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doi:10.1111/ncn3.

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ORIGINAL ARTICLE

Does a lesion in Broca’s area cause apraxia?


Natsuko Tsuruya,*,†,‡ Mutsutaka Kobayakawa,*,§ Akinori Futamura,* Azusa Sugimoto* and Mitsuru
Kawamura*
*Department of Neurology, Showa University School of Medicine, Tokyo, †Laboratory of Pharmacognosy & Phytochemistry, School of
Pharmaceutical Sciences, Showa University School of Medicine, Tokyo, ‡Practical Engineering Education Program, Academic Foundations
Programs, Kanazawa Institute of Technology, Ishikawa, and §Brain Science Institute, Tamagawa University, Tokyo, Japan

Key words Abstract


action, Broca’s area, ideomotor apraxia, Background and Aim: Broca’s area, which comprises the inferior frontal gyrus and
intransitive gesture, transitive gesture.
its surrounding regions, is associated with language function. Recent functional
imaging studies showed that it is also related to processing goal-directed
Accepted for publication 21 November 2012.
actions.This study aimed to determine the types of action disorders that occur
after damage to Broca’s area.
Correspondence
Mitsuru Kawamura, MD, PhD, Department of
Methods: Here, we report four patients with left inferior frontal lesions that
Neurology, Showa University School of
included Broca’s area. The patients did not exhibit severe language comprehension
Medicine, 1-5-8 Hatanodai, Shinagawa-ku, impairment or paralysis that affected the apraxia testing. The patients were asked
Tokyo 142-8666, Japan. Email: kawa@med. to perform intransitive gestures in response to verbal commands, imitate intransi-
showa-u.ac.jp tive gestures, perform transitive gestures in response to verbal commands, perform
transitive gestures in response to visual objects, imitate transitive gestures, and use
tools.
Results: All patients exhibited impaired gestures in response to verbal commands,
while the performances regarding imitation and actual tool use were better. An
error pattern analysis showed that the patients predominantly made spatial action
errors. This pattern corresponds to the classical definitions of ideomotor apraxia.
Conclusion: These results indicate that Broca’s area mediates action production
and that a lesion in this area can cause ideomotor apraxia. Although we should be
cautious about the influence of aphasia, we believe that the comprehension deficit
observed in our patients cannot account for their apraxic syndromes. Because the
deficit was seen mainly for verbal commands, damage in Broca’s area may have
disrupted the association between verbal and action domains.

the action was performed by the left or the right hand.11


Introduction Traditionally, lesion studies investigating the neural corre-
The posterior part of the left inferior frontal gyrus is known lates of limb praxis focused on the left parietal lobe.12
as Broca’s area and is regarded as the centre of speech pro- Assuming that Broca’s area is involved in various aspects of
duction and other aspects of language.1–3 Recent studies indi- action, its damage may impair various aspects of action.
cate that Broca’s area is engaged not only in language, but However, no research has investigated this issue. In the tra-
also in action.4 Previous functional imaging studies indicated ditional classification of apraxia, impaired tool use is classi-
that Broca’s area is involved in various aspects of action, fied as ideational apraxia (or conceptual apraxia) and
including execution, observation, imitation, mental simula- impaired pantomiming is classified as ideomotor apraxia.13–15
tion, planning, and naming.5–7 In addition, this area is Ideational apraxia often involves the misuse of tools, charac-
thought to play a role in coding an action goal in an abstract terized by a well-performed action that is appropriate to an
way, rather than in coding the exact details of the motion. object different from the target (semantic error), while ideo-
The type of action disorder that occurs after damage to motor apraxia involves errors in the direction, size and other
Broca’s area is unclear. Action disorders have been studied aspects of an action.15,16 Because Broca’s area is involved in
in the context of apraxia, which is a deficit of skilled goal- many aspects of action, symptoms of both ideational and
directed action that cannot be attributed to difficulties in ideomotor apraxia might be expected if this region is dam-
language or sensory or lower motor functions. Since its aged. If Broca’s area is involved in selecting a set of actions,
introduction by Liepmann,8 apraxia has been associated then an apraxia test may yield semantic errors. If it is
mainly with left-hemisphere lesions,9,10 regardless of whether involved in the articulation of the elemental movements that

