THE ANATOMICAL BASIS OF APHASIA AS SEEN BY PIERRE MARIE!

Monroe Cole

(Department of Neurology, Bowman Gray School of Medicine, Wake Forest University, Winston-Salem, North Carolina)

It is commonly held by most physicians, including neurologists and speech pathologists, and also commonly taught in medical schools, that aphasia may be divided into two separate syndromes. These two, expressive and receptive aphasia, are each aligned with a very specific locus of anatomical change. Indeed, this is the classical conception and one which came into vogue after the well known monograph of Wernicke in 1874. I have never personally been impressed with the exact correlation of pathological findings with the clinical manifestations of aphasia. On the contrary, I have found Pierre Marie's rather unitary concept of aphasia to be useful and reasonably accurate. In addition, the theoretical points which it raises may be worthy of discussion. For these reasons I welcome the opportunity to present some of his views before this Academy.

Pierre Marie was born in Paris on September 9, 1853 of an upper-middle-class family and died on April 13, 1940. He trained under Bouchard, Charcot, and, interestingly enough, under Broca. His major work concerning aphasia was started shortly before the turn of the century. His most famous paper on the subject was presented to the medical world dramatically and courageously in May 1906, and entitled "The Third Left Frontal Convolution Plays No Special Role in the Function of Language." (Marie, 1906a). He continued his studies on this subject through World War I.

In 1907 he was elected Professor of Pathologic Anatomy at the Faculty of Medicine of Paris, a Chair held by only two other

! Presented to the Academy of Aphasia, October 16, 1967, Ann Arbor, Michi­gan, U.S.A. This work was supported in part by National Institutes of Health Grant No. NB05865-03.

P. Marie and the anatomical basis of aphasia 173

neurologists, Vulpian and Charcot. After the death of Dejerine in 1918, Pierre Marie followed in his footsteps to the Chair of Clinical Neurology at the Salpetriere. Most of his work, incidentally, had been done at the Bicetre. It might parenthetically be stated that these biographical comments are taken fro~ the obituary published in Volume 72 of the Revue Neurologique, a journal which he founded with Edouard Brissaud, and in which he maintained a personal interest until the end of his life.

One is astounded by the productivity which Marie maintained throughout his professional life. In addition to his studies on aphasia he described with Charcot the hereditary neuropathy which now bears the name, in this country, of Charcot-Marie-Tooth disease. He attempted to separate a group of hereditary cerebellar ataxias of adult onset, which in some quarters today still bears the name of Marie's cerebellar ataxia. He wrote extensively on diseases of the spinal cord and in 1892 published the lectures on this subject which he gave to the Faculty of Medicine. His descriptions of the lacunar state have never been improved upon. He concerned himself with cerebral topography and with the general clinical presentation of lesions of the cerebrum and internal capsule. Like most neurologists of his day he was concerned with the problems of general medicine and wrote extensively on thyrotoxicosis and achondroplasia, in addition to which he gave the classical descriptions of acromegaly, hypertrophic pulmonary osteoarthropathy, and hereditary cleido-cranial dysostosis. He made a major contribution to the description of rheumatoid spondylitis, which he called "spondylose rhizomelique."

Like Wernicke, he had the ability to develop distinguished students, a number of whom, such as Guillain, Roussy, Lhermitte the elder, Foix, Bertrand, Marinesco, and van Bogaert, lecame leaders of their profession.

The breadth of his interests is noteworthy, but one is also impressed by the clarity, the vigor and the honesty of his writings. His clinical descriptions, for example the paper on the lacunar state, are precise and unequalled. Regarding his works on aphasia, he took an unpopular stand and, based on his own personal examinations of the patients and the anatomical specimens, had the courage to stand up to men such as Dejerine to express his views without equivocation.

