The pathology of sensory aphasia, with an analysis of fifty cases in which Broca's centre was not diseased. By M. Allen Starr, MD. Brain 1889: 12; 82–99; with A remarkable case of aphasia. Acute and complete destruction by embolic softening of the left motor-vocal speech centre (Broca's convolution), in a right-handed man: transient motor aphasia, marked inability to name objects and especially persons, considerable agraphia and slight word-blindness. By Byron Bramwell, MD. Brain 1898: 21; 343–373; and Recent work on aphasia. By James Collier, MD. Brain 1909: 31; 523–549.
Elsewhere in this issue, Dronkers et al. report on high-resolution MR scanning of the brains of the two patients on whom Paul Broca in 1861 based his famous theory about the localization of language production in the posterior inferior frontal gyrus. They report that the lesions extend beyond what has become conventionally known as ‘Broca's area’, in a medial as well as in an anterior direction. In the three Brain papers published in the decades after Broca's discovery, the discussion revolves not only around the exact location of the lesions associated with motor aphasia, but also around the question whether different aspects of language (interestingly called ‘speech’ in all three papers) can be localized at all. In this sense the debate echoes and parallels the controversy in the second half of the 19th century about localization of brain function in general: localizationists versus equipotentialists, Gall versus Flourens, Ferrier versus Goltz.Starr, writing from New York, is emphatically in the camp of the diagram-makers. He reviews 50 published clinico-anatomical case reports describing several varieties of sensory aphasia, excluding cases in which the lesion involved Broca's area or the Island of Reil (insular cortex). To start with, he points out that pure word deafness always results from a lesion in the posterior two-thirds of the first or second temporal convolution on the left side of the brain. Impairment of the ability to name objects, however, can result from lesions in different parts of the posterior part of the left hemisphere: angular gyrus, occipital lobe, temporal convolutions, inferior parietal region, or supramarginal gyrus. Starr explains this apparent unpredictability by pointing out that for the name of an object to be recalled, ‘the concept of the object in the first place must be brought to mind, and this is made up of the various residua of perceptions by various senses’. He illustrates this with Charcot's example of the bell, an object with many possible associations (Fig. 1). ‘To name the bell on seeing it is to revive one association; to name it on hearing its ring is to call up another association; and to tell the name of an object felt but not seen or heard, requires the passage of an impulse along still a third tract.’ In a footnote he adds that he has a patient under observation who, though able to name things seen or heard, cannot give the name when the object is felt. In other words, the statement that a patient is unable to recall words is imprecise—it depends on the sensory route, on whether the object is seen, heard, felt, smelt or tasted. The lesion should be in the corresponding association tract in the subcortical white matter. Similar reasoning is applied to the inability to recognize objects that are seen, apart from naming them.
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Starr concludes that ‘... in addition to these numerous and various memory pictures associated together there seems to be no reason to hypothecate the existence of an idea, or to suppose any ideational centre’. In other words, for each sense organ there would be a set of object representations in the brain—a visual bell, an auditory bell, a tactile bell, etc. (Fig. 1).
Nine years later Byrom Bramwell writes from Edinburgh: ‘It is, I think, no exaggeration to say that the case which I am about to relate is one of the most remarkable cases of aphasia which have ever been recorded, and that it is of very great importance from a physiological and a pathological point of view.’ The patient, a 70-year-old right-handed business man, suffered a stroke 6 weeks before he died from what turned out to be mesenteric artery thrombosis. The neurological deficits persisting in that interval were a striking inability to name persons and objects, whereas spontaneous speech became normal after the first few days, as did repetition of spoken language. Writing was initially affected but recovered to a large extent, reading was more or less normal but the patient made mistakes on reading aloud.
Bramwell suspected the lesion would be ‘in the neighbourhood of the visual speech centre’, but on postmortem examination he was greatly surprised to find an area of softening that involved more or less precisely the cortex of the posterior end of the lower (third) left frontal convolution, in other words Broca's area (Figs 2 and 3). He cannot think of a better explanation than ‘that the function of the left motor-vocal speech centre was taken up and carried on by the motor-vocal speech centre in the right hemisphere of the brain’, although he has to admit ‘that I have very great difficulty in giving a satisfactory explanation of the patient's inability to name persons and objects’. In contrast to Starr—whom he does not cite—Bramwell apparently assumes that any intellectual activity takes place only in the neurones of the cortical mantle.
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Another 10 years later, James Collier addresses the scientific controversy that had broken out in Paris between Pierre Marie and Jules Dejerine, about the localization of language functions—in fact the matter was complicated by a personal feud. Marie denied the existence of a motor speech centre and argued that there is only a single language centre, more or less corresponding to Wernicke's area in the left temporo-parietal area, a centre encompassing all intellectual aspects of language, not just ‘sensory images’. In his view the classical aphasia of Broca was a combination of aphasia with anarthria, the aphasia resulting from a lesion in Wernicke's area, the anarthria from a lesion within a quadrilateral area involving the lenticular nucleus and the insular cortex. In contrast, Dejerine vehemently championed the ideas of the old school. Collier remonstrates by referring (without direct citation) to ‘an unusual number of cases in which the third left frontal convolution had been destroyed without the appearance of aphasia’, while he is not fully convinced by the theory of ‘gaucherie’ and transference. On the other hand he criticizes Marie's localization in the quadrilateral area by pointing out the many connections through the white matter in that area with cortical areas in the frontal and temporal lobes. Yet finally he comes off the fence mostly on Marie's side: ‘The speech centre is localized as one centre in the left temporo-parietal region, and this centre is an intellectual centre specialized for speech, not a sensory centre for the storing of sensory images ... Strict and narrow localization of function in the cerebral cortex is, in all probability, an erroneous idea’.
Eventually, the notion of connecting white matter tracts in the production and recognition of language proposed by Starr and before him by Lichtheim (On aphasia. Brain 1885; 7: 433–484; and see Brain 2006; 129: 1347–1350) would be revived by Norman Geschwind (Disconnexion syndromes in animals and man. Brain 1965; 88: 237–294 and 585–644). The realization that cortical lesions can be bypassed if subcortical connections are intact helps to understand the clinico-anatomical correlations in Broca's patients (motor aphasia by cortical as well as subcortical damage to the left posterior third frontal convolution, as once again emphasized by Dronkers and colleagues) as well as in Bramwell's patient (cortical lesion of Broca's area alone, with preserved spontaneous speech). Marie, and Collier in his wake, have rightly alluded to the role of the basal ganglia in the programming of complex movements, including articulation. After all, is there a fundamental difference between mastering the art of skating or playing the cello and that of fluently pronouncing ‘West Register Street’?
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