers that during the period of dysphasia he was conscious, but that as he could not find the correct words to express himself, he either stopped talking or verbalized incorrectly. Two main types of paroxysmal dysphasia were recognized by us, viz. (a) expressive, and (b) combined receptive and expressive. Either could occur as an aura at the start of a seizure with or without subsequent loss of consciousness, or if consciousness was lost, immediately on recovery when dysphasia had to be distinguished from confusion. Sometimes an isolated episode of dysphasia may be the only clinical manifestation of a seizure. As paroxysmal dysphasia is as a rule brief, its appreciation and study are usually confined to the auditory and verbal aspects of speech. A cardinal feature of paroxysmal dysphasia as we have defined it, is that it occurs during a period of awareness and is subsequently recalled by the patient. B. Speech automatisms are utterances of identifiable words or phrases at the beginning, during, or just after a clinical attack, which are lin. guistically correct, but for which the patient is subsequently amnesic. I have already mentioned Jackson'S report - one of the earliest, if not the earliest - on ictal aphasia. Gowers (1893), whose astuteness as a clinical observer was no less legendary, is also credited with an early similar report. He made the very crucial observation that ictal aphasia is particularly associated with motor attacks commencing in the right upper limb or in part of the face. Later clinicians noted its not infrequent association with right-sided post-epileptic hemiplegia, which they interpreted as an additional manifestation of post-epileptic paralysis or exhaustion of the brain or as some others, more up-to-date, would put it, of the ensuing inhibition. Some, like Marchand and Ajuriaguerra (1948), comment on the differential incidence of ictal aphasia according to the type of epilepsy, i. e., it is frequent in partial or focal or minor attacks, but much less so in grand mal episodes. They also try to distinguish between dysarthria - following, not infrequently, generalized attacks and without localizing significance - and aphasia with its much more specific characteristics. The brief duration, usually minutes unless complicated by cerebrovascular episodes - the predominantly motor or expressive nature and the occasional concurrence of related symptoms, such as dysgraphia, in the chance instances when such
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observations could be made, all these and similar experiences of ictal aphasia have been encountered by clinicians habitually studying and caring for epileptic patients. Penfield and Jasper (1954) summarized as follows their experience with speech disturbances in epileptics. Epileptic aphasia occurs as the result of discharge in the dominant hemisphere only ... Unless (the patient) is occupied with words in some way, he is not aware that he is having such an attack ... Epileptic discharge produces activation and interference ... but the effect upon speech is only interference... Epileptic discharge in a cortical speech area undoubtedly activates the ganglion celles but it does not cause the patient to speak or to think of particular words. It produces aphasic arrest of speaking. Aphasic arrest is different from arrest of speaking due to discharge in a portion of the motor cortex that is devoted to movement of the mouth, or respiration or vocalization. Epileptic interference in such areas stops speaking by a motor block. The patient still undestands, and he knows what words he would like to use as soon as he has the mechanism of vocalization and of tongue movement and lip movement again at his disposal.
One appreciates the attempt on the part of Penfield and Jasper to tackle this thorny problem, namely what does constitute an aphasic arrest and what does not. In addition, however, to the fact that such attempts are bound to be either negative or speculative, considering the limited data available, another question arises, and this is whether it is permissible to introduce at this stage the theoretical problems of non-ictal aphasia. It would seem more appropriate to me to talk about ictal speech disturbances in general. If further differentiation is required, or is deemed to be desirable, then purely descriptive terms should be used, terms which would have the greatest relevance to the actual observed phenomena, and little reference to etiological or other preconceptions carried over from the study of non-ictal aphasia. If so little agreement exists as to what really constitutes the latter - and this despite the unlimited time for observation and study that non-ictal aphasia provides - is it not wishful thinking to try to answer fundamental questions on the basis of the usually fleeting and transient ictal speech disturbances, a very small portion of which are ever witnessed by a doctor? Nevertheless, to leave the theoretical implications of this rhetorical question unanswered, the practical implications of such symptoms are unquestionable. To quote Penfield and Jasper once more:
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The presence or absence of aphasia following an attack may ... answer the questions of the hemisphere harboring the focus, which may be of use in temporal lobe seizures, for it frequently happens that the pattern (of such seizures) points to the temporal cortex or to the deep sylvian region and yet gives no obvious clue as to the laterality. Penfield later assembled and published in association with Roberts his epileptic speech material (1959). 273 patients undergoing surgery on the dominant or major side were reviewed and compared with an equal number of patients with an operation on the minor side. Additionally detailed speech examinations were carried out on 72 of the patients. The authors first distinguished between positive and negative disturbances of speech associated with seizures. As positive disturbances or "effects" they considered the instances of vocalization, usually a cry, occurring with an ictus. They ascribed these to discharges originating in the Rolandic or supplementary motor areas of either hemisphere or in subcortical regions. As negative effects they described a number of symptoms. First, they described instances of inability to understand. They considered such instances as due either to discharges originating in the dominant hemisphere and affecting the speech mechanisms or to discharges affecting the primary auditory mechanisms within either hemisphere or subcortically. Disturbances in reading were described as another possibility if the discharges