Hemispheric dominance before broca

Hemispheric dominance before broca

Neurop~ycholoaia,Vol. 22. No. 6, pp. 807-811, 1984. Primed in Great Britain. 0028-3932/84 $3.00+0.00 V 1984PergamonPress Ltd. HEMISPHERIC D O M I N ...

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Neurop~ycholoaia,Vol. 22. No. 6, pp. 807-811, 1984. Primed in Great Britain.

0028-3932/84 $3.00+0.00 V 1984PergamonPress Ltd.

HEMISPHERIC D O M I N A N C E BEFORE BROCA* A R T H U R BENTON Departments of Neurology and Psychology, University of Iowa, Iowa C i t y , IA 52242, U.S.A.

(Accepted 1 February 1984~ Abstract--Analysis of early medical literature indicates that considerable evidence for a specific association between speech disorder and disease of the left hemisphere was incorporated within it. The diverse reasons for the failure of clinicians to perceive the association are discussed and the approach of Marc Dax to the question is described.

INTRODUCTION A PERSISTING question in the history of neuropsychology is why so many astute clinician-pathologists before 1860 failed to grasp the connection between aphasia and disease of the left hemisphere or, indeed, between aphasia and the occurrence of right hemiplegia. With the benefit of hindsight, one can see that the ingredients for establishing a correlation were already present in ancient medical writings. There is the statement in the Hippocratic corpus that associates temporary speechlessness following convulsions "either with paralysis of the tongue or of the arm and right side of the body" [5, p. 248]. Coupled with this is the well-known Hippocratic observation that "an incised wound in one temple produces a spasm in the opposite side of the body" [5, p 263]. Some 500 years later Aretaeus of Cappadocia sought to explain this observation of contralateral motor impairment following a head wound by postulating a crossing of the nerve tracts from the brain to the spinal cord [1, p. 306]. It is not unreasonable to think that an integration of these statements would have suggested a specific association between speech disorder and left hemisphere disease. A possible reason for the failure to make the correlation is that Aretaeus' remarkable conception was by no means universally accepted. Many physicians interpreted the occurrence of paralysis on the side contralateral to the side of injury as being the result of concussion, diffuse inflammation or a contrecoup effect. However, in the 18th century these factors were effectively eliminated as putative causes when Pourfour du Petit demonstrated the crossing of the descending nerve tracts at the level of the pyramids and Morgagni assembled an impressive mass of clinicopathologic case material to support the association between paralysis of one side of the body and disease of the opposite hemisphere, No doubt a systematic survey of the early medical literature would disclose a trend for "speechlessness', "aphonia", "alalia" and "speech amnesia" to be associated with paralysis of the right side of the body. But at the same time the unbiased compiler would have noted many cases that did not follow the rule, i.e. speechlessness without paralysis or with left-sided

