Arq Neuropsiquiatr 2007;65(4-B):1220-12231220

BROCA’S APHEMIA

An illustrated account of its clinico-anatomic validity

Ricardo de Oliveira-Souza

1,2

, Jorge Moll

, Egas M.A. Caparelli-Dáquer

1,2

ABSTRACT -

Objective:

To present the case of a 54-year-old man with loss of speech, but with preservationof voluntary facio-lingual motility, language and other cognitive abilities (Broca’s aphemia).

Method:

Ob-servation of patient oral communicative abilities and general behavior, neuropsychological assessment andcranial computed tomography.

Results:

Computed tomography showed a hyperdense lesion in the sub-cortex of the left precentral gyrus corresponding to Brodmann’s area 6 and 44. Neuropsychological assess-ment confirmed that the major cognitive domains were intact.

Conclusion:

Our patient reiterates the va-lidity of Broca’s aphemia as a clinico-anatomic entity allowing us to portray it for the first time in pictures.From a neurobehavioral perspective, aphemia is related to apraxia rather than to aphasia, a fact that mayhave hampered the full grasp of its far-reaching implications for neurology and aphasiology.KEY WORDS: aphemia, Broca’s area, Broca’s aphasia, apraxia.

Afemia de Broca: um relato ilustrado sobre sua validade anátomo-clínica

RESUMO -

Objetivo:

Apresentar o caso de um paciente de 54 anos de idade com perda da fala, mas pre-servação da linguagem, das demais capacidades cognitivas, e da motilidade fácio-lingual voluntária (afe-mia de Broca).

Método:

Observação da capacidade de comunicação oral e do comportamento geral, exa-me neuropsicológico e tomografia computadorizada do crânio.

Resultados:

A tomografia computadori-zada revelou lesão hiperdensa no subcórtex do giro precentral esquerdo correspondendo às áreas 6 e 44 deBrodmann. O exame neuropsicológico confirmou que os principais domínios cognitivos se encontravam in-tactos.

Conclusão:

Nosso paciente reiterou a validade da afemia de Broca como entidade anátomo-clínicopermitindo documentá-la em fotos pela primeira vez. Da perspectiva neurocomportamental, a afemia estávinculada às apraxias e não às afasias, o que pode ter prejudicado a apreensão plena do seu profundo sig-nificado para a neurologia e para a afasiologia.PALAVRAS-CHAVE: afemia, área de Broca, afasia de Broca, apraxia.

Hospital Universitário Gaffrée e Guinle, Rio de Janeiro RJ, Brazil;

Cognitive and Behavioral Neuroscience Unit, LABS - D´Or Hos-pitals Network, Rio de Janeiro RJ, Brazil.Received 27 July 2007. Accepted 22 September 2007.

Dr. Ricardo de Oliveira-Souza - Rua Conde de Bon

ﬁ

m 232 / 304 - 20550-012 Rio de Janeiro RJ - Brasil. E-mail: rdeoliveira@gmail.com

Pierre Paul Broca (1824-1880) coined the term“aphemia” for the loss of speech without impair-ment of language in patients with left frontal lobedamage

. As shown in the passage below, Broca wasmostly impressed by retained ability of such patientsto move the faciolingual territories employed inspeech:“There are cases where the general language fac-ulty persists unaltered, where the auditory appara-tus is intact, where all the muscles, not even except-ing those of the voice and those of articulation, obeythe will, and yet where a cerebral lesion abolishes ar-ticulated language. This abolition of speech (…) con-stitutes a symptom so singular that it seems to meuseful to designate it with a special name (…) aphe-mia (

deprive

;

ϕηµι

I speak, pronounce

); it is onlythe faculty of articulating words that these patientslack. They hear and comprehend all that one says tothem; they all have their intelligence; they emit vo-cal sounds with ease; they execute with their tongueand their lips movements much more extensive andenergetic than those required for the articulation ofsounds, and yet the perfectly sensible response thatthey would want to make is reduced to a very smallnumber of articulated sounds, always the same andalways performed in the same manner (…)”We report on a case of aphemia very similar tothe one Broca described on patient Lelong

. To ourknowledge, this is the first pictorial illustration ofthe amazing preservation of voluntary motor pow-er in the faciolingual territories employed in speechin a speechless patient. This dissociation rests at the

Arq Neuropsiquiatr 2007;65(4-B)1221

Broca’s aphemiaOliveira-Souza et al.

root of most inferences on the existence of a cerebral“speech center” apart from motor “centers” relat-ed to the production of voluntary faciolingual move-ments unrelated to speech.