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ª 2013 Japanese Society of Neurology and Wiley Publishing Asia Pty Ltd
Broca’s area and apraxia N Tsuruya et al.

make up an action, then spatial errors might be expected in rior frontal gyrus. A single-photon emission CT (SPECT)
apraxia testing. In addition, because Broca’s area is involved scan taken 10 days after admission showed decreased blood
in imitating action, damage to this site may impair such imi- flow at the same site as that found in the CT scan. No
tation. changes in the lesion were observed.
In this study, we investigated the effect of lesions in Neurological findings: On admission, the patient was alert
Broca’s area on apraxia. There are few reports of such and cooperative. He did not show sensory deficits or difficul-
apraxia. This may be because previous studies did not antic- ties with motor coordination. He did not have hemiplegia.
ipate that a lesion in Broca’s area would cause apraxia or Neuropsychological findings: The patient’s score on the
because apraxia testing was difficult or impossible because Mini-Mental State Examination (MMSE) was 12/30 (points
of the presence of a language disorder and hemiparesis in lost for orientation regarding time, calculation, delayed
these patients. Moreover, the effect of the presentation and recall of a phrase, repetition, written instruction and mim-
response modalities on apraxia is unclear. In the study per- icry). This low score was largely because of aphasia. He
formed by Goldenberg et al.,17 which indicated a relation- had impaired fluency, repetition and naming on the Wes-
ship between pantomime ability and the inferior frontal tern Aphasia Battery (WAB).18 In the WAB, his score on
gyrus, the authors used pantomime of tool use and imitation fluency was 2/10. His speech was nonfluent and he often
of meaningless gestures to test praxis ability. Because the used stereotypical phrases to respond, indicating poor word
apraxic syndrome can vary depending on the presenting finding and sentence production. His score on auditory
modality (verbal or visual), contents of action (intransitive comprehension could not be calculated because the task
or transitive), and response style (pantomime, imitation, or was not completed, but he was able to point at named
actual use), the effect of these factors on apraxia should be objects and answer questions using “yes” or “no.” His
examined. Here, we report four cases with lesions in the left score on repetition was 1.4/10, indicating that he was able
inferior frontal regions, including Broca’s area. We exam- to repeat words, but not sentences. His naming score was
ined apraxic syndrome in these patients using both intransi- 3.3/10, which was mainly due to the presence of phonologi-
tive and transitive gestures with visual and verbal cal paraphasia. On the standard language test for aphasia
presentation and using pantomime, imitation and actual tool (SLTA, which is a standardized Japanese test for apha-
use. sia),19 he scored 10/10 and 9/10 points in comprehending
words and short sentences, respectively, but had difficulty
obeying verbal commands (1/10 points on this aspect). He
Methods
had severe Broca’s aphasia, alexia with agraphia, buccofa-
Patients. We examined four patients with inferior frontal cial apraxia and ideomotor apraxia. A similarly strong
damage. Three had cerebral infarction, whereas the other impairment in reading was observed; this was more promi-
had a brain tumor. None of the patients had severe lan- nent for Japanese kana (syllabic system) than it was for
guage comprehension impairment and paralysis of both kanji (Chinese characters). The patient presented with orol-
hands was either nonexistent or mild. inguofacial apraxia, having difficulty with actions like whis-
tling and sticking the tongue out. The behavioral symptoms
Patient 1. This patients was a 79-year-old right-handed man that are associated with a frontal or callosal lesion were
who was a regular patient of the Division of Thoracic and not observed.
Cardiovascular Surgery of Showa University Hospital,
Tokyo, Japan, for atrial fibrillation. Patient 2. The patient was a 69-year-old right-handed man.
History of the present illness: While out, the patient was History of the present illness: Upon awakening, the patient
suddenly unable to speak and came to our facility for emer- had difficulty forming words and went to work in this state;
gency treatment. Head computed tomography (CT) scans however, he visited the Department of Neurology of our
obtained a few hours after the onset of the speaking impair- hospital for a consultation when the symptoms persisted.
ment revealed a low-absorption area. Electrocardiography Head CT scans showed a low-absorption area in the left
showed atrial fibrillation and a cerebral embolism was sus- frontal lobe and he was admitted with a diagnosis of cere-
pected. CT scans obtained on the following day showed bral infarction. Transesophageal echocardiography showed
absence of hemorrhaging. Fourteen days after the onset of an ulcerative plaque in the aortic arch; therefore, he was
the speaking impairment, convulsions occurred on the right diagnosed with arteriogenic embolism. His progression was
side of his face and in the upper and lower extremities; how- favorable and he was discharged 13 days after the onset of
ever, his progression thereafter was favorable and 55 days symptoms.
after onset of the symptoms, he was transferred for rehabili- Neuroradiological findings: Head CT scans obtained on
tation. This patient had developed an acute cardiac infarc- the day of onset of symptoms showed an indistinct cortico-
tion at age 60 and underwent coronary artery bypass graft medullary border region in the left frontal lobe. Head mag-
surgery at the age of 77 years. netic resonance imaging (MRI) taken 2 days after the onset
Neuroradiological findings: Head CT scans acquired on of symptoms showed an acute-phase infarct in the middle
the day of admission showed a comparatively localized cerebral artery region, centered on the opercular part of the
lesion centered on the orbital part of the left inferior frontal left frontal lobe and inferior frontal cortex. A head MR
gyrus and extending primarily to the middle frontal gyrus. angiogram (MRA) obtained on the same day did not show
The extension also included the triangular part of the infe- any obstruction or stenosis in the major blood vessels.

