0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Observation |

Agenesis of the Arcuate Fasciculi in Congenital Bilateral Perisylvian Syndrome A Diffusion Tensor Imaging and Tractography Study FREE

Byron Bernal, MD; Gustavo Rey, PhD; Catalina Dunoyer, MD; Harshad Shanbhag, MS; Nolan Altman, MD
[+] Author Affiliations

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.


Arch Neurol. 2010;67(4):501-505. doi:10.1001/archneurol.2010.59.
Text Size: A A A
Published online

ABSTRACT

Objective  To describe the absence of the arcuate fasciculi in 2 cases of congenital bilateral perisylvian syndrome (CBPS).

Design  Case series.

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.

Main Outcome Measures  Neuropsychology evaluation; fractional anisotropy, apparent diffusion coefficients, and anatomical aspect of the tracts.

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.

Conclusion  Agenesis of the arcuate fasciculus may accompany CBPS.

Figures in this Article

The 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/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 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 Volume-One 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).

Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 5.

Fractional anisotropy and color-coded directional map of case 2. Rudimentary superior longitudinal fasciculi are observed in both sides (arrows).

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location

COMMENT

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.57 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 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.1214 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.

ARTICLE INFORMATION

Correspondence: Byron Bernal, MD, 3100 SW 62nd Ave, Miami, FL 33176 (byron.bernal@mch.com).

Accepted for Publication: June 30, 2009.

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.

REFERENCES

Gropman  ALBarkovich  AJVezina  LGConry  JADubovsky  ECPacker  RJ Pediatric congenital bilateral perisylvian syndrome: clinical and MRI features in 12 patients. Neuropediatrics 1997;28 (4) 198- 203
PubMed Link to Article
Kuzniecky  RAndermann  FGuerrini  R The epileptic spectrum in the congenital bilateral perisylvian syndrome: CBPS Multicenter Collaborative Study. Neurology 1994;44 (3, pt 1) 379- 385
PubMed Link to Article
Guerrini  RCarrozzo  R Epileptogenic brain malformations: clinical presentation, malformative patterns and indications for genetic testing. Seizure 2002;11(suppl A)532- 543
PubMed
Guerrini  R Genetic malformations of the cerebral cortex and epilepsy. Epilepsia 2005;46(suppl 1)32- 37
PubMed Link to Article
Geschwind  N Disconnexion syndromes in animals and man: II. Brain 1965;88 (3) 585- 644
PubMed Link to Article
Geschwind  N The organization of language and the brain. Science 1970;170 (961) 940- 944
PubMed Link to Article
Wernicke  C The aphasic symptom complex: a psychological study on a neurological basis. Boston Stud Philos Sci 1874;4
Jung  REHaier  RJ The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 2007;30 (2) 135- 154
PubMed Link to Article
Sundaram  SKSivaswamy  LMakki  MIBehen  MEChugani  HT Absence of arcuate fasciculus in children with global developmental delay of unknown etiology: a diffusion tensor imaging study. J Pediatr 2008;152 (2) 250- 255
PubMed Link to Article
Mandonnet  ENouet  AGatignol  PCapelle  LDuffau  H Does the left inferior longitudinal fasciculus play a role in language? a brain stimulation study. Brain 2007;130 (pt 3) 623- 629
PubMed Link to Article
Duffau  HPeggy Gatignol  STMandonnet  ECapelle  LTaillandier  L Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with grade II glioma in the left dominant hemisphere. J Neurosurg 2008;109 (3) 461- 471
PubMed Link to Article
Powell  HWParker  GJAlexander  DC  et al.  Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage 2006;32 (1) 388- 399
PubMed Link to Article
Nucifora  PGVerma  RMelhem  ERGur  REGur  RC Leftward asymmetry in relative fiber density of the arcuate fasciculus. Neuroreport 2005;16 (8) 791- 794
PubMed Link to Article
Parker  GJLuzzi  SAlexander  DCWheeler-Kingshott  CACiccarelli  OLambon Ralph  MA Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 2005;24 (3) 656- 666
PubMed Link to Article
Vernooij  MWSmits  MWielopolski  PAHouston  GCKrestin  GPvan der Lugt  A Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: a combined fMRI and DTI study. Neuroimage 2007;35 (3) 1064- 1076
PubMed Link to Article
Rodrigo  SOppenheim  CChassoux  F  et al.  Language lateralization in temporal lobe epilepsy using functional MRI and probabilistic tractography. Epilepsia 2008;49 (8) 1367- 1376
PubMed Link to Article

Figures

Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 5.