originated in the dominant hemisphere for speech or affected the primary visual areas or affected certain subcortical regions. A third possibility - or negative effect - is inability to speak. In the case of misnaming objects or perseveration or similar known aphasic symptoms, the discharges are located in the speech areas of the dominant hemisphere, whereas if the symptoms are simply silence or dysarthria then the additional or alternative possibility of discharges in the Rolandic or supplementary motor areas of either hemisphere arises. Lastly the authors mention the possibility of dysgraphia, if discharges affect the appropriate speech areas of the major hemisphere. In discussing such symptoms, Penfield and Roberts point out that these can occur either as an aura or during the seizure itself or postictally. A note of caution is also issued. For example, the authors say, if aphasia is the initial symptom of a seizure an EEG determination of the exact locus of the discharges in the dominant hemisphere is still imperative, considering the fact that if the focus or foci are in the anterior temporal or superior
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parietal area, then surgery can be performed whereas if the focus is in the speech area itself, then, of course, surgery is out of the question. It seems, thus, that there is general agreement that paroxysmal dysphasia can occur with epilepsy arising in the dominant cerebral hemisphere although few have associated it with anterior temporal lobe epilepsy. Among the various relatively recent reports on the subject one should start with that of Hecaen and Piercy (1956). They selected 126 patients fulfilling certain criteria of lateralization out of 3000 epileptics. Half of the right-handed patients with left-sided foci showed paroxysmal dysphasia (31 cases out of 63). Of the 34 patients with right-sided foci 4 showed dysphasia. In left-handed patients 17 out of 18 with left hemisphere foci ond 9 out of 11 with right hemisphere foci showed ictal aphasia. Bingley (1958) also studied speech symptoms in patients with epilepsy due to lesions in the temporal lobe. Of the 33 patients with a dominant temporal lobe lesion and epilepsy, 16 had ictal dysphasia, whereas none of the 24 patients with a lesion in the non-dominant temporal lobe had this disturbance. Alajouanine and Sabouraud (1960) also reported similar findings. Russell and Espir (1961) reviewing a different series of patients, namely patients with penetrating war wounds of the brain, found that 280 cases out of a total of 916 showed aphasic symptoms as a result of such wounds. Of these 280 cases no less than 60% also had epileptic seizures. Furthermore - and this is most relevant to the present review - 64 patients reportedly had aphasic auras. They were tabulated as follows, according to handedness and site of lesion: Left Right-handers ft h d Le-aners
~ Aphas~c
aura group Aphasic aura T otal'10 group
~ Total
~
10
. . . .
52
343 6
28
Right 3
276
3
30
The authors although admitting lack of detailed analysis of these cases go on to say that their provisional findings give some support to the view put forward by Hecaen and Piercy (1956) according to which there is a higher tendency for aphasic auras to occur in left-handers even when the lesion is left-sided.
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Instances of ictal aphasia occurring during recording of an EEG thus permitting localization of the focus are very rare with ordinary recordings, i. e. outside the stimulation studies performed during operation. An interesting example was published by Boudouresques, Roger and Gastaut (1962). The patient was a 29 year old man who at the age of 7 developed a left mastoiditis, with high fever, which was complicated by right hemiconvulsive fits plus right hemiplegia and impaired speech, all of which cleared in the course of the subsequent few weeks. The fits reappeared four years later and the patient eventually underwent a left superficial temporal gyrectomy which failed, however, to control his seizure. The patient in addiction now had minor fits in which the main feature was speech arrest of a few seconds duration without loss of consciousness. The resting EEG showed infrequent left middle and anterior temporal slow waves. Metrazol activation produced a grand mal attack in one instance and localized left temporal electrical discharges only in another. However, the authors had the opportunity to perform EEG and psychological studies during a series of spontaneously occuring seizures. They found that the discharges first appeared in the left posterior and middle temporal lobe. They lasted for a minute and would reappear every 2-3 minutes. Altogether the authors recorded a few hundred such sequences throughout the two day period of observation of these spontaneous seizures. During these attacks the patient would appear conscious and could respond correctly. On testing, however, he would commit mistakes in counting and would finally stop counting altogether. He would also misname objects and was unable to speak or write. On the other hand he could identify colors, calculate in some instances, distinguish between right and left, and could understand and carry out commands. The authors concluded that cases with similar episodes may be much more frequent than is ordinarily appreciated, their lack of recognition being presumably due to the general lack of comparable opportunities and facilities, such as the ones the authors were fortunate to have at their disposal. In their study the focus was found, as expected, in the left side, i. e., the dominant hemisphere. However, things do not always happen as expected. Mendilaharsu et al. ( 1964) recently published a report on aphasic episodes provoked, or rather induced, in four patients by the same method as was used by the abovementioned French workers, i. e., 1. V. Metrazol. To summarize their