56 Neurology and Clinical Neuroscience 1 (2013) 55–62


ª 2013 Japanese Society of Neurology and Wiley Publishing Asia Pty Ltd
N Tsuruya et al. Broca’s area and apraxia

Neurological findings: The patient was lucid and alert. His and son-in-law from her home, where she had been living
sensory systems and coordinated movement were normal alone. For the next 10 days, she was unable to form words
and no motor paralysis was observed. or to use the television remote control; therefore, she visited
Neuropsychological findings: Immediately after the onset the Department of Neurology of our hospital and was
of the speaking impairment, severe motor aphasia was admitted. Head CT scans showed a low-absorption area in
observed and the patient had difficulty naming objects and the left frontal and temporal lobes and cerebral infarction
repeating phrases; however, this gradually improved. Part of was suspected. After 2 weeks, she was transferred to the
the SLTA19 was performed 7 days after the onset of symp- Neurosurgery Department and underwent brain tumor
toms and he scored 8/10 points in comprehending words resection surgery, as the presence of a brain tumor was also
and short sentences, but was unable to obey verbal com- possible.
mands (0/10 points). Naming objects (8/20 points) and Neurological findings: The patient was lucid and alert. Her
explaining actions (5/10 points) were moderately impaired sensory systems and coordinated movement were normal
and his speech was laborious. Repetition was also effortful and no motor paralysis was observed.
and was better regarding words (8/10 points) than sentences Neuropsychological findings: The patient had severe motor
(2/5 points). The patient presented difficulty reading and aphasia. Part of the WAB was performed. Her fluency score
writing, particularly Japanese kana. There was no orolinguo- was 9/20, with reduced words and impaired word recall, but
facial aphasia. normal speed and prosody. She had difficulty naming
objects without a cue effect, showing hesitation and persev-
Patient 3. The patient was an 87-year-old right-handed eration, but no paraphasia. Her score on auditory compre-
woman. hension was 4.6/10. She had difficulty understanding
History of the present illness: This patient lived alone. Her complex sequential commands, but could answer simple
family called and noticed that she was stumbling over her questions correctly using “yes” or “no.” She was also able
words. They visited her the next day and found that she to understand daily objects by name and pointed correctly
could not speak well; therefore, she was admitted to our hos- at the named objects. However, errors were frequently
pital. During the examination, she was unable to state her observed in pointing at pictures and body parts. Her repeti-
name, the date or location. A head CT scan showed hemor- tion and naming scores were 3.2 and 2.7, respectively. She
rhagic infarction in Broca’s area; thus, she was hospitalized. could only repeat short sentences. The patient also exhibited
Neuroradiological findings: CT scan showed a low-absorp- difficulty reading and writing both kanji and kana. She was
tion area that appeared to be a hemorrhagic infarction in able to read and write single letters, but had trouble with
the left frontal lobe. MRI and MRA obtained 2 days later words.
