Download Agenesis of the Arcuate Fasciculi in Congenital

OBSERVATION
Agenesis of the Arcuate Fasciculi in Congenital
Bilateral Perisylvian Syndrome
A Diffusion Tensor Imaging and Tractography Study
Byron Bernal, MD; Gustavo Rey, PhD; Catalina Dunoyer, MD; Harshad Shanbhag, MS; Nolan Altman, MD
Objective: To describe the absence of the arcuate fasciculi in 2 cases of congenital bilateral perisylvian syndrome (CBPS).
Main Outcome Measures: Neuropsychology evaluation; fractional anisotropy, apparent diffusion coefficients, and anatomical aspect of the tracts.
Design: Case series.
Results: Absence of the arcuate fasciculus was observed in both subjects. Ancillary findings were complete absence of the superior longitudinal fasciculi in 1
case and underdevelopment in the other. Low fractional
anisotropy of the left inferior occipitofrontal fasciculus
was found in both cases. The same tract was maloriented in 1 of the cases.
Setting: Pediatric referral hospital–based study.
Patients: Two patients with CBPS, referred to our
institution as candidates for surgical treatment of
epilepsy.
Intervention: Diffusion tensor imaging (1.5-T scanner; 15 encoding directions; b = 800 s/mm2) and deterministic tractography of the main projection and association tracts.
T
Author Affiliations: Miami
Children’s Hospital (Drs Bernal,
Rey, Dunoyer, and Altman and
Mr Shanbhag) and MCH Brain
Institute (Drs Bernal, Rey, and
Dunoyer), Miami, Florida.
Conclusion: Agenesis of the arcuate fasciculus may accompany CBPS.
Arch Neurol. 2010;67(4):501-505
HE CONGENITAL BILATERAL
perisylvian syndrome
(CBPS) is a type of cortical developmental abnormality characterized by
poor operculation of the parietal and
frontal lobes, wide lateral sulcus, polymicrogyria, orofacial diplegia, epilepsy, and
developmental delay.1,2 Seizures are present in 65% of cases.3,4 To our knowledge,
CBPS has not been studied to date with
diffusion tensor imaging and fiber tractography.
We describe 2 cases with absence of
the arcuate fasciculus (as part of agenesis
or hypoplasia of the superior longitudinal fasciculus) in CBPS using diffusion
tensor imaging and fiber tractography in
relation to clinical and neuropsychological findings. To our knowledge, there are
no existing reports describing bilateral
agenesis of the arcuate fasciculus in this
condition. The correlation of this finding
with the clinical analysis of the language/
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501
speech deficit may contribute to the
understanding of the arcuate fasciculus
function.
REPORT OF CASES
The clinical and neuroradiological findings of 2 cases with CBPS are summarized in the Table. Case 2 has no arcuate
fasciculus but has the remnant fibers of
the superior longitudinal fasciculus.
Normally, the superior longitudinal fasciculus has, in addition to the arcuate
fasciculus, a bundle of short fibers connecting the parietal areas (supramarginal
gyrus) with frontal areas. In addition, the
fractional anisotropy of the left inferior
occipitofrontal fasciculus was found to
be low in both cases and bilaterally in
the cingulum of case 2.
A single-shot, spin-echo, echo-planar
imaging sequence with diffusion weighting
consisting of 15 encoding directions was
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Table. Report of Cases
Age, y
Sex
Handedness
Main diagnosis
Onset of seizures, y
Type of seizure
General developmental
milestones
Language developmental
milestones
Neuropsychology evaluation
Overall intellectual functioning
Language
Prosody
Articulatory skills
Conduit d’approache c
Automatic series
Automatic series backward
Phonemic fluency
Semantic fluency
Verbal memory
Case 1
13
F
Right
Intractable epilepsy; CBPS
3
Right side head and eye version
Motor: normal; poor attention; deficit executive functions
Speech severely delayed; poor language comprehension
Moderate to severe impaired range (IQ = 41; VCI
score=55; PRI score= 49; WMI score = 50; PSI
score=50) a
Mildly impaired (IQ = 64; VCI score = 82; POI score=67) b
Poor
Poor
None
Normal
Normal
Severely impaired (standard score ⬍40) d
Borderline (standard score = 71)
Poor, with relatively preserved delayed recall
Poor
Poor
None (not described)
Normal
Unable
Moderately impaired (standard score = 52)
Moderately impaired (standard score = 54)
Borderline (scale score = 5) e; good delayed recall (scale
score = 6) e
Borderline (scale score = 6) b
Impaired (scale score = 4) b
Borderline (scale score = 5) f;
very poor graphomotor skills (VMI standard
score = 45)
Impaired (digit span, scale score = 3) b