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At the turn of the century students of the nervous system were perhaps more concerned than we are today with the question of holism versus localization in the higher cerebral centers. Much support was evident for a concept of "centers" of the brain, each more or less circumscribed and each responsible for various parameters of higher cerebral function. Marie concerned himself with reversing this trend and while he considered himself an anti-Iocalizationist, made a reasonable, and, I submit, rather accurate compromise between these two schools.

In his own words he was not concerned with doctrinaire and theoretical speculation concerning aphasia. For all their limitations, his studies are remarkable in the sense that the patients were studied clinically and their brains examined pathologically in an adequate manner, by one individual. Neuroanatomy had progressed sufficiently by this time so that Marie's concepts of brain morphology were by no means naive, as had been the case, for example, with Broca some 40 years earlier. It is true that he did not concern himself with the psychology or physiology of language; he never claimed to do so. For this reason it may be stated that he did not greatly enhance our understanding of language function, but it must be admitted that his observations are immutable. As he stated, "We must keep to the old anatomical clinical method which, judiciously applied, never led anyone into error." (Marie, 1906a).

Marie's major concepts include: 1) the error of relating lesions of the frontal operculum to aphasia; 2) the true nature of aphasia; 3) the lack of multiple forms of aphasia; 4) the "intellectual" disturbance in aphasics; and 5) the falsity of a conception of "centers" in the cerebral cortex.

Marie was led to the consideration of the frontal operculum as a nonessential locus in the production of aphasia by a number of considerations. It will be recalled that the concept of Broca's aphasia was based on the description of a patient named Leborgne who was on Broca's service for only six days, dying of a diffuse cellulitis. Although I could not find a comment by Marie concerning this patient's ability to comprehend, Broca himself noted "The state of his intelligence could not be exactly determined." (Broca, 1861). Actually, the patient was not, and due to his severe illness could not be, examined by sufficiently rigorous techniques, even were they available, to determine the exact state of his comprehension. While

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Broca remarked that his comprehension was intact, he also stated, "Nonetheless, several questions to which a man of ordinary intelligence would have found the means to respond by gesture, remained without response... At still other times the answer was clear but wrong, for instance, although he had no children he pretended to have some." (Broca, 1861).

But more important than the clinical findings, or the lack thereof, was the remarkable story of the anatomical specimen. In spite of the fact that important conclusions were drawn from this specimen, it was never sectioned but was deposited in alcohol in the Dupuytren Museum. The specimen was re-examined some 40 years later by Ma­rie. As far as I know, it was never cut. He found destruction not only in the posterior half of the third frontal convolution but also in T-1 and the gyrus supramarginalis. Broca, of course, recognized this and tried to point out that the lesion of F-3 was the oldest one and therefore the one responsible for the aphasia, but the evidence was not convincing.

Marie also criticized Broca's second case, Lelong, stating that there was no focal lesion at all on the external sudace of the brain. This brain also was not sectioned and simply showed cerebral atrophy. In this conclusion he was violently opposed by Dejerine, who felt that Broca's description was accurate, and one can only report this dispu­tation of fact without drawing any conclusion as to who was correct. Furthermore, Marie had considerable doubt that patient Lelong was aphasic at all, but rather felt that he was a senile dement. Broca's description of Lelong, however, does indicate that the patient sus­tained an acute aphasia eight years before his death.

Marie emphasized two additional points: 1) cases are not uncom­monly seen with a lesion of the third frontal gyrus without any evi­dence of aphasia during life; and 2) patients with what he calls typical Broca's aphasia need not have a lesion of the third frontal convolution. Marie noted a lesion. of this area in about half the cases of Broca's aphasia observed in his own service at the Bicetre. However, the lesion was not confined to this area, and he takes great pains to point out that it is only a portion of an infarct which, due to a middle cerebral artery occlusion, involves Wernicke's area as well. He is also careful to point out that the so-called cortical aphasias are never purely cortical as they also involve, to a greater or lesser degree, subcortical white matter. This observation appears to be borne out, at least in part, by the cortical ablation data of Lamar Roberts

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and Wilder Penfield (1959). It should be recalled, however, as these two authors point out, that their studies were done on people whose brains were abnormal.

