Iranian Journal Original Paper

of Neurology Iran J Neurol 2014; 13(2): 77-82

Brain areas impaired in oral and

verbal apraxic patients Received: 28 Nov 2013
Accepted: 29 Feb 2014

Fariba Yadegari1, Mojtaba Azimian2, Mahdi Rahgozar3, Babak Shekarchi4

1
Department of Speech Therapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran
2
Department of Clinical Sciences, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran
3
Department of Statistics, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran
4
Department of Radiology, School of Medicine, AJA University, Tehran, Iran

Keywords Oral apraxia is considered a higher order disorder of

Broca’s Area, Insula, Left Hemisphere Damage, Oral Apraxia, orofacial movements for non-speech gestures. It has
Verbal Apraxia been associated with inferior frontal, deep frontal
white matter, insula, the posterior pars opercularis of
the inferior frontal gyrus, the Rolandic operculum
and basal ganglia lesions.1-5
Abstract Verbal apraxia also called apraxia of speech (AOS)
Background: As both oral and verbal apraxia are related to is defined by Duffy6 as, “…a neurologic speech
vocal orofacial musculature, this study aimed at identifying
disorder that reflects an impaired capacity to plan or
brain regions impaired in cases with oral and verbal apraxia.
program sensorimotor commands necessary for
Methods: In this non-experimental study, 46 left brain
directing movements that result in phonetically and
damaged subjects (17 females) aged 23–84 years, were
examined by oral and verbal apraxia tasks. Impaired and prosodically normal speech.” (p. 307). Some
spared Broca’s area, insula, and middle frontal gyrus in the investigations have been focused on brain areas
left hemisphere were checked from magnetic resonance involved in verbal apraxia. The most famous of them
imaging and computed tomography scans utilizing is that of Dronkers7 who concluded that anterior
Talairach Atlas. Data were analyzed using chi-square test. insula was the main impaired cite in verbal apraxia.
Results: Insula was significantly impaired in both forms of Verbal apraxia has also been reported to result
oral and verbal apraxia and different severities and following damage to Broca’s area,8 basal ganglia,9
prominent forms of both apraxias (P < 0.05). Broca’s area was insular and temporal regions, even right inferior
slightly less involved than insula in two forms of apraxia. frontal regions.10,11
Conclusion: As the damage of insula was more prominent As oral and verbal apraxia both are occurred in
in both forms of apraxias, it seems that oral and verbal motor programming of the same orofacial apparatus,
apraxia may have commonalities regarding their the question remains whether there are commonalities
underlying brain lesions. between brain’s areas involved in them. Hillis et al.8
questioned lesion overlap studies validity, discussing
Introduction that the area of greatest overlap among large strokes
The term “apraxia” is typically defined as an inability to may just reflect the vulnerability of the regions to
plan and execute purposeful movements. Among ischemia, a point that was later addressed by Trupe et
different types of apraxia, there are two apparently al.12 who raised the possibility that the association
related apraxias: oral and verbal apraxia, which occurs mentioned between anterior insula infarction and
in relation to buccofacial musculatory motor planning. verbal apraxia might be accounted for by the fact that

Iranian Journal of Neurology © 2014 Corresponding Author: Mojtaba Azimian

Email: [email protected] Email: [email protected]

