Arcuate Fasciculus and Speech in Congenital Bilateral Perisylvian Syndrome

doi:10.1016/j.pediatrneurol.2010.11.006

Pediatric Neurology

Volume 44, Issue 4, April 2011, Pages 270-274

https://doi.org/10.1016/j.pediatrneurol.2010.11.006 Get rights and content

Standard magnetic resonance imaging can diagnose congenital bilateral perisylvian polymicrogyria, but is limited in explaining the heterogeneous clinical spectrum of the related congenital bilateral perisylvian syndrome, characterized by pseudobulbar dysfunction, developmental delay, and epilepsy. We analyzed arcuate fasciculi using diffusion tensor imaging, a major language tract in the perisylvian region interconnecting the Broca and Wernicke areas, and at high risk of becoming developmentally affected in this condition. Six patients with congenital bilateral perisylvian syndrome underwent diffusion tensor imaging and were evaluated. The arcuate fasciculus was manually isolated, using tractography. The tract was identified in three patients who had developed speech, and whose values for various diffusion parameters were similar to those in age-matched controls (patients/controls means: fractional anisotropy, 0.50/0.52; apparent diffusion coefficient, 0.0022/0.0022 mm²/second; P = ns for both). However, in three patients with severe impairment and no speech development, the arcuate fasciculus could not be identified by fiber-tracking. In this small series, the absence of arcuate fasciculi on diffusion tensor imaging correlated with a more severe phenotype, which cannot be appreciated via structural magnetic resonance imaging alone.

Introduction

Congenital bilateral perisylvian malformations, especially polymicrogyria, are known to cause the classic congenital bilateral perisylvian syndrome, characterized by pseudobulbar dysfunction, speech, motor, and cognitive delays, and epilepsy [1]. The syndrome is quite heterogeneous, with different degrees of neurologic impairment in affected individuals. Some studies suggest that the extent of the brain malformation and the severity of epilepsy are important predictors of disease severity [2], [3].

One study used 2-deoxy-2-[¹⁸F]fluoro-D-glucose positron emission tomography to demonstrate that the functional extent of brain abnormalities was greater than what was evident on standard magnetic resonance images of patients with unilateral and bilateral perisylvian polymicrogyria [4]. Another study, using diffusion tensor-magnetic resonance imaging, revealed significantly decreased fractional anisotropy values in the white matter subjacent to the abnormal cortical regions of patients with unilateral polymicrogyria [5]. However, individual tracts were not analyzed in that study. Because a major feature of developmental delay in congenital bilateral perisylvian syndrome is speech and language delay, we hypothesized that the arcuate fasciculus, a major language tract in close proximity to the perisylvian cortical region, may be affected in patients with congenital bilateral perisylvian syndrome.

The arcuate fasciculus in classic anatomic models of language connects the Broca speech and Wernicke comprehension centers in the left hemisphere, and when lesioned, may be responsible for conduction aphasia. The diffusion tensor-magnetic resonance imaging tractography approach has been useful in identifying this tract in vivo and increasing our knowledge of language function beyond the classic models. The arcuate fasciculus can be identified either in both hemispheres or in just the language-dominant hemisphere (left or right) of healthy subjects. Moreover, the properties of the arcuate fasciculus can be expressed using measured diffusion parameters, and correlated with specific cognitive abilities [6], [7], [8]. Therefore, we aimed to investigate the microstructural characteristics of the arcuate fasciculus using diffusion tensor-magnetic resonance imaging, and we postulated that abnormalities of this tract would correlate with speech development in patients with congenital bilateral perisylvian syndrome.

Section snippets

Patients

The study group consisted of six patients with congenital bilateral perisylvian syndrome who had been evaluated at the Division of Pediatric Neurology (Children’s Hospital of Michigan, Detroit, MI) because of developmental delay. Five were children (age range, 3-14 years; four boys), whereas one subject was a young adult (female, aged 20 years) (Table 1). Only patients undergoing diffusion tensor-magnetic resonance imaging as part of their magnetic resonance imaging protocol were included. The

Results

The arcuate fasciculus was identified in at least one hemisphere of three patients who had developed some degree of speech function, as determined by the history obtained and observations of the treating pediatric neurologist (Table 1). In these patients, the diffusion tensor imaging parameters were similar to those in the arcuate fasciculi of healthy, age-matched control subjects (n = 10), and they were not significantly different according to an independent-samples t test (mean fractional

Discussion

The most important finding of this study involved the identification of an arcuate fasciculus only in the group of patients with congenital bilateral perisylvian syndrome who exhibited some speech development by the time of the diffusion tensor-magnetic resonance imaging scan. In contrast, patients whose arcuate fasciculus was not identifiable exhibited a more severe disease phenotype and no speech development at all. These findings were consistent with our initial hypothesis.