I t would appear to me that denial of the special importance of the third frontal convolution was not the central and most important idea that Marie wanted to get across, but he stressed this in his first paper in order to dramatically draw the attention of his au­dience to something more important. This was the nature of aphasia and its contrast with a syndrome which he named anarthria. As he states in his first paper. "One fact dominates the study of aphasia, it is the following: in the case of all aphasics there exists a trouble, more or less pronounced, with comprehension of spoken language. The degree of intensity of this trouble can, however, be very variable. In certain marked cases of aphasia almost no word is understood, the patients are entirely unable to understand what is said to them; in other lighter cases the patients understand admirably the simple ques­tions which are put to them and execute in perfect manner the simple orders given to them, but if the questions or the orders become more complicated, one immediately sees produced the characteristic deficit of aphasia." (Marie, 1906a).

In this statement he therefore not only pointed out his own concept of the nature of aphasia (and the question of its accuracy and profundity will, I hope, generate some discussion in this Academy), but further, he emphasized the fact that tests must be graded in com­plexity and that unless the deficit is specifically searched for in a meticulous manner, it may well be missed. In this Academy today such a statement may be a non sequitur, but it was not such at the turn of the century. He then went on to describe his two famous tests, the Marie paper test, "Of the three pieces of paper of different sizes placed on this table, you will give me the largest one, you will crumple the middle-sized one and throw it down; as to the smallest, you will put it in your pocket." (Marie, 1906a). And the second test, "You will stand up, you will knock three times on the window with your finger, then you will return in front of the table, you will walk around your chair and you will sit down." (Marie, 1906a). It may be argued that in some cases of genuine aphasia careful search might reveal a deficit of comprehension, but it may be slight compared to the expressive difficulties and therefore of no importance. To Marie, however, even a slight comprehension deficit was of major "physio­logical," if you will, importance in determining the aphasic state. It

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may indeed be a fact that even small deficits of comprehension play a major role in the inability of the aphasic patient to use symbolic language. Many times Marie referred to this deficit as a deficit of "internal speech." Concomitant with the deficit of comprehension the individual would also have a variable deficit of reading, writing and intellect, though the last term needs further discussion.

Let Marie give his concepts in his own words: "What clinically characterizes the aphasia of Wernicke is that the patients can speak, sometimes they even speak too much, but they speak badly; they present jargon aphasia or at least a paraphasia. They understand badly what is said to them and this, as we have seen, is due not to so-called deafness for auditory verbal images, but to an intellectual loss. For the same reason they are no longer able to read or write." (Marie, 1906a).

"In the aphasia of Broca the patients are no longer able to read, they can no longer write, they understand badly what is said to them; in a word, the clinical aspect is very analogous in this respect to the aphasia of Wernicke, but an important difference is that they are no longer able to talk. Therefore the only essential difference which exists between an aphasic of Wernicke and an aphasic of Broca is only that one speaks and the other does not. But for all the rest they resemble one another and, taking it a little further, they are one like the other, incapable of reading and writing, incapable of under­standing what is said to them when the question is a little bit com­plicated." (Marie, 1906a).

Further he states, "The following formula: the aphasia of Broca is the aphasia of Wernicke minus speech - would present, within the doubtless too rigid confines of a formula, a large part of the truth." (Marie, 1906a). Parenthetically it may be stated, considering the modern studies of Howes (1964), that his formula would accurately differentiate so-called anterior and posterior aphasia.