http://ijnl.tums.ac.ir 3 April
 verbal apraxia generally persists in cases of large middle was determined according to the fifth percentile of
cerebral artery (MCA) strokes which always involve the 102 healthy adults’ performance (aged 20–80 years).
insula. So to better address this issue, we decided to Cut-off score also was validated by clinical judgment
examine a control area (middle frontal gyrus [MFG]) as is described in severity ratings section.
which is also fed by MCA branches.
Our specific questions were: (1) Are Broca’s area, left Diagnosis of verbal apraxia
insula and MFG impaired in patients with oral apraxia? The verbal apraxia task was originally translated into
(2) Are these areas impaired in patients with verbal Farsi and adapted from expressive speech subtest of
apraxia? (3) Are involvement of these areas in various Luria-Nebraska Neuropsychological Battery (LNNB)(I)
severities of apraxias different? (4) Which areas are to investigate adults brain neuropsychological profiles
more involved in subgroups of co-occurred apraxias? (Kapurkhani, 2007, unpublished MSc thesis). As it
And (5) are there commonalities between areas comprised oral expression parts and involved a
involved in oral and verbal apraxia? scoring system similar to our oral apraxia task which
rendered two apraxias comparable, it was adapted for
Materials and Methods verbal apraxia and used by the authors in this
Participants research. The task comprises 25 items in seven parts:
Among 83 early examined patients, 55 patients met the repetition of speech sounds and words, telling the
inclusion and exclusion criteria and just 46 patients had sound of letters, reading words, sentence repetition,
magnetic resonance imaging (MRI) or computed reciting automatic series, story retelling and narrative
tomography (CT) scans. These 46 brain damaged speech. Scoring procedure was according to the
patients of which 17 females participated in this study. number of errors in each section. We elucidate this
They were recruited from hospitals, private clinicians, scoring by the example of subtest of repetition of
and neuro-rehabilitation centers of Tehran, Karaj, speech sounds. This subtest is administered as follows:
Shiraz, and Mashad. All patients were native Farsi “please repeat theses sounds: /e/, /â/, /m/, /d/,
speakers with normal or corrected-to-normal hearing /ŝ/.” If the subject says all the sounds correctly the
and vision. Participants were right handed and scored score will be (0). If (s)he has 1–2 errors, the score will
at the ceiling in the Edinburgh handedness inventory be 1, and if 3–5 errors are produced, the score will be 2.
with unilateral left hemisphere lesions, and aged 23–84 For the subtest of story retelling and narrative
(mean = 54 years). They were all literate with 1–119 speech, the scoring comprised two criteria: time
month range of post onset time. Exclusion criteria taken to start to respond and the number of words in
included the presence of other neurological disease, the first 5 s. In story retelling, a story was read to the
severe auditory comprehension deficits, dementia or patients, while the passage was in front of him(her).
cognitive impairment, right hemisphere damage, and Then (s)he was asked to retell the story. The time
more than one cerebral accident. taken to start to respond was calculated. If this time
This study was approved by the Research Ethics was 0–10 s, the score was 0. If it was 11–22 s, the score
Committee of the University of Social Welfare and was 1, and if it was 23–31 s, the score was 2. Also if
Rehabilitation Sciences, Tehran, Iran. All participants the number of spoken words in the first 5 s was >9,
signed a free and informed consent form. the score was 0, if it was 6–9, the score was 1, and if it
Procedure was 0–5, the score was 2.
Apraxia tasks As many of the patients had a concomitant
*All task sessions were videotaped by a Sony Digital aphasia, anomic errors such as semantic and
Handy Cam (200M) for further analysis. phonological errors had to be separated from apraxic
errors, so we incorporated Wambaugh and Dabul’s
Diagnosis of oral apraxia criteria in order to make correct decisions about
Oral apraxia was assessed by a task in which patients speech apraxic errors.14,15 Therefore, while scoring,
are asked to reproduce a variety of buccofacial gestures we made differential diagnosis of paraphasias and
to verbal commands. This task has 22 items including verbal apraxia errors. The procedure of scoring for
instructions for tongue, lips, mouth, and vocal cords this task was time consuming and careful and videos
movements. The scoring procedure was as follows: 0 were seen several times.
for a correct response, 1 for an erroneous response Total score of verbal apraxia task was 50
according to 14 predicted errors and 2 for no response. representing the maximum error and the highest
Total score was 44 representing the maximum error and amount of apraxia (cut-off: 12). Lawsche’s content
the highest amount of apraxia (cut-off: 3). Lawsche’s validity ratio of this task was above 50% for all items
content validity ratio of this task was above 50% for all according to 25 experts’ opinions, and inter-rater
items according to 25 experts opinions.13 Cut-off score reliability coefficient was 83% (P < 0.001). Cut-off score