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findings: they found evidence suggesting that the clinical appearance of ictal aphasia coincides with the generalization of the abnormal EEG findings. They interpreted this as the effect of subcortical rather than cortical involvement, and by inference, ascribed to these subcortical changes the responsibility for the clinical phenomena observed. No strict comparison is however permissible between the results of this metrazol activation study and of the studies of spontaneous seizures as they are in so many ways the endproducts of dissimilar processes. Thus in the French study, Metrazol produced in its two applications on the same subject two different pictures - and neither of these were similar to his habitual seizures. The involvement of the supplementary motor area of the major hemisphere in paroxysmal speech disturbance has been emphasized by Arseni and Botez (1961) of Bucharest. These authors reported twelve cases with tumors, mainly meningiomas, in that area. Paroxysm. al speech symptoms alone appeared in three cases. In three other cases they were seen together with minor focal or major attacks. The speech disturbances consisted either of speech arrest or of involuntary repetition of words, onomatopoeic sounds, distorted words, and neologisms. It is quite possible that some of these symptoms could be termed ictal speech automatisms - although the majority of them were most likely aphasic. Finally a study (Serafetinides and Falconer, 1963) was made of the pre-operative seizure patterns in 100 cases of temporal lobe epilepsy submitted to an anterior temporal lobectomy and subsequently followed up for periods from two to ten years. Speech disturbances were observed in connexion with the seizures in 67 patients. These disturbances were of a dysphasic type in 34 patients and of a speech automatism type (e. g. warning, recurrent, irrelevant, emotional, and/or perplexity utterances) in 38. Ictal aphasia occurred either at the beginning of the ictus or immediately afterwards and was subsequently remembered, whereas ictal speech automatisms always occurred during a period for which the patient was subsequently amnesic. In four patients both types of symptoms were present but occurred independently. Ictal automatisms have been studied less than ictal aphasia. Bingley (1958) found the latter in 29 out of 74 cases of temporal lobe epilepsy. It was present in 25 per cent of cases with aunilateral
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EEG focus in the dominant lobe, and in 59 per cent of the cases with a unilateral focus in the non-dominant lobe. This difference is significant at the 0.01 level. Only 4 patients in this series had both paroxysmal dysphasia and speech automatism. Bingley therefore felt that the two features occurred independently. Hecaen and Angelergues (1960) reported similar findings. Driver, Falconer and Serafetinides (1964) reported the following case of speech automatisms. The patient, a Pole aged 38, was moved to Siberia at the age of 16 years, and became fluent in Russian as well as his mother tongue. At the age of 22 he went to England and started learning English in which he became proficient. His seizures started when he was 25 years old, and were of psycho-motor type with epigastric, cephalic, and occasionally olfactory auras. Witnesses described that at the onset of each attack he would say repeatedly in English "I beg your pardon, I beg your pardon ... " while his eyes would stare and he would make chewing movements, followed later by abduction of the left arm. An EEG focus had been noted consistently in the right sphenoidal area during resting recordings as well as during Metrazol activated recordings with reproduction of the automatisms. Similar observations were made on electrocortical stimulation in the course of a right temporal lobectomy which had a favorable effect on the seizures. In discussing this case the authors felt that if speech automatisms were a direct product of epileptic discharges arising in the minor hemisphere, they could be regarded as ictal analogues of the compulsive or emotional speech occurring in dysphasic patients with dominant hemisphere lesions and attributed by Jackson to function of the minor hemisphere. However, this hypothesis was not considered satisfactory as a general explanation since speech automatisms could occur in association with epileptogenic lesions of either hemisphere. An alternative explanation was then considered, namely that the ictal discharges in the minor hemisphere (or in some patients in an appropriate part of the major hemisphere) lead to an upsetting of reciprocal excitation-inhibition relationships. This, it was postulated, removes the normal control of the speech mechanisms which then embark on an automatic or stereotyped activity. The clinical and electrographic events observed during the electrically induced seizure at operation in this published case were thought to be compatible
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with such an hypothesis. During that period the ictal discharge activity was confined to a limited area of the right temporal lobe including the amygdala. The remaining areas in the right hemisphere (and by inference the left hemisphere also) showed a pattern compatible with normal functioning. With the generalization of the abnormal activity, the speech automatism ceased. We have so far examined data of clinical origin. The electrical stimulation data to which we will now turn are, as expected, much fewer, but nonetheless crucial. Jefferson as far back as 1935 reported speech arrest in patients whose angular gyrus was stimulated by electric current. Foerster (1936) produced, a year later, grunts and groans by stimulating the lower rolandic region. Our main body of evidence, however, on speech and cortical stimulation derives from Penfield's extensive work. The main conclusion of Penfield's work in relation to our subject is that aphasic arrest may be produced by electrical stimulation just as it is by epileptic discharge.
Altogether 114 patients were studied by this method during operation (Penfield and Roberts, 1959). Of these, in 94 cases the operation was on the left side and in 20 on the right. Excluding unsuitable cases, 5 out of 65 right-handed patients had post-operative aphasia - a usual but transient complication of cerebral resections involving the major temporal lobe and adjacent areas. All 54 patients had electrical stimulations of their exposed cortex while they were conscious and could thus collaborate with the surgeon in speech testing, before resection, by counting, reciting or naming objects. In all instances speech was affected, the usual end-result being speech arrest or misnaming of common objects. The areas which when stimulated produced these results were: Broca's area, the inferior parietal area and the posterior temporal area - all on the left or major side. Negative results were not accepted immediately as evidence that the areas in question were not related to speech, unless the same voltage had produced positive results in a neighboring area. Penfield is categorical as to the meaning of this positive response. To quote: When stimulation produces aphasic arrest it is clear that the hemisphere exposed is dominant for speech, for we have never been able to produce such an effect from the non-dominant hemisphere.