CASE

A 54-year-old right-handed (Edinburgh Inventory=100)waiter with 8 years of formal education lost the ability tospeak and swallow on the evening before consultation. Hisability to swallow rapidly returned to normal, but he re-mained speechless and unable to spontaneously generateand repeat even single words, although he retained theability to vocalize a sound resembling an “Ah…” Althoughhe strived to articulate consonant and other vowel sounds,he was absolutely unsuccessful. He did not present verbalstereotypies or recurring utterances. He nonetheless com-municated by gestures and writing, and by soliciting theaid of his wife and daughters to convey what he meant. Hewas oriented to time and place, and understood oral andwritten language perfectly. He could write meaningful sen-tences, both spontaneously and on dictation, with correctorthography and spelling. Figure 1 (bottom) shows a sam-ple of the patient’s handwriting and a freehand copy oftwo intersecting pentagons. He could sit, stand, and walk,and execute complex orofacial and limb movements in re-sponse to verbal and gestural (visuo-imitative) commands[Florida Apraxia Screening Test = 15/15

]. At rest, sponta-neous blinking was symmetric, but the lower face deviat-ed slightly to the left (Fig 1A). On command, he contractedthe frontalis, corrugator, and orbicularis occuli (Fig 1B). Hisability to pucker the lips (Fig 1C) contrasted with his inabil-ity to retract or lift the right corner of the mouth (Fig 1D).The tongue was trophic and without fasciculations (Fig 1E).The soft palate and tongue did not deviate at rest or dur-ing movement. There was no emotional incontinence. Fun-doscopy and eye movements were normal. He had no his-tory of hypertension or diabetes, the heart rate was regularand the blood pressure was 130x80 mmHg. He denied fe-ver, headache, visual symptoms, dizziness, incontinence, andfainting. He fared normally on the Mini-Mental State Exam(28/30), Token Test (33/36), Right-Left Orientation (20/20), 3DBlock Construction (29/29) (Fig 1F), Visual Form Discrimina-tion (28/32), Judgment of Line Orientation (19/30), and theVisual Organization (26/30) tests

. On the Wisconsin CardSorting test he completed one category and committed 23perseverative errors. He scored 24/36 (normal

≥

25/36) on theTower of London task

. Figure 1K shows a sample of spon-taneous handwriting, Figure 1H shows a freehand copy ofintersecting pentagons. CT (10 mm slices, parallel to the or-bito-meatal line) showed a hyperdense egg-shaped lesionsurrounded by a thin hypodense hallo in the subcortex ofthe left lower precentral gyrus exerting a slight mass effecton surrounding regions (Fig 1I). The lesion spared the in-sula, the temporal lobe, and the medial hemispheric wall,suggestive of a lobar hematoma in the subcortex of Brod-mann’s areas (BA) 6 and 44

. Written informed consent wasobtained from the patient to publish his pictures. He dieda few days later of an acute myocardial infarction beforecompletion of further tests.

DISCUSSION

The relevant

ﬁ

ndings of this case were (i) the lossof speech with preservation of voice, language andcognition, with (ii) relative sparing of faciolingual mo-tility and praxis, and (iii) the location of the lesion.Our patient presented loss of speech in the absenceof proportional faciolingual paralysis and aphasia. Hedid not develop agraphia, alexia, and apraxia – in par-

Fig 1. (A) Deviation of the lower face to theleft at rest. (B) Contraction of the corru-gator and frontalis muscles on verbal com-mand. (C) Retained ability to pucker thelips contrasting with (D) the impossibili-ty to retract or lift the right corner of themouth. (E) Normal trophism and strengthof tongue. (F) Flawless performance onthe 3D Block Construction Test (the insert shows the model to be reproduced by pa-tient). (G) A sample of spontaneous hand-writing: “I love God and my family”. (H)Freehand copy of intersecting pentagons.(I) Computed tomography suggestive of subcortical hemorrhage in the left poste-rior inferior frontal gyrus.

Arq Neuropsiquiatr 2007;65(4-B)1222

Broca’s aphemiaOliveira-Souza et al.

ticular, faciolingual praxis was preserved,

provided hewould not attempt to speak

. The clinical manifesta-tions of this case represent a typical instance of aphe-mia as described by Broca on patient Lelong

. Thusde

ﬁ

ned, aphemia must be differentiated from a hostof conditions that compromise

ﬂ

uent speech. At theoutset we would like to emphasize that, since our pa-tient could still produce vocal sounds, we did not con-sider him to be “mute”, a term that usually implies aninability to produce articulation

and

voice. The facialdeviation could lead to an erroneous impression of

Bell’s palsy

, which was discarded by the dispropor-tional affection of speech, the bilateral preservationof spontaneous blinking and the ability to close theeyes.