*Dedicated to the memory of Henry H6caen. 807

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paralysis and left hemisphere disease without speech disorder. Thus he would have to conclude there was no obligatory association between aphasia and right-sided paralysis (or left hemisphere disease). Moreover, he would find that the early literature did not yield as rich a harvest as might have been anticipated. These reports were generally only a few lines in length and lacking in essential details. When speechlessness or disordered speech is mentioned, it is usually impossible to determine whether the impairment in expression was aphasic in nature or a reflection of neuromotor disability, stupor, confusion, dementia or psychosis. Descriptions of aphasic patients that are sufficiently detailed to be informative first appeared in the late 17th century. At least nine such case reports were published before 1800--Schmidt (1673), Rommel (1683), Linn6 (1745), Dalin (1745), Gesner (1770, two cases), Spalding (1783), Herz (1791 ) and Crichton (1798) (Summaries and, in some instances, t he complete texts of these reports can be found in the review by BENTONand JOYNTI'3]). Of the nine patients, three had right-sided paralysis and a nonfluent aphasia. The other six patients had no paralysis and five of them had a fluent aphasic disorder. A reviewer of this series of cases might have noted that, when paralysis was present, it was always on the right side and never on the left. But evidently no student at that time was fortunate enough to be endowed with such serendipity. A possible distraction was the fact that medical interest in the 18th century was largely focused on patients showing the more florid forms of fluent aphasia, as reflected in jargon aphasia and"wild" paraphasic utterances, and these patients generally did not show motor disability. Three monumental treatise on clinical pathology, each of which dealt at some length with brain-behavior relationships, appeared in the 18th and early 19th centuries--Morgagni's De sedibus et causis morborum per anatomen indi#atis (1761), Bouillaud's Trait" physiolo#ique et clinique de l'encdphalite (1825) and Andral's Clinique mddicale (1829-1840). The present paper attempts an analysis of the basic data in each of these treatises with the aim of evaluating the strength of the latent evidence supporting a specific association between aphasic disorder and disease of the left hemisphere and discusses possible reasons for the failure to perceive the association. The singular story of the one man who did grasp the relationship but who elected at the time to withhold his discovery from the public will then be reviewed. MORGAGNI The first volume of Morgagni's great compilation includes numerous brief descriptions of speechlessness associated with apoplexy, head injury and fever, together with the findings at autopsy. He repeatedly emphasizes the connection between paralysis of one side of the body and the presence of disease in the opposite cerebral hemisphere. Many patients are described as speechless but more often than not the disability is noted within a context of stupor or a rapidly worsening condition resulting in death within hours. Consequently there are relatively few cases that are suitable for our analysis. From an inspection of the 1769 English translation by Benjamin Holland of De sedibus, I identified ten cases of unilateral paralysis in patients who were not comatose, stuporous or dying in whom autopsy disclosed a purely or predominantly unilateral hemispheric lesion and in whom it was possible to ascertain whether or not speech was disordered. Five patients had a right-sided paralysis and four of them were impaired in speech. Five patients had a leftsided paralysis and one was impaired in speech.

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BOUILLAUD Beginning in 1825 and for a half-century thereafter, Jean-Baptiste Bouillaud was the great champion of Gall's localization of the centers of speech and language in the frontal lobes and he argued repeatedly, vigorously and, at times, rancorously that aphasic disorder resulted only from lesions in this territory. In his TraiN... de l'encdphalite (1825), he presented 29 cases with and without aphasia and with and without lesions in the anterior, middle and posterior lobes. All of the aphasic patients had lesions that were in or close to the anterior lobes. Neither then nor subsequently could he find a valid example of aphasic disorder that was not a consequence of disease of the anterior lobes. Inspection of Bouillaud's 29 cases shows that 25 had lesions confined tO a single hemisphere, 11 in the left hemisphere and 14 in the right. Eight (73%) of the 11 left hemisphere cases were aphasic. Four (29%) of the right hemisphere cases were aphasic. Perhaps one reason why Bouillaud did not perceive this trend toward a higher frequency of aphasic disorder in his left hemisphere patients is that not only was he obsessed with the frontal lobe localization of aphasic disorder but he also accepted Gall's dual localization of the centers of speech and language in both hemispheres. Thus whether a lesion was found to be in the left or fight hemisphere was a matter of indifference to him.