Regarding his concept of anarthria, Marie states, "The anarthria which is in question here is certainly anarthria due to lesion in the site of the cerebrum. It is characterized by the fact that the speech of the patient is either almost gone or at least incomprehensible to the point where one might in this regard confound anarthria with the aphasia of Broca, but the characteristics that distinguish these two syndromes are numerous and decisive. Contrary to aphasics, the anarthrics understand perfectly what one says to them, even when it is a question of complicated phrases; they can read and write and

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are even capable of indicating by signs how many syllables or letters compose the words which they are unable to articulate." (Marie, 1906a). Furthermore, although he states in a number of places that anarthria does not belong exclusively to the left hemisphere, I have not been able to find in his writing one documented case of this assertion.

Marie, however, hedges this point about anarthria arising from either hemisphere in a footnote to his paper of October 17, 1906 entitled "What To Think About The Cortical Aphasias (Pure Apha­sias)." He states here, "In a general way anarthria due to a lesion of the lenticular zone of the left hemisphere will always present a greater intensity and duration than in cases of lesions in the right hemisphere. It is difficult to say whether this inequality in the diff­erent characteristics of this anarthria by lesion of the left hemisphere is due to the proximity of the center of language (territory of Wer­nicke) in the hemisphere , or whether it does not also arise partly from the fact that, in the course of the evolution of the human brain, there was produced in the left hemisphere a certain degree of specia­lization of the coordinator apparatus which presides over phonation and articulation." (Marie, 1906b).

He emphasizes the fact in distinguishing these syndromes that "aphasia is one" and states that all lesions producing aphasia occur in Wernicke's area, i.e., the gyrus supramarginalis, gyrus angularis, and the superior two temporal gyri.

Anarthria, on the other hand, has its locus in the so-called "lenticular zone" which is bound by drawing" a transversal line from the anterior sulcus of the insula to the corresponding point on the lateral ventricle and another transversal line from the posterior sul­cus of the insula to the corresponding point in the lateral ventricle," circumscribing thereby a "quadrilateral" (Marie, 1907). This area contains the caudate and lenticular nuclei, the external capsule and the internal capsule. Marie was uncertain of the exact superior and inferior limits of the zone.

Although Marie emphasized the distinction between aphasia and cortical anarthria, it appears that Broca was also aware of two dis­tinct syndromes. He distinguished "verbal amnesia," in which the "memory for words" written and spoken was lost, from "aphemia." In the latter, comprehension was intact but pronunciation was im­paired. The "verbal amnesia" of Broca corresponds closely to the

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"aphasia" of Marie, while "aphemia" corresponds to anarthria" (Bro­ca, 1869).

As an additional anatomical note, Marie stressed the point that the subcortical white matter appeared to play a more important role in the development of clinical aphasia than the cerebral cortex, a site which had been inordinately stressed over the previous years.

It is of some interest that Marie described a case of "anarthria" ( 1907) in which the individual, although a Parisian, developed a "well marked Alsatian accent." Similar observations have been made by Whitty (1964) and Monrad-Krohn (1947).

Marie generally retained his conception of speech difficulties in a later paper published in 1917, with Charles Foix, entitled "The Aphasias of War." In this paper he differentiated anterior anarthric syndromes from posterior aphasic syndromes, illustrating these by reference to the site of injury on the skull. The anarthric syndromes generally had a good prognosis as compared with the aphasic syndromes. He clinically distinguished four groups of anarthric conditions: 1) those which heal completely or nearly so, although after the patients recovered they would occasionally find some hesitation or difficulty in finding words; 2) the second group had more persistent dysarthric syndromes when tested with words of greater or lesser difficulty; 3) the third group displayed slight findings of an aphasic type, for example, difficulties with reading, writing or calculation; 4) a final group had a persistent slowness of speech and of idea formation with or without persistent dysarthric difficulties. It is to be noted that in the posterior zone of anarthria one would see more complex syndromes in which aphasia played an important role.

While Marie continued to have a unified concept of aphasia, he nevertheless differentiated four principal anatomical forms of aphasia caused by wounds of war: 1) temporal aphasias; 2) those due to lesions of the gyrus supramarginalis; 3) posterior aphasias, i.e., lesions of the gyrus angularis; and 4) small aphasic syndromes caused by marginal or superficial lesions. The temporal aphasias were usually not accompanied by hemiplegia or hemianesthesia but hemianopsia was frequent, especially quadrantic defects. Articulation was good; reading and writing were affected, and the naming of objects and comprehension was severely affected. Prognosis in this syndrome was generally poor.