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It seems that there are only three areas in the dominant hemisphere from which arrest or distortion of speech can be consistently obtained. These three areas are: 1) the posterior temporoparietal region occupying the posterior parts of the three lateral temporal gyri, the supra-marginal gyrus, and the angular gyrus; 2) Broca's area in front of the lower pre-ventral gyrus; and 3) the supplementary motor area lying in the medial aspect of the hemisphere just in front of the pre-central leg area. The electric current when applied to these areas produces a negative effect upon speech, which the authors named "interference," and which is akin to dysphasia. When, however, it is applied to the motor areas (Rolandic and supplementary) of either hemisphere it can produce a positive effect - "stimulation" which leads to vocalization. SUMMARY AND CoNCLUSION
The evidence presented so far, both clinical and experimental, can be looked at from two different viewpoints. From the point of view of epilepsy the implications are mainly of practical but also of theoretical interest. In those cases where neurosurgery is contemplated, or localization of the discharges is considered to be desirable, the presence of ictal aphasia, indicating involvement of the dominant hemisphere, and speech automatism indicating involvement of either hemisphere (possibly more so of the nondominant one) is undoubtedly helpful - this is the practical aspect. The theoretical implication is concerned with the realization that foci in regions such as the anterior temporal lobe lying outside the traditional speech areas can interfere with speech, without their resection affecting speech in any permanent way. One could also add the potential contribution that the study of speech automatisms offers for the study of epileptic automatisms in general, by presenting an example of "release" phenomena which differ from ictal aphasia in a number of characteristic ways, despite their both being paroxysmal speech disorders. From the viewpoint of language the contribution of such phenomena has been, as already admitted, limited. This is undoubtedly due in great part to the circumstances of the occurrence of these symptoms. Brief, of varying intensity and duration, missed by the doctor more often than not, and confounded to a greater or lesser extent by whatever changes in consciousness even a minor fit entails, such instances of paroxysmal speech disorders offer too little even to the most experienced clinical observer to attempt any but the crudest possible distinctions and characterizations. Even the planned stimulation studies in the surgical theater offer little more than that, inevitably hampered by the inadequate periods and rather strained circumstances of the observations. On the other hand, the lack of subtlety and systematic analysis of such observations and studies should not make one overlook the hard facts they have contributed. In short, these add up to the presentation of a dynamic
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model of the relationship of the dominant hemisphere to speech. After all, we should not forget that were it not for these simple but basic observations, i.e. of reversible speech disturbances, our only other evidence as to the speech mechanisms of the brain would still be of a static nature, inferential, in other words, rather than conclusive. I have deliberately left out from this review a number of topics, which although germane to the subject, have already become cardinal chapters in their own right, meriting a special discussion and not just a mention "en passant." Such topics include not only the controversial aspect of handedness versus dominance and the contribution that such methods as intracarotid sodium amy tal have made, but also the effects of subcortical electrical stimulation on the speech of Parkinsonian patients during basal ganglia operations. The significance of the latter has not yet been fully evaluated but the possibility remains that they may have ushered in a new and interesting phase in the study of the mechanisms of speech. REFERENCES ALAJOUANINE, T., and SABOURAUD, O. (1960) Paroxysmal disorders of speech in epilepsy, "Encephale," 49, 95-133. ARSENI, C., and BOTEZ, M. 1. (1961) Speech disturbances caused by tumours of the supplementary motor area, "Acta Psychiat. Scand," 36, 279-299. BINGLEY, T. (1958) Mental symptoms in temporal lobe epilepsy and temporal lobe gliomas. "Acta Psychit. Scand.," KBN, Supplement N. 120. BOUDOURESQUES, 1., ROGER, 1., and GASTAUT, H. (1962) Crises aphasiques subintrantes chez un epileptique temporal. Etude electroclinique, "Rev. Neurol.," 106, 381-393. DRIVER, M. V., FALCONER, M. A., and SERAFETINIDES, E. A. (1964) Ictal speech automatism reproduced by activation procedures, "Neurology," 14, 455-463. FOERSTER, O. (1936) In Handbuch der Neurologie, ed. by Bumke and Foerster, 6, 1-357. Springer, Berlin. GOWERS, W. R. (1893) A Manual of Disease of the Nervous System. Churchill, London. HECAEN, H., and PIERCY, M. (1956) Paroxysmal dysphasia and the problem of cerebral dominance. "Journal of Neurol., Neurosurg. and Psychiat.," 19, 194-20l. - , and ANGELERGUES, R. (1960) Epilepsy and speech disorders, "Encephale," 49, 138-169. JACKSON, J. H. (1898) Article in Selected Writings of John Hughlings Jackson, ed. by Taylor J., 1932. Hodder and Stoughton, London. JEFFERSON, G. (1935) Jacksonian epilepsy. A background and a postscript, "Post-Grad. Med. J.," London, 11, 150-162. MARCHAND, 1., and AJURIAGUERRA, J. (1948) Epilepsies. Declee de Brouver, Paris. MENDILAHARSU, de A., et al. (1694) Etude electroclinique ictale des crises dysphasiques provoquees par activation cardiazolique, "Neuropsychologia," 1, 299-312. PENFIELD, W., and JASPER, H. (1954) Epilepsy and the Functional Anatomy of the Human Brain. Churchill, London. - , and ROBERTS, 1. (1959) Speech and Brain Mechanisms. Princeton University Press, Princeton, New Jersey. RUSSEL, W. R., and ESPIR, M.1.E. (1961) Traumatic Aphasia. Oxford University Press, Oxford. SERAFETINIDES, E. A., and FALCONER, M. A. (1963) Speech disturbances in temporal lobe seizures, "Brain," 86, 333-346. E. A. Serafetinides, M.D., Ph.D., D.P.M., Associate Professor of Psychiatry, University of Oklahoma School of Medicine, Director: EEG Laboratories, University of Oklahoma Medical Center Oklahoma City, Oklahoma, USA.
This review will inevitably start with definitions. These are pever satisfying but serve at least the purpose of delineating the areas of our ignorance. The next step will be to tackle speech symptoms as part of epileptic symptomatology and to see if any useful differentiation can be made among such symptoms - especially in relation to the type of epilepsy and localization of the discharges associated with them. Lastly cortical stimulation observations will be brought in and compared with the clinical data. Since jackson's original report in 1898 it has been accepted that ictal aphasia often occurs in focal epileptic seizures originating in the dominant cerebral hemisphere. In addition speech automatisms have also been described as occurring during epileptic seizures. But what do we mean by ictal aphasia or speech automatisms? Most authors prefer to use these terms without precise definition thus suggesting universal agreement on their significance. This, to a certain extent and within certain time and space limits, may be so, but makes communication and research extremely difficult. Others prefer to paraphrase or use as operational a clinical definition as possible, but even in operational definitions of this kind, unless the terms of reference are themselves sub-defined, as it were, and kept constant, the tacit assumption of universal argreement, characterizing the non-definition school, is still present. In an already published paper (Serafetinides and Falconer, 1963) the following definitions were given: • Based on an invited talk given at the 1965 annual meeting of the Academy of Aphasia (U.S.A.). 2 Now at the University of Oklahoma Medical Center.
