Speech network regional involvement in bulbar ALS: a multimodal structural MRI study

References

• Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH. Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2009;10:131–46.
   Google Scholar
• Strong MJ, Abrahams S, Goldstein LH, Woolley S, Mclaughlin P, Snowden J, et al. Amyotrophic lateral sclerosis-frontotemporal spectrum disorder (ALS-FTSD): Revised diagnostic criteria. Amyotroph Lateral Scler Frontotemp Degener. 2017;18:153–74.
   Google Scholar
• Strong MJ, Grace GM, Orange JB, Leeper HA, Menon RS, Aere C. A prospective study of cognitive impairment in ALS. Neurology. 1999;53:1665–70.
   Google Scholar
• Flaherty-Craig C, Eslinger P, Stephens B, Simmons Z. A rapid screening battery to identify frontal dysfunction in patients with ALS. Neurology. 2006;67:2070–2.
   Google Scholar
• Kew JJ, Goldstein LH, Leigh PN, Abrahams S, Cosgrave N, Passingham RE, et al. The relationship between abnormalities of cognitive function and cerebral activation in amyotrophic lateral sclerosis: a neuropsychological and positron emission tomography study. Brain. 1993;116:1399–423.
   Google Scholar
• Abrahams S, Leigh PN, Harvey A, Vythelingum GN, Grise D, Goldstein LH. Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia. 2000;38:734–47.
   Google Scholar
• Abrahams S, Leigh PN, Goldstein LH. Cognitive change in ALS: a prospective study. Neurology. 2005;64:1222–6.
   Google Scholar
• Ichikawa H, Takahashi N, Hieda S, Hideki O, Kawamura M. Agraphia in bulbar-onset amyotrophic lateral sclerosis: not merely a consequence of dementia or aphasia. Behav Neurol. 2008;20:91–9.
   Google Scholar
• Yoshizawa K, Yasuda N, Fukuda M, Yukimoto Y, Ogino M, Hata W, et al. Syntactic comprehension in patients with amyotrophic lateral sclerosis. Behav Neurol. 2014;2014:1.
   Google Scholar
• Gordon PH, Goetz RR, Rabkin JG, Dalton K, Mcelhiney M, Hays AP, et al. A prospective cohort study of neuropsychological test performance in ALS. Amyotroph Lateral Scler. 2010;11:312–20.
   Google Scholar
• Phukan J, Pender NP, Hardiman O. Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol. 2007;6:994–1003.
   Google Scholar
• Elamin M, Pinto-Grau M, Burke T, Bede P, Rooney J, O’Sullivan M, et al. Identifying behavioural changes in ALS: validation of the Beaumont Behavioural Inventory (BBI). Amyotroph Lateral Scler Frontotemp Degener. 2017;18:68–73.
   Google Scholar
• Abrahams S, Newton J, Niven E, Foley J, Bak TH. Screening for cognition and behaviour changes in ALS. Amyotroph Lateral Scler Frontotemp Degener. 2014;15:9–14.
   Google Scholar
• Pinto-Grau M, Hardiman O, Pender N. The study of language in the amyotrophic lateral sclerosis-frontotemporal spectrum disorder: a systematic review of findings and new perspectives. Neuropsychol Rev. 2018;28:251–68.
   Google Scholar
• Leslie FV, Hsieh S, Caga J, Savage SA, Mioshi E, Hornberger M, et al. Semantic deficits in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemp Degener. 2015;16:46–53.
   Google Scholar
• Abrahams S. Executive dysfunction in ALS is not the whole story. J Neurol Neurosurg Psychiatry. 2013;84:474–5.
   Google Scholar
• Phukan J, Elamin M, Bede P, Jordan N, Gallagher L, Byrne S, et al. The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J Neurol Neurosurg Psychiatry. 2012;83:102–8.
   Google Scholar
• Taylor LJ, Brown RG, Tsermentseli S, Al-Chalabi A, Shaw CE, Ellis CM, et al. Is language impairment more common than executive dysfunction in amyotrophic lateral sclerosis? J Neurol Neurosurg Psychiatry. 2013;84:494–8.