78 Iran J Neurol 2014; 13(2) Yadegari et al.

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 was determined according to the fifth percentile of 102 demographic profile of patients, rated a yes–no
healthy adults’ performance (age range of 20–80 years). scale for each specified region for each patient
Cut-off score also was validated by clinical judgment as according to their CT or MRI scans using Thalairach
is described in severity ratings section. Atlas of the Brain.
Severity ratings
Two certified speech-language pathologists with good Results
experience with adult with apraxia who were blind to Subjects
lesion information, viewed each videotape and Table 1 summarizes clinical and demographic
determined the presence or absence of oral and verbal characteristics of subjects. Etiology was not
apraxia as well as a severity rating for each.
controlled, but as is evident from table 1 was
The five-point equal-appearing-interval scales used
dominated by ischemic stroke.
to evaluate the severity of oral and verbal apraxia was
Brain areas status in patients with or without oral
as follows: 0 = no impairment; 1 = mild; 2 = mild-to-
or verbal apraxia
moderate; 3 = moderate-to-severe; and 4 = severe.
Table 2 represents the number of impaired targeted
The same scores or 1 score difference were
brain areas for each group of patients with or without
considered as total agreement. If there were 2 or more
score difference, a third judge was recruited who no oral or verbal apraxia.
longer scored but just accepted one of the two scores. It is evident from table 2 that the frequency of
These ratings were used for severity analysis of impairment of Broca’s area and insula for oral apraxics
apraxias, also for validation of cut-off points. is high and close to each other (insula > Broca’s area)
It should be noted that except in one case (whose while MFG is lower than both areas. χ2 revealed that the
score in the oral apraxia task was 4 but was estimated difference between impaired and spared areas for any
without oral apraxia by judges), all cut-off points, three areas is significant (P < 0.05). In patients without
which were based on fifth percentile of healthy adults, oral apraxia the difference of impaired–spared areas are
fully matched to clinical judgments. not significant (Broca’s area and insula > MFG).
Brain areas In patients with verbal apraxia, χ2 showed a
Three brain areas were selected to study: Broca’s area, significant difference of impaired–spared areas for
left insula, and left MFG. Two former areas being Broca’s area and insula (P < 0.05) but not MFG. The
considered because of their history of contributions in frequency of impairments is as follows: insula >
speech articulation process and the latter was Broca’s area > MFG. In patients without verbal
considered as a control area. apraxia, the frequency of Broca’s area and insula
A neuroradiologist who was blind to clinical and impairment are equal and much higher than MFG.

Table 1. Clinical and demographic data

Education Post onset
Age (year) Etiology
(year) time (month)
Variable
Ischemic Hemorrhagic Stroke Operated Operated
Mean ± SD Mean ± SD Mean ± SD Trauma
stroke stroke (unspecified) tumor AVM
Gender
Female (n = 17) 59.47 ± 17.76 10.82 ± 5.19 33.11 ± 29.48 10 0 4 1 1 1
Male (n = 29) 50.8 ± 13.33 12.58 ± 4.10 20.75 ± 23.53 21 3 1 0 0 4
Total (n = 46) 31 3 5 1 1 5
SD: Standard deviation

Table 2. Brain regions involved in groups of with and without apraxia

Number
Group Impaired Spared
Impaired Spared Impaired Spared
Broca’s Broca’s χ2 χ2 χ2
MFG MFG insula insula
area area
With oral apraxia 32 7 16.02* 26 13 4.33* 35 4 24.64*
Without oral apraxia 5 2 1.28 1 6 3.57 4 3 0.14
With verbal apraxia 30 5 17.85* 25 10 6.42 32 3 24.02*
Without verbal apraxia 7 4 0.81 2 9 4.45* 7 4 0.81
*P < 0.05. MFG: Middle frontal gyrus

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 Table 3. Impaired brain regions in different severities of oral apraxia
Brain region
Broca’s area
Group MFG impairment Insula imparment
impairment χ2 χ2 χ2
Yes No Yes No Yes No
Without oral apraxia 5 2 1.28 1 6 3.57 4 3 0.14
Mild 4 4 0.00 5 3 0.50 5 3 0.50
Mild-to-moderate 12 2 7.14* 7 7 0.00 13 1 10.28*
Moderate-to-severe 9 0 5.44* 7 2 2.77 9 0 5.44*
Severe 7 1 4.50* 7 1 4.50* 8 0 4.50*
*P < 0.05. MFG: Middle frontal gyrus