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E. A. Serafetinides
A. Paroxysmal Dysphasia is an inability on the part of the patient to express himself by the correct words while he is still conscious and without obvious impairment of articulation or of hearing. The patient mayor may not comprehend fully what is said to him, but his replies are such as to rule out confusion with disorientation or mere speech arrest. On recovery from an attack the patient remembers that during the period of dysphasia he was conscious, but that as he could not find the correct words to express himself, he either stopped talking or verbalized incorrectly. Two main types of paroxysmal dysphasia were recognized by us, viz. (a) expressive, and (b) combined receptive and expressive. Either could occur as an aura at the start of a seizure with or without subsequent loss of consciousness, or if consciousness was lost, immediately on recovery when dysphasia had to be distinguished from confusion. Sometimes an isolated episode of dysphasia may be the only clinical manifestation of a seizure. As paroxysmal dysphasia is as a rule brief, its appreciation and study are usually confined to the auditory and verbal aspects of speech. A cardinal feature of paroxysmal dysphasia as we have defined it, is that it occurs during a period of awareness and is subsequently recalled by the patient. B. Speech automatisms are utterances of identifiable words or phrases at the beginning, during, or just after a clinical attack, which are lin. guistically correct, but for which the patient is subsequently amnesic. I have already mentioned Jackson'S report - one of the earliest, if not the earliest - on ictal aphasia. Gowers (1893), whose astuteness as a clinical observer was no less legendary, is also credited with an early similar report. He made the very crucial observation that ictal aphasia is particularly associated with motor attacks commencing in the right upper limb or in part of the face. Later clinicians noted its not infrequent association with right-sided post-epileptic hemiplegia, which they interpreted as an additional manifestation of post-epileptic paralysis or exhaustion of the brain or as some others, more up-to-date, would put it, of the ensuing inhibition. Some, like Marchand and Ajuriaguerra (1948), comment on the differential incidence of ictal aphasia according to the type of epilepsy, i. e., it is frequent in partial or focal or minor attacks, but much less so in grand mal episodes. They also try to distinguish between dysarthria - following, not infrequently, generalized attacks and without localizing significance - and aphasia with its much more specific characteristics. The brief duration, usually minutes unless complicated by cerebrovascular episodes - the predominantly motor or expressive nature and the occasional concurrence of related symptoms, such as dysgraphia, in the chance instances when such
Speech in Epilepsy and Electro-cortical Stimulation
465
observations could be made, all these and similar experiences of ictal aphasia have been encountered by clinicians habitually studying and caring for epileptic patients. Penfield and Jasper (1954) summarized as follows their experience with speech disturbances in epileptics. Epileptic aphasia occurs as the result of discharge in the dominant hemisphere only ... Unless (the patient) is occupied with words in some way, he is not aware that he is having such an attack ... Epileptic discharge produces activation and interference ... but the effect upon speech is only interference... Epileptic discharge in a cortical speech area undoubtedly activates the ganglion celles but it does not cause the patient to speak or to think of particular words. It produces aphasic arrest of speaking. Aphasic arrest is different from arrest of speaking due to discharge in a portion of the motor cortex that is devoted to movement of the mouth, or respiration or vocalization. Epileptic interference in such areas stops speaking by a motor block. The patient still undestands, and he knows what words he would like to use as soon as he has the mechanism of vocalization and of tongue movement and lip movement again at his disposal.
One appreciates the attempt on the part of Penfield and Jasper to tackle this thorny problem, namely what does constitute an aphasic arrest and what does not. In addition, however, to the fact that such attempts are bound to be either negative or speculative, considering the limited data available, another question arises, and this is whether it is permissible to introduce at this stage the theoretical problems of non-ictal aphasia. It would seem more appropriate to me to talk about ictal speech disturbances in general. If further differentiation is required, or is deemed to be desirable, then purely descriptive terms should be used, terms which would have the greatest relevance to the actual observed phenomena, and little reference to etiological or other preconceptions carried over from the study of non-ictal aphasia. If so little agreement exists as to what really constitutes the latter - and this despite the unlimited time for observation and study that non-ictal aphasia provides - is it not wishful thinking to try to answer fundamental questions on the basis of the usually fleeting and transient ictal speech disturbances, a very small portion of which are ever witnessed by a doctor? Nevertheless, to leave the theoretical implications of this rhetorical question unanswered, the practical implications of such symptoms are unquestionable. To quote Penfield and Jasper once more:
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The presence or absence of aphasia following an attack may ... answer the questions of the hemisphere harboring the focus, which may be of use in temporal lobe seizures, for it frequently happens that the pattern (of such seizures) points to the temporal cortex or to the deep sylvian region and yet gives no obvious clue as to the laterality. Penfield later assembled and published in association with Roberts his epileptic speech material (1959). 