In aphasias of the gyrus supramarginalis there was usually an

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associated hemiplegia or brachial monoplegia with marked sensory difficulties; comprehension was relatively good except for complicated tests; naming was difficult and there was trouble in pronouncing words. Calculation was impaired as was writing; the patient was able to understand written orders.

With lesions of the gyrus angularis, there was almost always an incomplete hemianopsia, although no hemiplegia. The characteristic feature of this syndrome was an extremely marked alexia. Comprehension of speech was somewhat diminished; naming was also somewhat diminished; writing was altered but not nearly as much as reading; calculation was involved.

Finally, there was a fourth group, characterized by poor facility with speech and a variable deficit of the modalities tested, but especially noteworthy was an incapacity to "reunite ideas and to condense them into phrases, which explains the poor quality of their spontaneous writing and notably their letters which are uniquely composed of ready-made phrases and banal ideas." (Marie and Foix, 1917).

In addition there was a group of cases which demonstrated a so-called global aphasia of the Broca type involving a mixture of aphasia and anarthria.

Regarding those patients wounded in the right hemisphere Marie and Foix observed slight and transitory difficulties affecting articulation and naming. These difficulties were insignificant and, in some respects, ascribed to left-handedness. Once again no good cases of severe and persistent dysarthria were reported with lesions of the right hemisphere.

No discussion of anarthria would be complete without comment on Marie's attitude towards subcortical or pure aphasias. One may say that the descriptions of pure motor aphasia or subcortical motor aphasia and anarthria are equal, and it is only a matter of terminology. Marie insisted, "Let no one believe we are dealing here simply with a question of words." Although the clinical picture is exactly the same and admitted to be so by Marie, he remained adamant in his view that there is a distinct qualitative difference between those disorders which involve a deficit of comprehension and those which do not. This qualitative disorder concerns the presence or absence of "interior language." Marie continued to insist that the anarthric group of patients could be differentiated from true aphasics by their undiminished ability to read, write and comprehend.

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Finally, another attribute which Marie considered typical of aphasics should be commented upon - that is, "in the case of aphasics there is something much more important and much more grave than the loss of the sense of words; it is a very marked diminution in intellectual capacity in general." (Marie, 1906a). The real problem here lies in exactly what Marie meant by "intellectual capacity." Perhaps this can be best described in his own words: "I have said that the zone of Wernicke was not a psychosensory center but an intellectual center - I have tried to bring to light the fact that it is not the whole intelligence which darkens with lack of comprehension of spoken language and that these troubles of intelligence of aphasics constitute a specialized deficit bearing especially on the stock of things learned by didactic processes." (Marie, 1907). As examples of this deficit of intellect he mentioned amusia, acalculia and probably apraxia, the last demonstrated by his rather charming case of the former cook whom he tested by taking him into the kitchen and asking him to cook an egg, giving him the necessary ingredients of a plate, egg, butter, pepper, salt, etc. As he states, "The supervisor was scandalized to see how badly a cook did with a test that even for a simple housewife would be nothing at all." (Marie, 1906a). After describing all the errors the cook made in cooking the egg, he added that, useless to say, the platter was absolutely not presentable. In further qualifying the intellectual deficit he states that it is not comparable to the harsh deficit in certain dementias and general paralysis. He said, "I will recall only that it is to the very lesion in the zone of Wernicke as an intellectual center that I directly relate the deficit noted in the intelligence of aphasics; the troubles of language which are thus determined in those cases are due to a trouble of intellectual elaboration and not, as the authors say, to a trouble of sensory reception." (Marie, 1907). It is thus difficult, at least for me, to be fully certain what Marie meant by this deficit of intellect, but I would assume that he equated it with the deficit of comprehension.