showed a high-signal region presumed to be an acute-phase
infarct in the left frontal lobe cortex/white matter. The bilat- Lesion analysis. MRI was performed for all patients,
eral corona radiata level of the deep white matter showed a with the exception of patient 1, who underwent CT scan
patchy high-signal area that appeared to be due to age- because of his heart pacemaker. MRI was performed at
related changes, while the midbrain/bridge showed a high- Showa University Hospital using a 1.5 T MR imager (Mag-
signal area that was suggestive of chronic ischemia. netom Essenza; Siemens, M€ unchen, Germany). T2-weighted
Neuropsychological findings: The patient presented with axial slices were acquired (23 slices; thickness, 5 mm) using
disorientation and motor aphasia characterized by word- an interslice gap of 6 mm, a field of view of
finding difficulty, phonological paraphasia and persevera- 196 9 320 mm2, a repetition time of 4000 ms, and an echo
tion. In addition, her speech consisted of only several words. time of 99 ms. MRI was performed 2 days after infarction
She retained language understanding regarding both reading in patient 2 and 3 days after infarction in patient 3. CT
and hearing simple sentences, such as “close your eyes” or axial slices were obtained (Sensation 64; Siemens) at a slice
“raise your right hand,” and was able to make simple con- thickness of 4.8 mm 13 days after infarction in patient 1.
versation; however, she had difficulty with longer sentences, The mapping of lesions was performed by one of the
such as “pinch your left ear with your right thumb and authors (MKo), without knowledge of the test results or
index finger.” She was able to answer simple questions cor- the patients’ clinical features, and the mapping was verified
rectly using “yes” or “no.” Repetition was similar, in that independently by MKa, an expert neurologist. Where there
she was able to repeat shorter sentences. She could name 69 were differences, MKa’s decision prevailed. The lesions
daily objects out of 100, with major error perseveration and were mapped using the MRIcro software (http://www.sph.
circumscribing, and was able to point at objects after hear- sc.edu/comd/rorden/) on slices of a T1-weighted template
ing their names. The patient also exhibited difficulty writing MRI from the Montreal Neurological Institute. This tem-
kanji. At the time of discharge (17 days after admission), plate is approximately oriented to match the Talairach
mild perseveration and impaired word recall remained, space20 and is distributed with MRIcro. The lesions were
whereas the other symptoms had disappeared. mapped onto the slices that corresponded to z coordinates
–10, –5, 5, 10, 15, 20, 25, 30, 35, 40, 45, 50, and 55 mm in
Patient 4. The patient was an 81-year-old right-handed Talairach coordinates using the identical or the closest-
woman. matching transversal slices of each patient. We superim-
History of the present illness: Two days after having diffi- posed the lesions using MRIcro to find regions of mutual
culty forming words, the patient moved in with her daughter involvement.

Neurology and Clinical Neuroscience 1 (2013) 55–62 57


ª 2013 Japanese Society of Neurology and Wiley Publishing Asia Pty Ltd
Broca’s area and apraxia N Tsuruya et al.

