Speech and language functions that depend on Broca’s area

Cameron Davis, Jonathan T. Kleinman, Melissa Newhart,Jennifer Heidler-Gary, Argye E. Hillis *

Johns Hopkins University School of Medicine, Department of Neurology, USA

Accepted 6 July 2006

Introduction

Functional imaging and studies of chronic aphasia have indicated animportant role of Broca’s area in various speech and language functions.For example, Grodzinsky (2000) has claimed that Broca’s area is essentialspecifically for creating and maintaining traces or chains of movement inmovement-derived (e.g., passive and object-relative clause) sentences. Oth-ers argue that this area is more generally required for thematic role assign-ment or for verbal (semantic or phonological) working memory. Mostlesion studies designed to evaluate the language functions that are depen-dent on Broca’s area have studied patients with chronic Broca’s aphasia,who often have large lesions (that may involve but are not limited to Bro-ca’s area), and who may have recovered language functions that were ini-tially impaired. Functional imaging studies can show that Broca’s area isengaged in a process, but not that it is essential for the process. Our goalwas to identify language functions that are impaired when Broca’s area isdysfunctional (due to low blood flow) and immediately recover when Bro-ca’s area becomes functional again (due to restored blood flow). Thisopportunity was provided by a patient with hyperacute stroke whoshowed selective hypoperfusion, with minimal infarct, in Broca’s area.We tested the hypothesis that temporary dysfunction (due to hypoperfu-sion) of Broca’s area would result in impairment of selective processes,and reperfusion of Broca’s area would result in recovery of theseprocesses.

Subject

A 67-year-old, dextral man with atrial fibrillation developed suddenmuteness at 4 AM, the day after a surgical procedure. He was examinedby the neurologist 34 min after onset. Due to recent surgery he couldnot have intravenous thrombolysis. On examination, he was initially mute,but within an hour began to articulate words and phrases with numerousand varied off-target attempts, particularly with polysyllabic words (e.g.,hospital-> [taspIdcl]. . .[hastIbcl]) despite normal strength, rate and rangeof movements of the muscles of articulation. He described the ‘‘cookietheft’’ picture as ‘‘kis-kitchen—in kitchen. . .picture. The laundry runningover. The kid on the thing.’’ He accurately followed simple commands. He

could not form letters to write. The remainder of his neurological exami-nation was normal.

After an MRI scan showed an area of hypoperfusion that was notinfarcted, he was treated with intravenous saline to increase his bloodpressure, to increase blood flow to the ischemic region.

Methods

Lexical tests included: oral and written naming, oral reading, spellingto dictation, and repetition, with items matched in word length and fre-quency across tasks and versions of each task (given on separate days).He was also administered two film clip/sentence verification tests; onewith auditory and one with written sentences. Each of 13 film clipsdepicted a semantically reversible subject–verb–object relationship (e.g.,the man pushed the girl). Each film clip was presented four times incounterbalanced order with: correct active sentence; correct passive sen-tence; incorrect active sentence; and incorrect passive sentence (semanti-cally reversed forms), intermixed with other stimulus pairs. In anothertest, printed object-relative clause sentences were presented with homo-phonic pictures, depicting different meanings of the verb following theobject-relative clause. The trace deletion hypothesis (Grodzinsky, 2000)predicts that patients with deficits in maintaining traces in movement-de-rived sentences should misunderstand these verbs as nouns. For example,the written sentence, The teacher that the girl likes rings the bell was pre-sented with a picture of rings and picture of ringing a bell. He was askedto point to the picture matching the meaning of the underlined word.Finally, 10 auditory yes/no questions were presented (e.g., ‘‘Does a tigerhave spots?’’).

Language tests were administrated at 5 h post-onset of symptoms(pre-treatment), and again 32 h post-onset of symptoms (post-treatment).MRI scans were obtained at 4 h post-onset and again 36.5 h post-onset.MRI sequences included diffusion weighted imaging (DWI), which ishighly sensitive to infarct in the first hours of stroke, and perfusionweighted imaging (PWI), which shows areas of poor perfusion (lowblood flow).

Results

Day 1 testing (before intervention)

Excluding self-corrected articulatory errors, he had mild impairment oforal naming (88.2% correct; normal mean = 98.3 ± 4.0), and scored nor-

doi:10.1016/j.bandl.2006.06.080

* Corresponding author. Fax: +1 410 614 9807.E-mail address: argye@jhmi.edu (A.E. Hillis).

www.elsevier.com/locate/b&l

Brain and Language 99 (2006) 8–219

mally on oral reading of words and pseudowords (96.6%;mean = 96.5 ± 5.6) and repetition of words and pseudowords (96.6% cor-rect). He was 100% correct in answering simple yes/no questions (e.g., Dodogs fly?) and 91.7% correct in comprehension of object-relative clausesentences. However, on auditory sentence/film clip verification withsemantically reversible sentences, he scored 61.5% correct for passive sen-tences and 65.4% correct for active sentences. On written verification hewas 42.3% correct for passive and 53.8% correct for active sentences.Finally, he was unable to form letters, and had a moderate impairmentin oral spelling to dictation (75.9%; mean = 98.4% ± 4.2).

Day 1 DWI showed only a tiny infarct in the superficial cortexwithin Broca’s area. PWI showed severe hypoperfusion in the Broca’sarea.

Day 2 testing (after intervention)

Performance on all tests and spontaneous speech were normal. Hescored 100% on all lexical tests except repetition (98.3% correct), and osraland written spelling to dictation (both 94.8% correct; mean =98.4% ± 4.2). He was 100% correct on auditory and written sentence/filmclip verification for passive and active sentences, yes/no questions, andsentences with object-relative clauses.

Day 2 DWI and PWI showed complete reperfusion of Broca’s area andminimal extension of the tiny stroke (Fig. 1).

Conclusion

Acute hypoperfusion of the Broca’s area was associated with severeimpairment in comprehension of active and passive semantically reversiblesentences, and moderate impairment of motor speech, grammatical sen-tence production, and spelling. Restoration of normal blood flow to Bro-ca’s area resulted in immediate recovery of these functions. This caseprovides direct evidence for an essential role of Broca’s area in under-standing and producing sentences, before reorganization or recovery.Impaired comprehension of both active and passive semantically revers-ible sentences, with relatively preserved comprehension of object-relativeclause sentences without semantically reversed foils indicates a generalproblem with thematic role assignment or working memory.

Reference

Grodzinsky, Y. (2000). The neurology of syntax: Language use withoutBroca’s area. Behavioral and Brain Sciences, 23, 1–71.

Fig. 1. DWI and PWI before intervention (Day1) and after intervention (Day 2). (A) DWI (upper panel) and PWI (lower panel) obtained at 4 h post-onsetof symptoms (pre-treatment). PWI show substantial hypoperfusion within Broca’s area. (B) DWI and PWI obtained again at 36.5 h post-onset ofsymptoms (post-treatment). Black arrows point to Broca’s area.

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