Aphasia induced by gliomas growing in the ventrolateral frontal region: Assessment with diffusion MR tractography, functional MR imaging and neuropsychology

INTRODUCTION Lesions in the ventrolateral region of the dominant frontal lobe have been historically associated with aphasia. Recent imaging results suggest that frontal language regions extend beyond classically defined Broca's area to include the ventral precentral gyrus (VPCG) and the arcuate fasciculus (AF). Frontal gliomas offer a unique opportunity to identify structures that are essential for speech production. The aim of this prospective study was to investigate the correlation between language deficits and lesion location in patients with gliomas. METHODS Nineteen patients with glioma and 10 healthy subjects were evaluated with diffusion tensor imaging magnetic resonance (MR) tractography, functional MR (verb generation task) and the Aachener Aphasie Test. Patients were divided into two groups according to lesion location with respect to the ventral precentral sulcus: (i) anterior (n=8) with glioma growing in the inferior frontal gyrus (IFG) and underlying white matter; (ii) posterior (n=11) with glioma growing in the VPCG and underlying white matter. Virtual dissection of the AF, frontal intralobar tract, uncinate fasciculus (UF) and inferior frontal occipital fasciculus (IFOF) was performed with a deterministic approach. RESULTS Seven posterior patients showed aphasia classified as conduction (4), Broca (1), transcortical motor (1) and an isolated deficit of semantic fluency; one anterior patient had transcortical mixed aphasia. All posterior patients had invasion of the VPCG, however only patients with aphasia had also lesion extension to the AF as demonstrated by tractography dissections. All patients with language deficits had high grade glioma. Groups did not differ regarding tumour volume. A functional pars opercularis was identified with functional MR imaging (fMRI) in 17 patients. CONCLUSIONS Gliomas growing in the left VPCG are much more likely to cause speech deficits than gliomas infiltrating the IFG, including Broca's area. Lesion extension to the AF connecting frontal to parietal and temporal regions is an important mechanism for the appearance of aphasia.

[1]  N. Geschwind Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[2]  Abraham Z. Snyder,et al.  Word Retrieval Learning Modulates Right Frontal Cortex in Patients with Left Frontal Damage , 2002, Neuron.

[3]  K. Hasan,et al.  Language Dysfunction After Stroke and Damage to White Matter Tracts Evaluated Using Diffusion Tensor Imaging , 2008, American Journal of Neuroradiology.

[4]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[5]  M. Brell,et al.  Estimulación cortical intraoperatoria en el tratamiento quirúrgico de los gliomas de bajo grado situados en áreas elocuentes , 2003 .

[6]  A. Ardila,et al.  The role of the arcuate fasciculus in conduction aphasia. , 2009, Brain : a journal of neurology.

[7]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[8]  M. Ruge,et al.  Intraoperative mapping of language functions: a longitudinal neurolinguistic analysis. , 2008, Journal of neurosurgery.

[9]  M. Catani,et al.  The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state , 2008, Cortex.

[10]  M. Desmurget,et al.  Contrasting acute and slow-growing lesions: a new door to brain plasticity. , 2006, Brain : a journal of neurology.

[11]  A. Thiel,et al.  From the left to the right: How the brain compensates progressive loss of language function , 2006, Brain and Language.

[12]  J. M. Anderson,et al.  Conduction Aphasia and the Arcuate Fasciculus: A Reexamination of the Wernicke–Geschwind Model , 1999, Brain and Language.

[13]  Matthew P. G. Allin,et al.  Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography , 2011, NeuroImage.

[14]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[15]  Christopher Nimsky,et al.  Combining fMRI and MEG increases the reliability of presurgical language localization: A clinical study on the difference between and congruence of both modalities , 2006, NeuroImage.

[16]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[17]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[18]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[19]  M. Annett The Binomial Distribution of Right, Mixed and Left Handedness , 1967, The Quarterly journal of experimental psychology.

[20]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[21]  Cornelius Weiller,et al.  How the ventral pathway got lost – And what its recovery might mean , 2011, Brain and Language.

[22]  E. Cabanis,et al.  Paul Broca's historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. , 2007, Brain : a journal of neurology.

[23]  D. Pandya,et al.  The extreme capsule in humans and rethinking of the language circuitry , 2009, Brain Structure and Function.

[24]  K Herholz,et al.  Plasticity of language networks in patients with brain tumors: A positron emission tomography activation study , 2001, Annals of neurology.

[25]  Angela D. Friederici,et al.  Pathways to language: fiber tracts in the human brain , 2009, Trends in Cognitive Sciences.

[26]  Hugues Duffau,et al.  The “frontal syndrome” revisited: Lessons from electrostimulation mapping studies , 2012, Cortex.

[27]  A. Bizzi,et al.  Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. , 2008, Radiology.

[28]  U. Ebeling,et al.  Circumscribed low grade astrocytomas in the dominant opercular and insular region: A pilot study , 2005, Acta Neurochirurgica.

[29]  Angela D. Friederici,et al.  Allocating functions to fiber tracts: facing its indirectness , 2009, Trends in Cognitive Sciences.

[30]  Matthew A. Lambon Ralph,et al.  Arcuate fasciculus variability and repetition: The left sometimes can be right , 2012, Cortex.

[31]  A. Nobre,et al.  Dissociating Linguistic Processes in the Left Inferior Frontal Cortex with Transcranial Magnetic Stimulation , 2022 .

[32]  W. Penfield,et al.  Speech and Brain‐Mechanisms , 1960 .

[33]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[34]  A. Ardila,et al.  Repetition in aphasia , 1992, Journal of Neurolinguistics.

[35]  Cornelius Weiller,et al.  Please don’t underestimate the ventral pathway in language , 2009, Trends in Cognitive Sciences.