The arcuate

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Cited by (20)

Functional dysregulation of the auditory cortex in bilateral perisylvian polymicrogyria: Multiparametric case analysis of the absent speech phenotype
2024, Cortex
The absence of speech is a clinical phenotype seen across neurodevelopmental syndromes, offering insights for neural language models. We present a case of bilateral perisylvian polymicrogyria (BPP) and complete absence of speech with considerable language comprehension and production difficulties. We extensively characterized the auditory speech perception and production circuitry by employing a multimodal neuroimaging approach. Results showed extensive cortical thickening in motor and auditory-language regions. The auditory cortex lacked sensitivity to speech stimuli despite relatively preserved thalamic projections yet had no intrinsic functional organization. Subcortical structures implicated in early stages of processing exhibited heightened sensitivity to speech. The arcuate fasciculus, a suggested marker of language in BPP, showed similar volume and integrity to a healthy control. The frontal aslant tract, linked to oromotor function, was partially reconstructed. These findings highlight the importance of assessing the auditory cortex beyond speech production structures to understand absent speech in BPP. Despite profound cortical alterations, the intrinsic motor network and motor-speech pathways remained largely intact. This case underscores the need for comprehensive phenotyping using multiple MRI modalities to uncover causes of severe disruption in language development.
Telencephalic Flexure and Malformations of the Lateral Cerebral (Sylvian) Fissure
2016, Pediatric Neurology
Citation Excerpt :
The insula is usually dysplastic as well.125-127 In addition, diffusion tensor imaging or fiber tractography often demonstrates agenesis or dysgenesis of the arcuate fasciculus,128-130 and some children have severe expressive language delay out of proportion to other developmental delays, consistent with this specific neuroanatomic defect.131 This finding is reminiscent of the looping or elongation of some fiber tracts with the bending of the telencephalon and rotation of the hippocampus as mentioned earlier.
After sagittal division of the prosencephalon at 4.5 weeks of gestation, the early fetal cerebral hemisphere bends or rotates posteroventrally from seven weeks of gestation. The posterior pole of the telencephalon thus becomes not the occipital but the temporal lobe as the telencephalic flexure forms the operculum and finally the lateral cerebral or Sylvian fissure. The ventral part is infolded to become the insula. The frontal and temporal lips of the Sylvian fissure, as well as the insula, all derive from the ventral margin of the primitive telencephalon, hence may be influenced by genetic mutations with a ventrodorsal gradient of expression. The telencephalic flexure also contributes to a shift of the hippocampus from a dorsal to a ventral position, the early rostral pole of the hippocampus becoming caudal and dorsal becoming ventral. The occipital horn is the most recent recess of the lateral ventricle, hence most vulnerable to anatomic variations that affect the calcarine fissure. Many major malformations include lack of telencephalic flexure (holoprosencephaly, extreme micrencephaly) or dysplastic Sylvian fissure (lissencephalies, hemimegalencephaly, schizencephaly). Although fissures and sulci are genetically programmed, mechanical forces of growth and volume expansion are proposed to be mainly extrinsic (including ventricles) for fissures and intrinsic for sulci. In fetal hydrocephalus, the telencephalic flexure is less affected because ventricular dilatation occurs later in gestation. Flexures can be detected prenatally by ultrasound and fetal magnetic resonance imaging and should be described neuropathologically in cerebral malformations.
DTI-based tractography of the arcuate fasciculus in patients with polymicrogyria and language disorders
2015, European Journal of Radiology
To assess the integrity of the arcuate fasciculus (AF) with diffusion tensor imaging (DTI) and tractography in patients with congenital polymicrogyria (PMG) and language disorders.
Twelve patients with PMG and 12 matched controls were prospectively evaluated with DTI (32 gradient encoding directions, b-value = 1000 s/mm²) at 3.0 T. The AF was virtually dissected with a deterministic streamline approach. DTI metrics included FA (fractional anisotropy), mean diffusivity (MD), axial diffusivity (AD) and radial diffusivity (RD). A subset of patients (n = 4) was evaluated to assess cognitive performance and language skills.
Qualitative evaluation revealed several abnormalities in tracts size and architecture in nearly all PMG patients. Remarkably, in 3 patients with bilateral PMG, the AF was not delineated on both hemispheres. In comparison to controls, patients exhibited significant decrease of FA (p = 0.003) in addition to increase of RD (p = 0.03) in the right AF, whereas there was significant increase of MD in the left AF (p = 0.04). All 4 patients with language evaluation had suboptimal performance on lexical fluency and prosodic linguistic.