Apraxia testing. Patients were tested in three domains to frontal gyrus, that is, Brodmann areas 44 (116 voxels) and
assess apraxia: pantomime, imitation and actual tool use. 45 (16 voxels). Other lesions were located in the precentral
The tasks consisted of seven transitive gestures of tool use gyrus, middle frontal gyrus, pars triangularis, pars opercu-
(combing hair using a comb, brushing teeth with a tooth- laris, partly extending to the inferior orbitofrontal cortex,
brush, pounding on a nail with a hammer, eating with a insula, postcentral gyrus, caudate nucleus, putamen, superior
spoon, clipping the fingernails with nail scissors, unlocking a temporal gyrus and temporal pole.
door with a key and cutting with scissors) and seven intran-
sitive gestures (making a salute, forming a fist, waving good- Apraxia testing. The performances observed using the
bye, shooing away, scratching the head, snapping the fingers right and left hand were not significantly different; thus, the
and beckoning). Apraxia testing was performed 1–2 weeks analysis was based on the overall mean of all performances.
after the patients were hospitalized. In general, a decline was observed in the performance of
To pantomime verbal commands, patients were given ver- actions in response to verbal commands (Fig. 2). For intran-
bal instructions to perform gestures. For transitive gestures, sitive gestures, all patients had a significantly lower number
participants were instructed to pretend to hold the object in of correct responses for verbal command compared with
their hand and perform the gesture (e.g., “Show me how imitation (patient 1, chi-squared = 6.09, d.f. = 1, P < 0.05;
you would use a hammer”). For intransitive gestures, patient 2, chi-squared = 4.67, d.f. = 1, P < 0.05; patient 3,
patients were told, for example, “Show me how you would chi-squared = 9.33, d.f. = 1, P < 0.01; and patient 4, chi-
wave goodbye.” To pantomime visually presented tools, the squared = 4.09, d.f. = 1, P < 0.05). For transitive gestures, a
participants were presented with a tool and asked to show significant difference was observed between verbal com-
how they would use it without touching the tool. For imita- mands and actual tool use for all patients, with the excep-
tion, patients imitated gestures presented by the examiner. tion of patient 2 (patient 1, chi-squared = 6.09, d.f. = 1,
The examiner continued the presentation of the gesture until P < 0.05; patient 3, chi-squared = 7.63, d.f. = 1, P < 0.01;
the patient performed the imitation. For actual tool use, the and patient 4, chi-squared = 20.5, d.f. = 1, P < 0.01). For
patients were given the actual tool to hold and were asked patient 4, a difference in performance was observed between
to pretend to use the tool. The items used to test actual tool verbal commands and imitation (chi-squared = 9.96, d.f. =
use were the same as those used to test transitive gestures. 1, P < 0.01) and between visually presented tools and actual
All of these tasks were performed by each hand. The tool use (chi-squared = 12.1, d.f. = 1, P < 0.01).
patients were allowed to restart as many times as desired, Figure 3 shows the results of the error analysis. No signif-
until they were satisfied. icant differences were observed between intransitive and
Patients were videotaped while executing the test. These transitive gestures and between verbal command and visu-
tapes were scored by two trained judges. If the judges ally presented tools; therefore, the sums of these values are
arrived at different decisions, they consulted the video presented. Regarding these gestures, spatial errors were more
recording for reaffirmation. Gestures were scored quantita- common than were other errors for patients 1, 2 and 4. Per-
tively regarding accuracy. If a patient restarted an action severation was observed frequently for patients 3 and 4. In
but was able to express the correct action, it was counted as addition, regarding imitation and actual tool use, the spatial
being the correct response. Error types were scored for each errors observed were similar to, or less than, those detected
apraxic gesture using the scoring system developed by Rothi for pantomiming. Hesitation was the most frequent of the
et al.21 Errors were categorized as spatial (body-part-as-tool other types of error.
[BPT]), movement, amplitude (internal and external configu-
ration), temporal (sequencing, timing and occurrence), con-
Discussion
tent (related and unrelated content), perseveration or other
errors (unrecognizable movement, hesitation or no In this study, we investigated four patients with symptoms of
response). All false responses that occurred when the patient apraxia who had a common lesional site: Broca’s area and
restarted the action were included in the analysis; thus, a test the left inferior frontal gyrus. These patients did not have
could have more than one type of error. severe language comprehension impairment and paralysis
was either nonexistent or mild. Both left-handed and right-
Statistical analysis. We compared the performances of handed apraxia was confirmed. Declined performance related
intransitive gestures (on verbal command vs. imitation) and to verbal commands for both intransitive and transitive ges-
transitive gestures (on verbal command, in response to visu- tures was observed for all patients, whereas the performances
ally presented tools, imitation and actual tool use) separately of imitation and actual tool use were preserved. Analyses of
using a chi-squared test, with Bonferroni correction for mul- error patterns showed the presence of frequent spatial errors
tiple comparisons when necessary. Statistical significance and perseveration. These symptoms fall under the classifica-
was set at P < 0.05. tion of ideomotor apraxia.13–16 Previous reports have stated
that the performance of transitive gestures is worse than that
of intransitive gestures in apraxia22–24; on this point, our
Results findings differ from the results of previous studies. The symp-
Lesion analysis. Figure 1 illustrates the superimposed toms of apraxia were observed equally for the left and right
lesion data of our patients. The center of the lesion was in hands, which is consistent with the finding that the left hemi-
the pars triangularis or the pars opercularis of the inferior sphere is dominant with respect to actions.9,10