Suprabulbar paralysis

consists of impairment ofvoice, articulation, lower face motility, and swallow-ing with preservation of trophism and re

ﬂ

exes in theaffected territories, most often caused by multiplecerebral infarcts. The latter differentiate suprabulbarfrom the

bulbar paralysis

of motor neuron disease,marked by lingual and masticatory atrophy and ar-reflexia. Thus, even conceding that the dysphagiaof our patient might have represented a fragmentof a suprabulbar paresis at the onset of symptoms,the severe speech de

ﬁ

cit could not be attributed tointerruption of corticobulbar fascicles. A

non-

ﬂ

uent aphasia

was altogether discarded by the intactnessof language, as de

ﬁ

ned by the ability to comprehendand express ideas and thoughts by means other thanby articulated speech. Finally, the typical “misarticu-latory symptoms among areas of

ﬂ

uent speech” de-scribed in cases of damage to the precentral gyrus ofthe insula

were conspicuously absent.The lesion responsible for aphemia is typicallyseated in the opercular division of the inferior frontalgyrus (“Broca’s area”, BA 44)

. Lesions of the opercu-lar cortex or of the short cortico-cortical

ﬁ

bers issuingfrom it lead to “true” aphemia because they impairspeech without compromising language, faciolingualmotility, and the ability to produce vocal sounds. Thiswas the case in our patient and in two others report-ed in the recent literature

9,10

. In contrast, lesions ofthe lower precentral gyrus, where the cranial mo-tor territories are represented, that spare the frontaloperculum impair speech due to “anarthria”

[Case2], a term that should be reserved for paralysis frominterruption of corticobulbar pathways

. In practice,lesions are seldom small enough to produce pureaphemia or pure anarthria. Most often, variable com-binations of aphasia, aphemia and anarthria producecomplex impairments of oral language output thatmay be inadvertently taken as unique. A systematicassessment of such cases will often show that they

ﬁ

tcurrent concepts of the anatomical organization ofthe anterior language zone.The left frontal operculum is composed of hetero-modal (“association”) cortex lying at the interface oflanguage and speech. It sends short projections tothe adjacent motor cortex, where the corticonuclearneurons responsible for the integration betweenarticulation and voice are ultimately recruited. Thefrontal operculum contains the kinetic formula (

Be-wegungsformel

) responsible for the automatic con-version of verbal language, a cognitive phenomenon,into speech, the product of the motor innervation ofthe articulatory muscles. The aphemia in our patientprobably resulted from a lobar hematoma in the leftfrontal lobe. Coincidentally, aphemia in Lelong maylikewise have resulted from an identical hemorrhage,both in size and in shape (“Il s’agit donc d’un

ancienfoyer apoplectique

”

). Ruff and Arbit

described a 15-year-old girl who developed aphemia after evacuationof a hematoma in the left precentral gyrus and frontaloperculum. To our knowledge, these are the only in-stances of aphemia due to intracerebral hemorrhage.The diagnostic value of the status of faciolingualmotility in the differentiation of aphemia (frontaloperculum) and anarthria (lower precentral gyrus andits efferent pathways) has seldom been emphasized.Nevertheless, the relative preservation of faciolingualmotility constituted the most interesting

ﬁ

nding inour patient, as it provided a fresh insight into themechanism of aphemia. The impairment of learnedmotor actions that manifests itself in certain behav-ioral contexts but not in others is a core feature ofapraxia

13,14

. Conceptually, then, the aphemia of ourpatient represented a particular instance of apraxia,namely, an apraxia of speech. The relationship be-tween aphemia due to injury of the left precentralgyrus of the left frontal lobe and the articulatory syn-drome that results from lesion of the left precentralgyrus of the insula

remains to be determined

. Therecognition of aphemia as a discrete neurobehavioralsyndrome provides a natural solution for inconsisten-cies that have confounded aphasiology for decades.Our case also underscores the validity of Broca’s aptdistinction between speech (“le langage articulé” or,more simply, “la parole”) and language (“la facultégénérale du langage”) and his contention that whatwas lateralized to the left hemisphere was speechonly. For him, language was a non-localizable facultythat was equipotentially supported by both cerebralhemispheres