273 patients undergoing surgery on the dominant or major side were reviewed and compared with an equal number of patients with an operation on the minor side. Additionally detailed speech examinations were carried out on 72 of the patients. The authors first distinguished between positive and negative disturbances of speech associated with seizures. As positive disturbances or "effects" they considered the instances of vocalization, usually a cry, occurring with an ictus. They ascribed these to discharges originating in the Rolandic or supplementary motor areas of either hemisphere or in subcortical regions. As negative effects they described a number of symptoms. First, they described instances of inability to understand. They considered such instances as due either to discharges originating in the dominant hemisphere and affecting the speech mechanisms or to discharges affecting the primary auditory mechanisms within either hemisphere or subcortically. Disturbances in reading were described as another possibility if the discharges originated in the dominant hemisphere for speech or affected the primary visual areas or affected certain subcortical regions. A third possibility - or negative effect - is inability to speak. In the case of misnaming objects or perseveration or similar known aphasic symptoms, the discharges are located in the speech areas of the dominant hemisphere, whereas if the symptoms are simply silence or dysarthria then the additional or alternative possibility of discharges in the Rolandic or supplementary motor areas of either hemisphere arises. Lastly the authors mention the possibility of dysgraphia, if discharges affect the appropriate speech areas of the major hemisphere. In discussing such symptoms, Penfield and Roberts point out that these can occur either as an aura or during the seizure itself or postictally. A note of caution is also issued. For example, the authors say, if aphasia is the initial symptom of a seizure an EEG determination of the exact locus of the discharges in the dominant hemisphere is still imperative, considering the fact that if the focus or foci are in the anterior temporal or superior
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parietal area, then surgery can be performed whereas if the focus is in the speech area itself, then, of course, surgery is out of the question. It seems, thus, that there is general agreement that paroxysmal dysphasia can occur with epilepsy arising in the dominant cerebral hemisphere although few have associated it with anterior temporal lobe epilepsy. Among the various relatively recent reports on the subject one should start with that of Hecaen and Piercy (1956). They selected 126 patients fulfilling certain criteria of lateralization out of 3000 epileptics. Half of the right-handed patients with left-sided foci showed paroxysmal dysphasia (31 cases out of 63). Of the 34 patients with right-sided foci 4 showed dysphasia. In left-handed patients 17 out of 18 with left hemisphere foci ond 9 out of 11 with right hemisphere foci showed ictal aphasia. Bingley (1958) also studied speech symptoms in patients with epilepsy due to lesions in the temporal lobe. Of the 33 patients with a dominant temporal lobe lesion and epilepsy, 16 had ictal dysphasia, whereas none of the 24 patients with a lesion in the non-dominant temporal lobe had this disturbance. Alajouanine and Sabouraud (1960) also reported similar findings. Russell and Espir (1961) reviewing a different series of patients, namely patients with penetrating war wounds of the brain, found that 280 cases out of a total of 916 showed aphasic symptoms as a result of such wounds. Of these 280 cases no less than 60% also had epileptic seizures. Furthermore - and this is most relevant to the present review - 64 patients reportedly had aphasic auras. They were tabulated as follows, according to handedness and site of lesion: Left Right-handers ft h d Le-aners
~ Aphas~c
aura group Aphasic aura T otal'10 group
~ Total
~
10
. . . .
52
343 6
28
Right 3
276
3
30
The authors although admitting lack of detailed analysis of these cases go on to say that their provisional findings give some support to the view put forward by Hecaen and Piercy (1956) according to which there is a higher tendency for aphasic auras to occur in left-handers even when the lesion is left-sided.
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Instances of ictal aphasia occurring during recording of an EEG thus permitting localization of the focus are very rare with ordinary recordings, i. e. outside the stimulation studies performed during operation. An interesting example was published by Boudouresques, Roger and Gastaut (1962). The patient was a 29 year old man who at the age of 7 developed a left mastoiditis, with high fever, which was complicated by right hemiconvulsive fits plus right hemiplegia and impaired speech, all of which cleared in the course of the subsequent few weeks. The fits reappeared four years later and the patient eventually underwent a left superficial temporal gyrectomy which failed, however, to control his seizure. The patient in addiction now had minor fits in which the main feature was speech arrest of a few seconds duration without loss of consciousness. The resting EEG showed infrequent left middle and anterior temporal slow waves. Metrazol activation produced a grand mal attack in one instance and localized left temporal electrical discharges only in another. However, the authors had the opportunity to perform EEG and psychological studies during a series of spontaneously occuring seizures. They found that the discharges first appeared in the left posterior and middle temporal lobe. They lasted for a minute and would reappear every 2-3 minutes. Altogether the authors recorded a few hundred such sequences throughout the two day period of observation of these spontaneous seizures. During these attacks the patient would appear conscious and could respond correctly. On testing, however, he would commit mistakes in counting and would finally stop counting altogether. He would also misname objects and was unable to speak or write. On the other hand he could identify colors, calculate in some instances, distinguish between right and left, and could understand and carry out commands. The authors concluded that cases with similar episodes may be much more frequent than is ordinarily appreciated, their lack of recognition being presumably due to the general lack of comparable opportunities and facilities, such as the ones the authors were fortunate to have at their disposal. In their study the focus was found, as expected, in the left side, i. e., the dominant hemisphere. However, things do not always happen as expected. Mendilaharsu et al. ( 1964) recently published a report on aphasic episodes provoked, or rather induced, in four patients by the same method as was used by the abovementioned French workers, i. e., 1. V. Metrazol. To summarize their