58 Neurology and Clinical Neuroscience 1 (2013) 55–62


ª 2013 Japanese Society of Neurology and Wiley Publishing Asia Pty Ltd
N Tsuruya et al. Broca’s area and apraxia

Figure 1 Anatomical location of lesions in our patients. The overlapping lesions of our four patients are shown on the template brain. The
number of overlapping lesions is illustrated by different colors that code increasing frequencies, from violet (n = 1) to red (n = 4). The common
lesioned areas in our four patients were Brodmann areas 44 and 45. The right side of the image corresponds to the left hemisphere.

The left parietal lobe is thought to be the brain region Our results suggest that the region centered on the left
that is primarily related to apraxia.10,12,25,26 Clinical neuro- inferior frontal gyrus is important for pantomiming.
psychological research has revealed that lesion responses in Recently, Binkofski and Buccino. described a 50-year-old
ideomotor apraxia were from the left frontal to parietal patient with a focal lesion on the right frontal operculum,
lobes and the role of the parietal association area, such as probably including the ventral premotor cortex, who was
the supramarginal gyrus and angular gyrus, was empha- unable to associate simple gestures and colors. This suggests
sized. However, the patients diagnosed with ideomotor that the ventral premotor cortex plays a substantial role in
apraxia include cases with different combinations of impair- pantomiming, at least in the initial phase of visuomotor
ment. Past research of impaired pantomiming reported its associative learning.30 A lesion subtraction analysis per-
association with a subcortical lesion of the parietal lobe,27 formed by Goldenberg and colleagues showed that defective
whereas other researchers noted that patients with lesions pantomiming of tool use was associated with damage to the
of the parietal lobe have normal pantomiming ability.28,29 inferior frontal gyrus and adjacent portions of the insula
These findings show that lesions of the parietal lobe do not and precentral gyrus of the left hemisphere. In contrast,
necessarily lead to pantomiming impairment. In fact, the parietal lesions did not specifically impact pantomime.17
cases described here presented with pantomiming impair- Similarly, Bohlhalter et al investigated the effect of continu-
ment even though CT and SPECT scan findings failed to ous theta burst stimulation (cTBS) on gesture production
confirm the presence of any lesions in the parietal lobe. and recognition. cTBS of the left inferior frontal gyrus sig-
However, the lesions of the four cases spread to the white nificantly impaired action production, whereas stimulation
matter; thus, the lesion may have severed the bond to of the inferior parietal lobule did not.31
another region related to actions, which may have caused The apraxic symptoms in our patients were most promi-
the apraxia. nent on verbal commands: gestures performed in response

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ª 2013 Japanese Society of Neurology and Wiley Publishing Asia Pty Ltd
Broca’s area and apraxia N Tsuruya et al.

Intransitive and transitive gestures


40

35

30

25

No. of errors
20

15

10

0
Spatial Temporal Content Perseveration Other

Figure 2 Performance in the apraxia tests. For intransitive gestures, Case 1 Case 2 Case 3 Case 4
our patients performed worse regarding verbal commands compared
with imitation. For transitive gestures, patient performances were Imitation
generally worse regarding verbal commands compared with other 25
conditions.
20

to objects presented visually and imitation or actual tool use

No. of errors
15
yielded comparatively better performance, suggesting that
trauma to Broca’s area adversely affected associations
between language and actions. Regarding pantomiming to 10

verbal commands, knowledge about tools and their func-


tions should be transformed into motor sequences that are 5
only triggered from verbal cues. Regarding actual tool use,
the shape of the tool may provide clues about how it is held 0
and used.17 For example, the movement of using a hammer Spatial Temporal Content Perseveration Other
can be cued by the shape and size of the hand-gripped por- Case 1 Case 2 Case 3 Case 4
tion, whereas during pantomiming on verbal commands, this
must be planned without such cues. All of our patients
8
Actual tool use
showed significantly worse performance of intransitive ges-
tures, which are actions that must also be exclusively 7
recalled based on verbal cues, without using external stimuli.
This interpretation is consistent with the fact that perfor- 6