Fractional anisotropy and color-coded directional map of case 2. Rudimentary superior longitudinal fasciculi are observed in both sides (arrows).

Graphic Jump Location
Place holder to copy figure label and caption
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.

Graphic Jump Location

References

Gropman  ALBarkovich  AJVezina  LGConry  JADubovsky  ECPacker  RJ Pediatric congenital bilateral perisylvian syndrome: clinical and MRI features in 12 patients. Neuropediatrics 1997;28 (4) 198- 203
PubMed Link to Article
Kuzniecky  RAndermann  FGuerrini  R The epileptic spectrum in the congenital bilateral perisylvian syndrome: CBPS Multicenter Collaborative Study. Neurology 1994;44 (3, pt 1) 379- 385
PubMed Link to Article
Guerrini  RCarrozzo  R Epileptogenic brain malformations: clinical presentation, malformative patterns and indications for genetic testing. Seizure 2002;11(suppl A)532- 543
PubMed
Guerrini  R Genetic malformations of the cerebral cortex and epilepsy. Epilepsia 2005;46(suppl 1)32- 37
PubMed Link to Article
Geschwind  N Disconnexion syndromes in animals and man: II. Brain 1965;88 (3) 585- 644
PubMed Link to Article
Geschwind  N The organization of language and the brain. Science 1970;170 (961) 940- 944
PubMed Link to Article
Wernicke  C The aphasic symptom complex: a psychological study on a neurological basis. Boston Stud Philos Sci 1874;4
Jung  REHaier  RJ The Parieto-Frontal Integration Theory (P-FIT) of intelligence: converging neuroimaging evidence. Behav Brain Sci 2007;30 (2) 135- 154
PubMed Link to Article
Sundaram  SKSivaswamy  LMakki  MIBehen  MEChugani  HT Absence of arcuate fasciculus in children with global developmental delay of unknown etiology: a diffusion tensor imaging study. J Pediatr 2008;152 (2) 250- 255
PubMed Link to Article
Mandonnet  ENouet  AGatignol  PCapelle  LDuffau  H Does the left inferior longitudinal fasciculus play a role in language? a brain stimulation study. Brain 2007;130 (pt 3) 623- 629
PubMed Link to Article
Duffau  HPeggy Gatignol  STMandonnet  ECapelle  LTaillandier  L Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with grade II glioma in the left dominant hemisphere. J Neurosurg 2008;109 (3) 461- 471
PubMed Link to Article
Powell  HWParker  GJAlexander  DC  et al.  Hemispheric asymmetries in language-related pathways: a combined functional MRI and tractography study. Neuroimage 2006;32 (1) 388- 399
PubMed Link to Article
Nucifora  PGVerma  RMelhem  ERGur  REGur  RC Leftward asymmetry in relative fiber density of the arcuate fasciculus. Neuroreport 2005;16 (8) 791- 794
PubMed Link to Article
Parker  GJLuzzi  SAlexander  DCWheeler-Kingshott  CACiccarelli  OLambon Ralph  MA Lateralization of ventral and dorsal auditory-language pathways in the human brain. Neuroimage 2005;24 (3) 656- 666
PubMed Link to Article
Vernooij  MWSmits  MWielopolski  PAHouston  GCKrestin  GPvan der Lugt  A Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: a combined fMRI and DTI study. Neuroimage 2007;35 (3) 1064- 1076
PubMed Link to Article
Rodrigo  SOppenheim  CChassoux  F  et al.  Language lateralization in temporal lobe epilepsy using functional MRI and probabilistic tractography. Epilepsia 2008;49 (8) 1367- 1376
PubMed Link to Article

Correspondence

CME
Also Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
Please click the checkbox indicating that you have read the full article in order to submit your answers.
Your answers have been saved for later.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.

Multimedia

Some tools below are only available to our subscribers or users with an online account.

1,148 Views
10 Citations
×

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Collections
Jobs