Table 4. Impaired brain regions in different severities of verbal apraxia

Brain region
Broca’s area
Group MFG impairment Insula imparment
impairment χ2 χ2 χ2
Yes No Yes No Yes No
Without verbal apraxia 7 4 0.81 2 9 4.45* 7 4 0.81
Mild 4 2 0.66 3 3 0.00 4 2 0.66
Mild-to-moderate 5 2 1.28 3 4 0.14 7 0 5.44*
Moderate-to-severe 15 1 12.25* 14 2 9.00* 15 1 12.25*
Severe 6 0 4.50* 5 1 2.66 6 0 4.50*
*P < 0.05. MFG: Middle frontal gyrus

Brain areas status in different severities of apraxia apraxias, we further grouped them into six
Tables 3 and 4 compare impaired–spared brain areas in categories: (1) patients who did not have any form of
different severities of oral and verbal apraxia apraxia (without any apraxia), (2) patients who just
respectively. had oral apraxia without verbal apraxia (oral apraxia
As is evident from table 3, in mild-to-moderate oral only), (3) patients who just had verbal apraxia
apraxia both Broca’s area and insula are significantly without oral apraxia (verbal apraxia only), (4)
impaired (P < 0.05) while MFG shows indifference. This is patients who had both forms of apraxia with
also through for moderate-to-severe cases, but here MFG identical severity (co-occurred apraxia), (5) patients
is more impaired than spared. In severe cases three areas who had both forms of apraxia with different
are much impaired (insula > Braca’s area and MFG). severities so that oral apraxia was with two or more
It can be seen from table 4 that in mild-to-moderate severity score higher than verbal apraxia (oral
cases of verbal apraxia, insula is significantly impaired apraxia prominent), and (6) patients who had both
(all seven patients had impaired insula), but Broca’s forms of apraxia with different severities so that
area and MFG are not significantly impaired (Broca’s verbal apraxia was with two or more severity score
area > MFG). In moderate-to-severe and severe cases all higher than oral apraxia (verbal apraxia prominent).
three areas are much impaired. Table 5 provides comparison of impaired–spared
Comparison of brain regions impairment in different areas in these subgroups.
groups As is shown in table 5, in oral apraxia only cases,
In order to consider the co-occurrence of two Broca’s area shows a relative homology, while insula

Table 5. Impaired brain regions in different co-occurred groups

Brain region
Broca’s area Insula
Group MFG impairment
impairment χ2 χ2 impairment χ2
Yes No Yes No Yes No
Without any apraxia 4 2 0.66 1 5 2.66 3 3 0.00
Oral apraxia only 3 2 0.20 1 4 1.80 4 1 1.80
Verbal apraxia only 1 0 - 0 1 - 1 0 -
Co-occurred apraxia 27 3 19.20* 23 7 8.53* 28 2 22.53*
Oral apraxia prominent 1 1 0.00 1 1 0.00 2 0 1.00
Verbal apraxia
1 1 0.00 1 1 0.00 1 1 0.00
prominent
*P < 0.05. MFG: Middle frontal gyrus