ANDRAL Gabriel Andral was one of the luminaries of French clinical pathology in the 1830s and 1840s. His Clinique mddicale and Prdcis d'anatomie patholooique were widely used in France and known throughout the world in English, German and Italian translations. In Vol. 5 (Maladies de r encdphale) oftbe Clinique mddicale he addressed the question of the localization of speech disorder with special reference to the Gall-Bouillaud doctrine and presented his conclusions in the following succinct statement: M. le professeur BouiUaud a publi6, il y a d6jfi plusieurs ann6s, un m6moire rempli de faits curieux desquels il a cru pouvoir d6duire la cons6quence que la formation de la parole a pour instrument l'extr6mit6 ant&ieure de chaque h6misph&e, attendu qu'il a trouv6 cette partie 16s6e, toutes les fois que pendant la vie la parole elle-m~me avait 6t~ perdue. Voici, cet ~gard, ce que nous ont appris nos recherches. Sur trente-sept cas observ6s par nous ou par d'autres, rdatifs fi des h6morrhagies ou d'autres 16sions, dans lesquels l'alt6ration r6sidait dans un des lobules anterieurs ou dans tous les deux, la parole a 6t6 abolie vingt-et-une fois, et conserv6 seize lois. D'un autre c6t6, nous avons rassembl6 quatorze cas off il y avait abolition de la parole, sans aucune alteration dans les lobules ant6rieurs. De ces quatorze cas, sept 6taient relatifs des maladies des lobules moyens, et sept autres ~t des maladies des lobules post6rieurs. La perte de la parole n'est donc pas le r6sultat n6cessaire de la 16sion des lobules ant6rieurs, et, en outre, elle peut avoir lieu dans des cas oti l'anatomie ne montre dans ces lobules aucune alt6ration [2, p. 368]. It is quite evident from inspection of the Ciinique mddicale (4th Edition, 1840) that not all 37 cases mentioned by Andral are described in the book. I was able to identify 11 cases of unilateral disease, five with lesions in the left hemisphere and six with lesions in the right hemisphere, where the status of the patient's speech during his illness is described. Of the five left hemisphere cases, three were aphasic. Of the six right hemisphere cases, none was aphasic.

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A collaborator and admirer of P. C. A. Louis, who introduced the statistical approach into medical observation, Andral applied the latter's mdthode numdrique to his case material in evaluating Bouillaud's claims. Evidently it did not occur to him to extend its application to the question of a right-left hemisphere difference. The few lines he wrote on aphasia suggests that the topic was not of great interest to him and probably he was content with disproving t-he Gall-Bouillaud thesis. Bouillaud and Andral were polar opposites in temperament and in their approach to problems. Bouillaud was passionate, polemical and dogmatic; Andral was sober, analytic and wary of speculation. Moreover, the two men were opponents in other respects as well. Andral campaigned vigorously against the practice of blood-letting while Bouillaud was, as GARRISON [8] describes him, "a furious bloodletter" who "favored pitilessly rapid bleeding, coup sur coup". In summary, the observations reported in each of the three treatises show a trend towards a specific association between speech disorder and left hemisphere disease. However, in no single instance is the trend statistically significant, as assessed by the Fisher Exact Probability Test (two-tailed), although it approaches significance (P = 0.10) in Bouillaud's sample. If it is permissible to combine the cases in the three samples and apply a chi-square test to the data, the resulting chi-square (10.3) indicates a between-hemispheres difference which is significant at the 0.002 level. Some of the possible reasons for the failure to perceive this difference have already been noted, such as the occurrence of exceptional cases, the presence of left hemisphere disease without speech disorder and the desperate conditions of so many patients. But perhaps the most important single reason is to be found in the circumstance that these men were very busy practitioners who at the same time actively pursued numerous and varied investigative interests. None of them was a specialist in the modern sense of the term, either in their medical practice or in their research. So far as can be seen, Morgagni had no interest in aphasia beyond noting on occasion that a patient was speechless and Andral had only a passing interest which quite clearly had been aroused by Bouillaud's claims. Aphasia was a topic of major concern only to Bouillaud. Yet, when one considers his subsequent activity, it is understandable that, having embraced Galrs hypothesis of centers of speech in both frontal lobes, he proceeded to defend it vigorously without exploring the matter further. After 1825 he turned his attention to the fields of cardiology and rheumatology, to which he made a number of notable contributions, the most important of which was his demonstration of the association between rheumatic fever and endocarditis. Indeed, it was Bouillaud who introduced the terms "endocardium" and "endocarditis" into medicine [10]. Thus it is not unlikely that the major reason why the aphasia-left hemisphere association escaped the attention of Morgagni, Bouillaud and Andral is that their busy schedule and competing interests did not allow them the time to consider the data bearing on the association. It was left to a thoughtful country doctor with scholarly interests and the time to reflect on the meaning of his own observations and those of others to discover the correlation.