To summarize: I would submit that the following are Marie's contributions to the study of aphasia:

1) a reassertion of the importance of careful clinical testing and the use of graded quantitative tests;

2) a reassertion of the importance of the careful recording of anatomical correlates of aphasia;

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3) the concept that a deficit of comprehension was the sine qua non of aphasia, and to this it may be parenthetically added that he has had some recent support from the work of De Renzi and Vignolo (1962);

4) the relationship of aphasia to posterior lesions of the dominant hemisphere;

5) his detailed differentiation of cortical dysarthria, which he related to lesions of the "lenticular quadrilateral";

6) his denial of the importance of the frontal operculum in the genesis of aphasia;

7) his emphasis on the importance of lesions of the subcortical white matter as opposed to lesions of the cortical mantle per se;

8) his insistence on the presence of an intellectual deficit in aphasia. (As has been pointed out, this is a circumscribed deficit and may be the same as that of comprehension);

9) his unified concept of aphasia.

Marie, brought up in a tradition of localization, concluded that the anatomical evidence warranted a more integrated view of higher cerebral function. He denied the existence of cerebral centers and stressed his belief that the cortex controlled functions in a broader sense. Yet perhaps he was more of a localizationist than he realized. It is to his credit that he considered his clinico-pathologic observations more reliable than a half-century of hallowed tradition. In this, he was a worthy representative of the French school of neurology and a master we can all well emulate.

REFERENCES

BROCA, P. (1861) Remarques sur Ie siege de la faculte du language articute, "Bulletin de 1a Societe Anatomique de Paris," 6, 330-351, reproduced in VON BONIN, G. (1960) Some Papers on the Cerebral Cortex. C. C. Thomas, Springfield, Ill.

-, (1869) Sur Ie siege de la faculte du language articule, "La Tribune Medicale," 74, 254-256; 75, 265-269.

DE RENZI, E., and VIGNOLO, L. A. (1962) The Token Test: A sensitive test to detect receptive disturbances in aphasics, "Brain," 85, 665-678.

HOWES, D. (1964) Application of the Word Frequency Concept to Aphasia, in Disor­ders of Language, ed. by AV.S. de Reuck and M. O'Connor, Little, Brown & Co., Boston, Mass.

MARIE, P. (1906a) La troisieme circonvolution frontale gauche ne ;oue aucun role special dans la fonction du langage, "Semaine Medicale," May 23, reproduced in MARIE, P. (1926) Travaux et Memoires. Tome I. Masson et Cie., Paris, pp. 3-30.

P. Marie and the anatomical basis of aphasia 183

(1906b) Que faut-it penser des aphasies sous-corticales (aphasies pures)?, "Se­maine Medicale," October 17, reproduced in MARIE, P. (1926) Travaux et Me­moires, tome I, Masson et Cie, Paris, pp. 31-64. (1907) Sur la fonction du language, "Revue de Philosophie," reproduced in Marie, P. (1926) Travaux et Memoires. Tome I, Masson et Cie., Paris, pp. 93-113.

(Obituary): Pierre Marie (1853-1940) "Revue Neurologique" 72: 533-543, 1939-40. -, and Forx, C. (1917) Les aphasies de guerre, "Revue Neurologique," 31-32, 54-87. MONRAD-KROHN, G. H. (1947) Dysprosody or altered "melody of language," "Brain,"

70, 405-415. PENFIELD, W., and ROBERTS, 1. (1959) Speech and Brain Mechanism, Princeton Univ.

Press, Princeton, N.J. WHITTY, C. W. M. (1964) Cortical dysarthria and dysprosody of speech, "J. Neurol..

Neurosurg. Psychiat." 27, 507-510.

Monroe Cole, M. D., Department of Neurology, Bowman Gray School of Medicine, Winston·Salem, North Carolina 27103, U.S.A.