Moderately impaired (raw score = 7) g; better for delayed
recall (raw score = 10) g
Impaired (PSI standard score = 57)
Severely impaired: RH standard score ⬍40; LH standard
score ⱕ40 h
“Multiple cognitive domains impairment with a trend of
greater dysfunction of the nondominant hemisphere
[with] preserved mesiotemporal regions”
Interictal: bilateral temporal spikes and right temporal
slow waves; ictal: bilateral centrotemporal sharp slow
waves more prominent in the right side
Bilaterally poorly formed operculum; cortical thickening,
polymicrogyria in opercular and hippocampal regions
(Figure 1B); left cerebellar aplasia
Color-coded FA map: small and poorly defined SLFs
(Figure 5); fiber tractography: absence of the arcuate
fibers (Figure 6)
Left IOFF: 0.38 i/0.85
Right IOFF: 0.46/0.86
Left ILF and IOFF: 0.47/0.94
Right ILF and IOFF: 0.52/0.90
Left cingulum: 0.39 i/0.82
Right cingulum: 0.35 i/0.81
Left internal capsule: 0.53/0.78
Right internal capsule: 0.51/0.82
Verbal reasoning
Nonverbal reasoning
Constructional praxis
Severely impaired (scale score = 3) a
Severely impaired (scale score = 1) a
Poor (VMI standard score = 61; scale score = 1) a
Auditory working memory
Memory for faces
Severely impaired (digit span, scale score = 1) a
Borderline (scale score= 6) g; normal delayed recall (scale
score=9) g
Severely impaired (PSI standard score ⬍40)
Severely impaired bilaterally: RH standard score ⬍40;
LH standard score=unable to perform h
“Diffuse cerebral dysfunction, with relatively preserved
performance on measures associated with
mesiotemporal systems”
Interictal: right frontotemporal slowing; ictal: bilateral
central epileptiform activity
Visual psychomotor speed
Fine motor dexterity
Neuropsychological global
profile
EEG
MRI
DTI/tractography
Other associative tracts (FA/ADC)
Case 2
18
M
Right
Intractable epilepsy; CBPS
12
Right side head version, staring, jaw movements
Motor: normal, but with sucking and swallowing
problems as infant
Speech severely delayed; poor language comprehension
Bilateral opercular cortical malformation; thick cortex,
small gyri, abnormal sulcation (Figure 1A); left
cerebellum hypoplasia
Color-coded FA map: failure to demonstrate the SLF
bilaterally (Figure 4); bilateral abnormal IOFF
orientation (curved upward); lack of cerebellar fibers
Left IOFF: 0.33 i/0.88
Right IOFF: 0.53/0.81
Left ILF and IOFF: 0.48/0.84
Right ILF and IOFF: 0.47/0.89
Left cingulum: 0.44/0.76
Right cingulum: 0.40/0.80
Left internal capsule: 0.61/0.80
Right internal capsule: 0.55/0.82
Abbreviations: ADC, apparent diffusion coefficients; CBPS, congenital bilateral perisylvian syndrome; DTI, diffusion tensor imaging;
EEG, electroencephalography; FA, fractional anisotropy; IOFF, inferior occipitofrontal fasciculus; ILF, inferior longitudinal fasciculus; LH, left hand; MRI, magnetic
resonance imaging; POI, Perceptual Organization Index; PRI, Perceptual Reasoning Index; PSI, Processing Speed Index; RH, right hand; SLF, superior longitudinal
fasciculus; VCI, Verbal Comprehension Index; VMI, Beery-Buktenica Developmental Test of Visual-Motor Integration; WMI, Working Memory Index.
a Wechsler Intelligence Scale for Children–Fourth Edition Spanish Version.
b Wechsler Adult Intelligence Scale–Third Edition Full-Scale IQ.
c Conscious effort to correct mispronunciations.
d Multilingual Aphasia Examination Spanish Version.
e Wide Range Assessment of Memory and Learning, Second Edition.
f Wechsler Adult Intelligence Scale–Third Edition Block Design.
g NEPSY Memory for Faces subtest.
h Grooved Pegboard Test.
i Values lower than normal range accordingly with in-house standardization.
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A
B
A
P
Figure 1. T1-weighted axial magnetic resonance images showing main
findings of congenital bilateral perisylvian syndrome. A, Case 1. B, Case 2.
Notice the distinctive widening of the sylvian fissure with “exposure” of the
insula to the cortical surface and abnormal sulcation.
A
P
Figure 2. Normal appearance of the superior longitudinal fasciculus (arrows)
in a normal volunteer defined at this level as triangular green shapes lateral
to the blue descending fibers of the corticospinal tract.
Figure 3. Normal appearance of the superior longitudinal fasciculi and the
arcuate fasciculi in a normal volunteer. The superior longitudinal fasciculi
(double thin arrows), conformed by parietal fibers (arrowheads), and the
arcuate fasciculi (long single arrows). The superior longitudinal fasciculi on
the right side does not carry arcuate fibers. Red indicates left side;
yellow, right side; A, anterior; P, posterior.