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findings: they found evidence suggesting that the clinical appearance of ictal aphasia coincides with the generalization of the abnormal EEG findings. They interpreted this as the effect of subcortical rather than cortical involvement, and by inference, ascribed to these subcortical changes the responsibility for the clinical phenomena observed. No strict comparison is however permissible between the results of this metrazol activation study and of the studies of spontaneous seizures as they are in so many ways the endproducts of dissimilar processes. Thus in the French study, Metrazol produced in its two applications on the same subject two different pictures - and neither of these were similar to his habitual seizures. The involvement of the supplementary motor area of the major hemisphere in paroxysmal speech disturbance has been emphasized by Arseni and Botez (1961) of Bucharest. These authors reported twelve cases with tumors, mainly meningiomas, in that area. Paroxysm. al speech symptoms alone appeared in three cases. In three other cases they were seen together with minor focal or major attacks. The speech disturbances consisted either of speech arrest or of involuntary repetition of words, onomatopoeic sounds, distorted words, and neologisms. It is quite possible that some of these symptoms could be termed ictal speech automatisms - although the majority of them were most likely aphasic. Finally a study (Serafetinides and Falconer, 1963) was made of the pre-operative seizure patterns in 100 cases of temporal lobe epilepsy submitted to an anterior temporal lobectomy and subsequently followed up for periods from two to ten years. Speech disturbances were observed in connexion with the seizures in 67 patients. These disturbances were of a dysphasic type in 34 patients and of a speech automatism type (e. g. warning, recurrent, irrelevant, emotional, and/or perplexity utterances) in 38. Ictal aphasia occurred either at the beginning of the ictus or immediately afterwards and was subsequently remembered, whereas ictal speech automatisms always occurred during a period for which the patient was subsequently amnesic. In four patients both types of symptoms were present but occurred independently. Ictal automatisms have been studied less than ictal aphasia. Bingley (1958) found the latter in 29 out of 74 cases of temporal lobe epilepsy. It was present in 25 per cent of cases with aunilateral
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EEG focus in the dominant lobe, and in 59 per cent of the cases with a unilateral focus in the non-dominant lobe. This difference is significant at the 0.01 level. Only 4 patients in this series had both paroxysmal dysphasia and speech automatism. Bingley therefore felt that the two features occurred independently. Hecaen and Angelergues (1960) reported similar findings. Driver, Falconer and Serafetinides (1964) reported the following case of speech automatisms. The patient, a Pole aged 38, was moved to Siberia at the age of 16 years, and became fluent in Russian as well as his mother tongue. At the age of 22 he went to England and started learning English in which he became proficient. His seizures started when he was 25 years old, and were of psycho-motor type with epigastric, cephalic, and occasionally olfactory auras. Witnesses described that at the onset of each attack he would say repeatedly in English "I beg your pardon, I beg your pardon ... " while his eyes would stare and he would make chewing movements, followed later by abduction of the left arm. An EEG focus had been noted consistently in the right sphenoidal area during resting recordings as well as during Metrazol activated recordings with reproduction of the automatisms. Similar observations were made on electrocortical stimulation in the course of a right temporal lobectomy which had a favorable effect on the seizures. In discussing this case the authors felt that if speech automatisms were a direct product of epileptic discharges arising in the minor hemisphere, they could be regarded as ictal analogues of the compulsive or emotional speech occurring in dysphasic patients with dominant hemisphere lesions and attributed by Jackson to function of the minor hemisphere. However, this hypothesis was not considered satisfactory as a general explanation since speech automatisms could occur in association with epileptogenic lesions of either hemisphere. An alternative explanation was then considered, namely that the ictal discharges in the minor hemisphere (or in some patients in an appropriate part of the major hemisphere) lead to an upsetting of reciprocal excitation-inhibition relationships. This, it was postulated, removes the normal control of the speech mechanisms which then embark on an automatic or stereotyped activity. The clinical and electrographic events observed during the electrically induced seizure at operation in this published case were thought to be compatible
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with such an hypothesis. During that period the ictal discharge activity was confined to a limited area of the right temporal lobe including the amygdala. The remaining areas in the right hemisphere (and by inference the left hemisphere also) showed a pattern compatible with normal functioning. With the generalization of the abnormal activity, the speech automatism ceased. We have so far examined data of clinical origin. The electrical stimulation data to which we will now turn are, as expected, much fewer, but nonetheless crucial. Jefferson as far back as 1935 reported speech arrest in patients whose angular gyrus was stimulated by electric current. Foerster (1936) produced, a year later, grunts and groans by stimulating the lower rolandic region. Our main body of evidence, however, on speech and cortical stimulation derives from Penfield's extensive work. The main conclusion of Penfield's work in relation to our subject is that aphasic arrest may be produced by electrical stimulation just as it is by epileptic discharge.
Altogether 114 patients were studied by this method during operation (Penfield and Roberts, 1959). Of these, in 94 cases the operation was on the left side and in 20 on the right. Excluding unsuitable cases, 5 out of 65 right-handed patients had post-operative aphasia - a usual but transient complication of cerebral resections involving the major temporal lobe and adjacent areas. All 54 patients had electrical stimulations of their exposed cortex while they were conscious and could thus collaborate with the surgeon in speech testing, before resection, by counting, reciting or naming objects. In all instances speech was affected, the usual end-result being speech arrest or misnaming of common objects. The areas which when stimulated produced these results were: Broca's area, the inferior parietal area and the posterior temporal area - all on the left or major side. Negative results were not accepted immediately as evidence that the areas in question were not related to speech, unless the same voltage had produced positive results in a neighboring area. Penfield is categorical as to the meaning of this positive response. To quote: When stimulation produces aphasic arrest it is clear that the hemisphere exposed is dominant for speech, for we have never been able to produce such an effect from the non-dominant hemisphere.