mance was better during imitation. To test imitation, infor- 5


No. of errors

mation related to an action was presented by the tester and


4
the patients did not need to evoke memories or knowledge
about the actions. Because it has been demonstrated that the 3
observation of meaningless gestures does not activate Broca’s
2
area,32 our patients may have succeeded in imitating using an
alternative neural system that does not need action knowl- 1
edge. As previously reported, a lesion of the parietal lobe
0
impaired the spatial relationship processing of the body Spatial Temporal Content Perseveration Other
parts, resulting in impaired imitation.26 The parietal lobe was
Case 1 Case 2 Case 3 Case 4
spared in our patients; therefore, they may have achieved
imitation based on the processing of body-part information
Figure 3 Results of the error analyses. The sums of errors in the
via the parietal lobe. Our results appear to be at odds with performance of intransitive and transitive gestures are presented.
the results of functional imaging studies, which indicated the Spatial errors were more common than were other types of error in
presence of a relationship between the inferior frontal region patients 1, 2 and 4 regarding intransitive and transitive gestures.
and imitation. However, research on imitation uses meaning- Perseveration was observed frequently in patients 3 and 4. Regarding
ful gestures as targets for imitation; thus, it is possible that imitation and actual tool use, the spatial errors were observed similar
Broca’s area functioned in reading the intent of these actions. to, or less than, those observed for intransitive and transitive gestures.
In addition, imitation of goal-directed actions leads to bilat-
eral inferior frontal activation.33 Covert verbalization (“inter- Finally, our study had several limitations. First, there was
nal speech”) during motor actions may be another possible no control group. To ascertain whether trauma to Broca’s
factor involved in the activation of Broca’s area.34 area causes apraxia, a similar set of tests should be per-

60 Neurology and Clinical Neuroscience 1 (2013) 55–62


ª 2013 Japanese Society of Neurology and Wiley Publishing Asia Pty Ltd
N Tsuruya et al. Broca’s area and apraxia

formed using a group of patients with brain damage without 8 Liepmann H. The left hemisphere and action. In: Kimura D, ed.
lesions in Broca’s area. Second, we cannot exclude the influ- Translations of Liepmann’s Essays on Apraxia. London, Ontario:
ence of the language disorder on the results of the test. The DK Consultants; 1980; 17–50.
apraxic syndrome was observed in our patients during tasks 9 Goldenberg G, Hartmann K, Schlott I. Defective pantomime of
object use in left brain damage: apraxia or asymbolia?
that used linguistic components (i.e., verbal commands).
Neuropsychologia 2003; 41: 1565–73.
Therefore, the pantomime deficits in relation to verbal com- 10 Heilman KM, Rothi LJ. Limb apraxia: A look back. In: Rothi
mands might have been affected by uncontrolled linguistic LJ, Heilman KM, eds. Apraxia: The neuropsychology of Action.
processes. However, our patients did not show a comprehen- Hove, UK: Psychology Press; 1997; 7–18.
sion impairment that would affect the understanding of the 11 Johnson-Frey SH, Newman-Norlund R, Grafton ST. A
task instructions. Although language comprehension deficits distributed left hemisphere network active during planning of
were reported in patients with lesions in Broca’s area, these everyday tool use skills. Cereb. Cortex 2005; 15: 681–95.
deficits were observed predominantly in response to syntacti- 12 Buxbaum LJ. Ideomotor apraxia: a call to action. Neurocase
cally complex sentences.3,35 Further, the spatial errors 2001; 7: 445–58.
recorded during apraxia testing in the present study cannot 13 Ochipa C, Rothi LJ, Heilman KM. Conceptual apraxia in
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14 Ochipa C, Rothi LJ, Heiloman KM. Ideational apraxia:
each patient had a different etiology. The most severe symp- A deficit in tool selection and use. Ann. Neurol. 1989; 25: 190–3.
toms of apraxia were observed in the case with a brain 15 Rothi LJ, Raymer AM, Heilman KM. Praxis assessment. In:
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