MARC DAX In about 1836 this physician, who practiced in Sommi6res (about 25 k from Montpellier), wrote a paper purporting to show that aphasic disorder is exclusively associated with lesions of the left hemisphere. Marc Dax was born in 1770 and died in 1837. He was thus about 66 years old when he wrote his famous mdraoire.

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It is a remarkable document. Dax describes the successive observations that led him gradually to the conviction that aphasia was the product of left hemisphere disease. An aphasic patient with w h o m he had first become acquainted in 1800 had sustained a left parietal wound. At the time this meant to Dax only that Galrs frontal lobe doctrine could not be altogether correct. In 1809 he had an aphasic patient with an extensive tumor on the left side of the face who died some months later. He attached no special significance to the circumstance that the lesion was left-sided. However, when in 1811 he read that the naturalist Broussonet had become aphasic after a left hemisphere stroke, he reflected on the fact that the three cases with which he was familiar had left hemisphere lesions. F r o m this time onward, Dax had a "prepared mind" and, when he encountered three additional cases of aphasia with presumptive left hemisphere disease over the period of 1812-1814, he formulated his hypothesis. He continued to collect cases over the ensuing 20 years, so that at the time of writing his paper he reported having a series of over 40 cases in w h o m the diagnosis of left hemisphere disease had been made, primarily on clinical grounds without pathological confirmation. It was on this empirical basis that he wrote: De tout ce qui pr6c6de, je crois pouvoir conclure, non que toutes les maladies de l'h6misph6re gauche doivent alt6rer la m6moire verbale, mais que, lorsque cette m6moire est alt6r6e par une maladie du cerveau, il faut chercher la cause du d6sordre dans l'h6misph&e gauche, et r y chercher encore si les deux h6misph&es sont malades ensemble. MARC DAX'S paper I7] was published in 1865 by his son, GUSTAV DAX 1'6], who stated that it had been read at a regional medical meeting in Montpellier in 1836. In fact there is no evidence that he did present the paper on that occasion [9]. It is not mentioned in accounts of the meeting, nor could anyone be found who remembered having heard it. It seems almost certain that, if the paper had been presented, it would not have been totally neglected and would have had some repercussions. The tone of Dax's paper is personally modest but firm in conviction. Its style indicates that it was meant to be a communication to his peers. He was quite aware of the importance of his discovery and he made one or two copies which he sent to professional friends. Why he did not make his discovery known at the time through publication or oral presentation is not clear. Perhaps he planned to publish after the collection of further data but death intervened. In any case, whether by intention or not, his manuscript became in effect a paquet cachet~ that was brought to light only after Broca's discovery. REFERENCES 1. ADAMS,F. The Extant Works of Aretaeus, the Cappadocian. The Sydenham Society, London, 1856. 2. ANOg~,L, G. Clinique mbdicale, 4th Edn. Fortin. Masson, Paris, 1840. 3. BEI~TO~q,A. L. and JOYNT,R. J. Early descriptions of aphasia. Arch. Neurol. 3, 205--222, 1960. 4. BOUmL^UD,J. B. Traitd clinique et physiologique de l'encdphalite. J. B. ,Bailli6re, Paris, 1825. 5. CHADWICK,J. and MANN, W. N. The Medical Works of Hippocrates. Biackwell Scientific Publications, London, 1950. 6. DAx, G. Notes sur ie m~me sujet. Gaz. hebd. M~d. Chit. 2, 262, 1865. 7. DAX,M. L6sionsde la moiti~ gauche de l'encephale coincidant avec I'oubli des signes de la pens6e. Gaz. hebd. Mbd. Chit. 2, 259-262, 1865. 8. GARRISON,F. H. An Introduction to the History of Medicine, 4th Edn. W. B. Saunders, Philadelphia, PA, 1929. 9. JovN'r, R. J. and BENTON,A. L. The memoir of Marc Dax on aphasia. Neurology 14, 851-854, 1964. 10. MAJOR,R. H. A History of Medicine. C. C. Thomas, Springfield, IL., 1954. 11. MORGANI,G. The Seats and Causes of Diseases Investigated by Anatomy, (trans. by B. A. ALEXANDER).A Millar and T. Cadeil, London, 1769.