DTI and tractography suggest that the AF is severely disrupted in patients with PMG, providing an anatomical in vivo substrate for the language disorders commonly associated with these cortical malformations.
Bilateral agenesis of arcuate fasciculus demonstrated by fiber tractography in congenital bilateral perisylvian syndrome
2015, Brain and Development
Citation Excerpt :
It could be speculated that the AF has a great importance in language development by facilitating the repetition of phonological clues, therefore it helps learning language and organizing speech [5]. Recently Saporta et al. demonstrated bilateral absence of AF in three cases of CBPS with more severe motor and cognitive impairments and no speech development [2]. In these three patients, global developmental delay and epileptic seizures were seen as seen in our patient.
Congenital bilateral perisylvian syndrome (CBPS) is a type of cortical developmental abnormality associated with distinctive clinical and imaging features. Clinical spectrum of this syndrome is quite heterogeneous, with different degrees of neurological impairment in affected individuals. High-definition magnetic resonance imaging (MRI) has a great importance in revealing the presence of CBPS, but is limited in elucidating the heterogeneous clinical spectrum. The arcuate fasciculus (AF) is a prominent language tract in the perisylvian region interconnecting Broca and Wernicke areas, and has a high probability of being affected developmentally in CBPS. Herein, we report a case of CBPS with investigation of AF using diffusion tensor imaging (DTI) and fiber tractography in relation to clinical findings. We postulated that proven absence of AF on DTI and fiber tractography would correlate with a severe phenotype of CBPS.
Applications of blood-oxygen-level-dependent functional magnetic resonance imaging and diffusion tensor imaging in epilepsy
2014, Neuroimaging Clinics of North America
Altered white matter connectivity and network organization in polymicrogyria revealed by individual gyral topology-based analysis
2014, NeuroImage
Citation Excerpt :
Based on these prior post-mortem and imaging studies, we propose structural connectivity and graph theoretical network analysis based on an individual's primary gyral pattern for a more accurate description of the network in PMG brains, overcoming the limitations of the atlas-based parcellation. Furthermore, we investigated whether the structural network changes were associated with regional distribution and extent of PMG involvement as well as language impairment (deficits in comprehension, production, and use of language), which is one of the typical features of developmental delay in PMG (Guerreiro et al., 2002; Saporta et al., 2011). In order to compare with an atlas-based approach, we performed supplementary network analysis based on FreeSurfer parcellation, which has been widely used for node definition (Cheng et al., 2012; Hagmann et al., 2008, 2010; Honey et al., 2009).
Polymicrogyria (PMG) is a cortical malformation characterized by multiple small gyri and altered cortical lamination, which may be associated with disrupted white matter connectivity. However, little is known about the topological patterns of white matter networks in PMG. We examined structural connectivity and network topology using individual primary gyral pattern-based nodes in PMG patients, overcoming the limitations of an atlas-based approach. Structural networks were constructed from structural and diffusion magnetic resonance images in 25 typically developing and 14 PMG subjects. The connectivity analysis for different fiber groups divided based on gyral topology revealed severely reduced connectivity between neighboring primary gyri (short U-fibers) in PMG, which was highly correlated with the regional involvement and extent of abnormal gyral folding. The patients also showed significantly reduced connectivity between distant gyri (long association fibers) and between the two cortical hemispheres. In relation to these results, gyral node-based graph theoretical analysis revealed significantly altered topological organization of the network (lower clustering and higher modularity) and disrupted network hub architecture in cortical association areas involved in cognitive and language functions in PMG patients. Furthermore, the network segregation in PMG patients decreased with the extent of PMG and the degree of language impairment. Our approach provides the first detailed findings and interpretations on altered cortical network topology in PMG related to abnormal cortical structure and brain function, and shows the potential for an individualized method to characterize network properties and alterations in connections that are associated with malformations of cortical development.

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Original ArticleArcuate Fasciculus and Speech in Congenital Bilateral Perisylvian Syndrome

Introduction

Section snippets

Patients

Results

Discussion

Lancet

Pediatr Neurol

Comput Methods Programs Biomed

Epilepsy Res

Am J Hum Genet

Brain Dev

Neuroimage

Syndromes of bilateral symmetrical polymicrogyria

AJNR

Congenital perisylvian dysfunction—Is it a spectrum?

Dev Med Child Neurol

Original Article
Arcuate Fasciculus and Speech in Congenital Bilateral Perisylvian Syndrome