COMMENT
performed in a 1.5-T scanner (Figure 1). A diffusion
weighting (b) of 800 s/mm2 was used. Fractional anisotropy and tractography was performed using VolumeOne software (http://www.volume-one.org/). The superior longitudinal fasciculus containing the arcuate
fasciculus fibers was sought in a coronal plane at the level
of the rostral aspect of the splenium. The tract appears
normally as a green triangle lateral to the blue descending fibers of the corticospinal tracts (Figure 2), from
where the arcuate fasciculus can be tracked (Figure 3).
This area was contoured bilaterally defining the seeding
region of interest (ROI). Tract propagation was terminated when the tract trajectory reached a voxel with fractional anisotropy less than 0.13 or when the angle between 2 consecutive steps was greater than 45°. Fractional
anisotropy and apparent diffusion coefficients values were
obtained from the inferior occipitofrontal fasciculi, cingulum (single coronal ROIs at the level of the anterior
commissure), the inferior longitudinal fasciculi in conjunction with the inferior occipitofrontal fasciculi (single
coronal ROI at the level of the retrosplenial surface), and
the internal capsules (single axial ROI at the level of the
thalamus) (Figures 4, 5, and 6).
The superior longitudinal fasciculus consists mainly of
the long curved fibers with posterior end points in the
temporal cortex and a bundle of rather horizontal fibers
whose posterior end points are located in the parietal lobe
(Figure 3). The curved fibers correspond to the arcuate
fasciculus, a tract considered crucial for the communication between receptive and expressive language brain
areas.5-7 Lesions of the arcuate fasciculus result in a deficiency in the capacity to repeat, a syndrome that has
been coined “conduction aphasia.” Other authors have
proposed that the arcuate fasciculus also plays a role in
intelligence8 and nonlanguage cognitive functions.9
The absence of the arcuate fasciculus in our 2 cases
provides an opportunity to look into its role. We were
more concerned in what has been preserved as opposed
to the deficit, since our cases have many other cortical
abnormalities that could be the cause of any cognitive
or motor deficiency. Looking at what has been preserved gives us an idea of what the arcuate fasciculus is
not involved in.
Automatized language (eg, reciting automatic series)
and delayed recall of verbal and nonverbal material was
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A
P
Figure 6. Tractography of the superior longitudinal fasciculi in case 2. The
tracts are color coded for laterality: red, left; yellow, right. Notice the absence
of the arcuate fasciculus component in both sides. A indicates anterior;
P, posterior.
Figure 4. Fractional anisotropy and color-coded directional map of case
1.The coronal cut location is similar to the one used for Figure 2. Notice the
absence of the green anteroposterior bundle lateral to the blue corticospinal
tract that defines the superior longitudinal fasciculus. Arrows point to the
estimated location they should appear.
Figure 5. Fractional anisotropy and color-coded directional map of case 2.
Rudimentary superior longitudinal fasciculi are observed in both sides
(arrows).
preserved in both patients. Strikingly, no report of conduction aphasia was mentioned. Therefore, at least for
these 2 patients, the arcuate fasciculus was not needed
for these functions. The common clinical findings in these
cases with arcuate fasciculus agenesis were delayed speech
development with poor articulation and poor prosody and
other aspects of speech. In addition, both patients showed
poor phonemic and semantic word generation, and difficulties in visuospatial, organization/assembly skills, that
may prompt a diagnosis of constructional apraxia.
The idea to attribute the phonological difficulties of
our patients merely to the arcuate fasciculus absence
seems supported by a recent report of intraoperative
electrophysiological studies that have shown the arcuate fasciculus transmits phonological cues.10,11 However, concomitant cortical and connectivity findings
confound this observation.
The role of the arcuate fasciculus (and the entire
superior longitudinal fasciculus) in speech and language
is not completely understood. Normal volunteers show a
longer left arcuate fasciculus, with more fibers, and
higher fractional anisotropy values. Moreover, in many
cases, the right arcuate fasciculus is nonexistent.12-14
Strikingly, left arcuate fasciculus dominance has been
reported in subjects with right hemisphere language
dominance.15 More recently, lateralization of the arcuate
fasciculus has been found correlated with the lateralization index of language determined by functional magnetic resonance imaging on patients with right but not
left temporal lobe epilepsy.16
We present for the first time, to our knowledge, 2 cases
of CBPS with bilateral absence of the arcuate fasciculi.
This finding analyzed in the context of the associated clinical findings may help to understand the clinical presentation of the condition and further expose language
organization.
Accepted for Publication: June 30, 2009.
Correspondence: Byron Bernal, MD, 3100 SW 62nd Ave,
Miami, FL 33176 ([email protected]).
Author Contributions: Study concept and design: Bernal.
Acquisition of data: Bernal, Rey, Dunoyer, and Shanbhag. Analysis and interpretation of data: Bernal, Rey, and
Altman. Drafting of the manuscript: Bernal, Rey, and Dunoyer. Critical revision of the manuscript for important intellectual content: Bernal, Rey, Shanbhag, and Altman. Administrative, technical, and material support: Dunoyer. Study
supervision: Bernal, Rey, and Altman.
Financial Disclosure: None reported.
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