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 is highly impaired and MFG is highly spared. In the ganglia, external capsule, and internal capsule. They
single case of verbal apraxia only, Broca’s area and proposed that we should regard verbal apraxia as a
insula are impaired and MFG is spared. In collection of symptoms related to different brain areas.
co-occurred apraxia all three cases are significantly We may reason here that instead of considering the
impaired (P < 0.05) (insula > Broca’s area > MFG). In most severe forms of apraxia, which raise the
two cases with oral apraxia prominent pattern, insula possibility of co-occurrence and overlapping, it is
is impaired, while the other areas show half and half better to stick to more moderate forms to better
impairment. In two cases with verbal apraxia segregate areas responsible for it.
prominent pattern, three areas show fifty-fifty Regarding our forth question in relation to co-
impairment. occurrence of apraxias, we had the opportunity of
It should be mentioned here that in calculating χ2, looking at more pure forms in patients. In the oral
we encountered with the problem of low expected apraxia only group, Insula was significantly impaired
values in some cells, which could not be solved by while MFG was significantly spared and Broca’s area
combining values because of the nature of variables. although was more impaired than spared, the
For interpretation of the results on those situations, difference was not significant. In the only case with
we were more relying on the total number of pattern of verbal apraxia only, both Broca’s area and
individuals in each subgroup. Insula were impaired, while MFG was spared. Also in
oral apraxia prominent subgroup, Insula was
Discussion prominently impaired. Overall as we can infer from
This research exploited lesion study to search for table 5, Insula (not Broca’s area) was more evidently
possible commonalities between brain areas impaired impaired in oral apraxia subgroups, and both areas
in patients with oral and verbal apraxia. Regarding were impaired in verbal apraxia subgroups. The latter
our first question on the subject of oral apraxia, the result may challenge the results of Hillis et al.8 that
number of impaired–spared brain areas for all three proved Broca’s area, but not Insula to be associated
regions in oral apraxic patients was significantly strongly with verbal apraxia. Likewise, our results
different. But what should be noticed is that the regarding verbal apraxia is neither consistent with
frequencies of involvement of these regions were Richardson et al.17 conclusion that damage to the
dissimilar. Broca’s area and Insula were both posterior portion of Broca’s area is a better predictor
considerably more impaired in comparison to MFG. of AOS than insula involvement nor with Ogar et al.16
The second question targeted verbal apraxia, and and Dronkers7 who found that insula damage is a
the results showed that the impaired Broca’s area and more reliable predictor of motor speech impairment
insula in patients with verbal apraxia were compared to Broca’s area involvement. It can be seen
significantly higher than spared areas, but it was not from our results that both Broca’s area and Insula are
true for MFG. Hence, it is apparent from the results involved in verbal apraxia.
that both Broca’s area and Insula were impaired On the other hand, when we consider our results
significantly for both kinds of apraxia. for both forms of apraxia, Insula was conspicuously
Concerning the third question which was focused impaired in oral and verbal apraxia and different
on severity of apraxias, the noticeable finding was severities and prominent forms of both apraxias. This
seen in mild-to-moderate oral apraxia subgroup, finding is in line with literature that view Insula as a
where both Broca’s area and insula were significantly main cite of damage in some case reports of verbal
impaired while MFG showed indifference. apraxia,5,7 and as one of the impaired areas mentioned
Furthermore, this was true for moderate-to severe for oral apraxia.18
cases, but here impaired–spared areas for MFG were The last question of the present research regards
somewhat closer to the other areas. This pattern was the commonalities of neuropathology of oral and
changed for verbal apraxia (Table 4), in which Insula verbal apraxia. Ackermann and Riecker5 concluded
was prominently impaired in moderate-to-severe that no strict co-occurrence of verbal apraxia and oral
patients but for the other more severe cases, the status apraxia in subjects within trasylvian pathology seems
of the three areas were somewhat closer to each other. to occur.5 This seems to be the case with our results
The relationship of severity of verbal apraxia to because despite great correlations, no one-to-one
extent of brain damage and lesion site has been correspondence was seen in clinical or neuroimaging
investigated by Ogar et al.16 They found out that mild profile of the patients. Yet, integrating all the results
cases had lesions restricted to the insula and may reveal Insula as the common area involved in
immediately surrounding areas. But more severe cases both apraxias of this research.
had lesions encompassing the insula and MFG, with It seems that the most important finding of the
most lesions also involving Broca’s area, the basal present research is that examining neural correlates of

Brain areas impaired in oral and verbal apraxia Iran J Neurol 2014; 13(2) 81

http://ijnl.tums.ac.ir 3 April
 apraxia is better performed with milder forms. For chance in comparison to MFG in both verbal and oral
future investigations, it seems reasonable that we apraxic patients, and Insula was more prominently
should not seek for absolute frequencies in calculation impaired. Also it is concluded that milder forms of
of brain areas impaired in a neuropsychological apraxia are better candidates for identification of
disorder, but looking for relative frequencies as has involved brain areas.
been applied in this study. Another way of answering
the questions of this research may be searching for Conflict of Interests
pure types of apraxia in milder forms and comparing The authors declare no conflict of interest in this study.
their brain areas involved.
Finally, the results of this study should be Acknowledgments
considered cautiously because of the limitations
We deeply thank the patients and their families for the
which we recommend to be controlled in future
time and effort they offered to our project.
studies. We did not control the age range of the
subjects. Furthermore, the post-onset time was just
controlled for the acute phase not for the evolutionary How to cite this article: Yadegari F, Azimian M,
stage of spontaneous recovery. Rahgozar M, Shekarchi B. Brain areas impaired in oral and
verbal apraxic patients. Iran J Neurol 2014; 13(2): 77-82.
Conclusion
Based on the results of this study, we may conclude
that Broca’s area and left Insula were impaired above

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