[36]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[37]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[38]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. 1989. , 2008, Journal of neurosurgery.

[39]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[40]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[41]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[42]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[43]  Mitchel S Berger,et al.  Functional outcome after language mapping for glioma resection. , 2008, The New England journal of medicine.

[44]  Angela D. Friederici,et al.  Who did what to whom? The neural basis of argument hierarchies during language comprehension , 2005, NeuroImage.

[45]  K. Boulanouar,et al.  Language Functional Magnetic Resonance Imaging in Preoperative Assessment of Language Areas: Correlation with Direct Cortical Stimulation , 2003, Neurosurgery.

[46]  M. Berger,et al.  Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the Broca area. , 2003, Journal of neurosurgery.

[47]  A. Thiel,et al.  Essential language function of the right hemisphere in brain tumor patients , 2005, Annals of neurology.

[48]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[49]  Marcella Laiacona,et al.  Tre test clinici di ricerca e produzione lessicale , 1986 .

[50]  C. Wernicke Der aphasische Symptomencomplex: Eine psychologische Studie auf anatomischer Basis , 1874 .

[51]  J. Ilmberger,et al.  Surgical resection of gliomas WHO grade II and III located in the opercular region , 2004, Acta Neurochirurgica.

[52]  H. Funkenstein,et al.  Broca aphasia , 1978, Neurology.

[53]  Wilhelm Eisner,et al.  Surgical Resection of Grade II Astrocytomas in the Superior Frontal Gyrus , 2002, Neurosurgery.

[54]  Manuel Lopes,et al.  Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study. , 2002, Brain : a journal of neurology.

[55]  J W Belliveau,et al.  Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. , 1997, AJNR. American journal of neuroradiology.

[56]  P. Broca Remarques sur le siège de la faculté du langage articulé, suivies d'une observation d'aphémie (perte de la parole) , 1861 .

[57]  Franck-Emmanuel Roux,et al.  What Makes Surgical Tumor Resection Feasible in Broca's Area? Insights Into Intraoperative Brain Mapping , 2010, Neurosurgery.

[58]  The aachen aphasia test aat ii psychometric properties of the italian version , 1987 .

[59]  Patrizia Bisiacchi,et al.  L'aachner Aphasie Test (Aat) II. Proprietà Psicometriche Della Versione Italiana , 1987 .

[60]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[61]  M. Catani,et al.  Monkey to human comparative anatomy of the frontal lobe association tracts , 2012, Cortex.

[62]  Costanza Papagno,et al.  What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. , 2011, Brain : a journal of neurology.

[63]  U. Ebeling,et al.  Surgery of astrocytomas in the motor and premotor cortex under local anesthesia: report of 11 cases. , 1995, Minimally invasive neurosurgery : MIN.

[64]  Laurent Capelle,et al.  Preferential brain locations of low‐grade gliomas , 2004, Cancer.

[65]  Derek K. Jones Studying connections in the living human brain with diffusion MRI , 2008, Cortex.

[66]  G A Ojemann,et al.  Individual variability in cortical localization of language. , 1979, Journal of neurosurgery.

[67]  M E Meyerand,et al.  Reliability of functional MR imaging with word-generation tasks for mapping Broca's area. , 2001, AJNR. American journal of neuroradiology.

[68]  Michel Thiebaut de Schotten,et al.  Short frontal lobe connections of the human brain , 2012, Cortex.

[69]  A. Thiel,et al.  Role of the Contralateral Inferior Frontal Gyrus in Recovery of Language Function in Poststroke Aphasia: A Combined Repetitive Transcranial Magnetic Stimulation and Positron Emission Tomography Study , 2005, Stroke.

[70]  R. Cox,et al.  Functional MR activation correlated with intraoperative cortical mapping. , 1997, AJNR. American journal of neuroradiology.

[71]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[72]  Antoine Rosset,et al.  Informatics in radiology (infoRAD): navigating the fifth dimension: innovative interface for multidimensional multimodality image navigation. , 2006, Radiographics : a review publication of the Radiological Society of North America, Inc.

[73]  Stefan Klöppel,et al.  Early functional magnetic resonance imaging activations predict language outcome after stroke. , 2010, Brain : a journal of neurology.

[74]  Keith D. White,et al.  Structural connectivity of Broca's area and medial frontal cortex , 2010, NeuroImage.

[75]  H Duffau,et al.  Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation , 2003, Journal of neurology, neurosurgery, and psychiatry.

[76]  Simon B. Eickhoff,et al.  Specialisation in Broca's region for semantic, phonological, and syntactic fluency? , 2008, NeuroImage.

[77]  C. Papagno,et al.  INTRAOPERATIVE SUBCORTICAL LANGUAGETRACT MAPPING GUIDES SURGICAL REMOVALOF GLIOMAS INVOLVING SPEECH AREAS , 2007, Neurosurgery.

[78]  Ernst Nennig,et al.  Localizing and lateralizing language in patients with brain tumors: feasibility of routine preoperative functional MR imaging in 81 consecutive patients. , 2007, Radiology.

[79]  A. Anwander,et al.  Connectivity-Based Parcellation of Broca's Area. , 2006, Cerebral cortex.

[80]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[81]  Stefan Klöppel,et al.  Combining Functional and Anatomical Connectivity Reveals Brain Networks for Auditory Language Comprehension , 2022 .

[82]  Hugues Duffau,et al.  RESECTION OF WORLD HEALTH ORGANIZATION GRADE II GLIOMAS INVOLVING BROCA'S AREA: METHODOLOGICAL AND FUNCTIONAL CONSIDERATIONS , 2007, Neurosurgery.