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It seems that there are only three areas in the dominant hemisphere from which arrest or distortion of speech can be consistently obtained. These three areas are: 1) the posterior temporoparietal region occupying the posterior parts of the three lateral temporal gyri, the supra-marginal gyrus, and the angular gyrus; 2) Broca's area in front of the lower pre-ventral gyrus; and 3) the supplementary motor area lying in the medial aspect of the hemisphere just in front of the pre-central leg area. The electric current when applied to these areas produces a negative effect upon speech, which the authors named "interference," and which is akin to dysphasia. When, however, it is applied to the motor areas (Rolandic and supplementary) of either hemisphere it can produce a positive effect - "stimulation" which leads to vocalization. SUMMARY AND CoNCLUSION
The evidence presented so far, both clinical and experimental, can be looked at from two different viewpoints. From the point of view of epilepsy the implications are mainly of practical but also of theoretical interest. In those cases where neurosurgery is contemplated, or localization of the discharges is considered to be desirable, the presence of ictal aphasia, indicating involvement of the dominant hemisphere, and speech automatism indicating involvement of either hemisphere (possibly more so of the nondominant one) is undoubtedly helpful - this is the practical aspect. The theoretical implication is concerned with the realization that foci in regions such as the anterior temporal lobe lying outside the traditional speech areas can interfere with speech, without their resection affecting speech in any permanent way. One could also add the potential contribution that the study of speech automatisms offers for the study of epileptic automatisms in general, by presenting an example of "release" phenomena which differ from ictal aphasia in a number of characteristic ways, despite their both being paroxysmal speech disorders. From the viewpoint of language the contribution of such phenomena has been, as already admitted, limited. This is undoubtedly due in great part to the circumstances of the occurrence of these symptoms. Brief, of varying intensity and duration, missed by the doctor more often than not, and confounded to a greater or lesser extent by whatever changes in consciousness even a minor fit entails, such instances of paroxysmal speech disorders offer too little even to the most experienced clinical observer to attempt any but the crudest possible distinctions and characterizations. Even the planned stimulation studies in the surgical theater offer little more than that, inevitably hampered by the inadequate periods and rather strained circumstances of the observations. On the other hand, the lack of subtlety and systematic analysis of such observations and studies should not make one overlook the hard facts they have contributed. In short, these add up to the presentation of a dynamic
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model of the relationship of the dominant hemisphere to speech. After all, we should not forget that were it not for these simple but basic observations, i.e. of reversible speech disturbances, our only other evidence as to the speech mechanisms of the brain would still be of a static nature, inferential, in other words, rather than conclusive. I have deliberately left out from this review a number of topics, which although germane to the subject, have already become cardinal chapters in their own right, meriting a special discussion and not just a mention "en passant." Such topics include not only the controversial aspect of handedness versus dominance and the contribution that such methods as intracarotid sodium amy tal have made, but also the effects of subcortical electrical stimulation on the speech of Parkinsonian patients during basal ganglia operations. The significance of the latter has not yet been fully evaluated but the possibility remains that they may have ushered in a new and interesting phase in the study of the mechanisms of speech. REFERENCES ALAJOUANINE, T., and SABOURAUD, O. (1960) Paroxysmal disorders of speech in epilepsy, "Encephale," 49, 95-133. ARSENI, C., and BOTEZ, M. 1. (1961) Speech disturbances caused by tumours of the supplementary motor area, "Acta Psychiat. Scand," 36, 279-299. BINGLEY, T. (1958) Mental symptoms in temporal lobe epilepsy and temporal lobe gliomas. "Acta Psychit. Scand.," KBN, Supplement N. 120. BOUDOURESQUES, 1., ROGER, 1., and GASTAUT, H. (1962) Crises aphasiques subintrantes chez un epileptique temporal. Etude electroclinique, "Rev. Neurol.," 106, 381-393. DRIVER, M. V., FALCONER, M. A., and SERAFETINIDES, E. A. (1964) Ictal speech automatism reproduced by activation procedures, "Neurology," 14, 455-463. FOERSTER, O. (1936) In Handbuch der Neurologie, ed. by Bumke and Foerster, 6, 1-357. Springer, Berlin. GOWERS, W. R. (1893) A Manual of Disease of the Nervous System. Churchill, London. HECAEN, H., and PIERCY, M. (1956) Paroxysmal dysphasia and the problem of cerebral dominance. "Journal of Neurol., Neurosurg. and Psychiat.," 19, 194-20l. - , and ANGELERGUES, R. (1960) Epilepsy and speech disorders, "Encephale," 49, 138-169. JACKSON, J. H. (1898) Article in Selected Writings of John Hughlings Jackson, ed. by Taylor J., 1932. Hodder and Stoughton, London. JEFFERSON, G. (1935) Jacksonian epilepsy. A background and a postscript, "Post-Grad. Med. J.," London, 11, 150-162. MARCHAND, 1., and AJURIAGUERRA, J. (1948) Epilepsies. Declee de Brouver, Paris. MENDILAHARSU, de A., et al. (1694) Etude electroclinique ictale des crises dysphasiques provoquees par activation cardiazolique, "Neuropsychologia," 1, 299-312. PENFIELD, W., and JASPER, H. (1954) Epilepsy and the Functional Anatomy of the Human Brain. Churchill, London. - , and ROBERTS, 1. (1959) Speech and Brain Mechanisms. Princeton University Press, Princeton, New Jersey. RUSSEL, W. R., and ESPIR, M.1.E. (1961) Traumatic Aphasia. Oxford University Press, Oxford. SERAFETINIDES, E. A., and FALCONER, M. A. (1963) Speech disturbances in temporal lobe seizures, "Brain," 86, 333-346. E. A. Serafetinides, M.D., Ph.D., D.P.M., Associate Professor of Psychiatry, University of Oklahoma School of Medicine, Director: EEG Laboratories, University of Oklahoma Medical Center Oklahoma City, Oklahoma, USA.