   Google Scholar
• Tsermentseli S, Leigh PN, Taylor LJ, Radunovic A, Catani M, Goldstein LH. Syntactic processing as a marker for cognitive impairment in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemp Degener. 2016;17:69–76.
   Google Scholar
• Massman PJ, Sims J, Cooke N, Haverkamp LJ, Appel V, Appel SH. Prevalence and correlates of neuropsychological deficits in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1996;61:450–5.
   Google Scholar
• Sterling LE, Jawaid A, Salamone AR, Murthy SB, Mosnik DM, McDowell E, et al. Association between dysarthria and cognitive impairment in ALS: a prospective study. Amyotroph Lateral Scler. 2010;11:46–51.
   Google Scholar
• Neary D, Snowden JS, Mann D. Cognitive change in motor neurone disease/amyotrophic lateral sclerosis (MND/ALS). J Neurol Sci. 2000;180:15–20.
   Google Scholar
• Ogawa T, Tanaka H, Hirata K. Cognitive deficits in amyotrophic lateral sclerosis evaluated by event-related potentials. Clin Neurophysiol. 2009;120:659–64.
   Google Scholar
• Piao YS, Wakabayashi K, Kakita A, Yamada M, Hayashi S, Morita T, et al. Neuropathology with clinical correlations of sporadic amyotrophic lateral sclerosis: 102 autopsy cases examined between 1962 and 2000. Brain Pathol. 2006;13:10–22.
   Google Scholar
• Buchanan CR, Pettit LD, Storkey AJ, Abrahams S, Bastin ME. Reduced structural connectivity within a prefrontal‐motor‐subcortical network in amyotrophic lateral sclerosis. J Magn Reson Imaging. 2015;41:1342–52.
   Google Scholar
• Verstraete E, Veldink JH, van den Berg LH, van den Heuvel MP. Structural brain network imaging shows expanding disconnection of the motor system in amyotrophic lateral sclerosis. Hum Brain Mapp. 2014;35:1351–61.
   Google Scholar
• Bede P, Bokde A, Elamin M, Byrne S, McLaughlin RL, Jordan N, et al. Grey matter correlates of clinical variables in amyotrophic lateral sclerosis (ALS): a neuroimaging study of ALS motor phenotype heterogeneity and cortical focality. J Neurol Neurosurg Psychiatry. 2013;84:766–73.
   Google Scholar
• Schuster C, Kasper E, Dyrba M, Machts J, Bittner D, Kaufmann J, et al. Cortical thinning and its relation to cognition in amyotrophic lateral sclerosis. Neurobiol Aging. 2014;35:240–6.
   Google Scholar
• Schuster C, Kasper E, Machts J, Bittner D, Kaufmann J, Benecke R, et al. Focal thinning of the motor cortex mirrors clinical features of amyotrophic lateral sclerosis and their phenotypes: a neuroimaging study. J Neurol. 2013;260:2856–64.
   Google Scholar
• Iwata NK, Aoki S, Masutani Y, Yoshida M, Okabe S, Arai N, et al. Corticospinal tract and corticobulbar tract dysfunction in ALS: combined study using transcranial magnetic stimulation and diffusion tensor tractography. Int Cong Ser. 2005;1278:181–4.
   Google Scholar
• Aoki S, Iwata NK, Masutani Y, Yoshida M, Abe O, Ugawa Y, et al. Quantitative evaluation of the pyramidal tract segmented by diffusion tensor tractography: feasibility study in patients with amyotrophic lateral sclerosis. Radiat Med. 2005;23:195–9.
   Google Scholar
• Ellis CM, Simmons A, Jones DK, Bland J, Dawson JM, Horsfield MA, et al. Diffusion tensor MRI assesses corticospinal tract damage in ALS. Neurology. 1999;53:1051–8.
   Google Scholar
• Prell T, Peschel T, Hartung V, Kaufmann J, Klauschies R, Bodammer N, et al. Diffusion tensor imaging patterns differ in bulbar and limb onset amyotrophic lateral sclerosis. Clin Neurol Neurosurg. 2013;115:1281–7.
   Google Scholar
• Agosta F, Rocca M, Valsasina P, Sala S, Caputo D, Perini M, et al. A longitudinal diffusion tensor MRI study of the cervical cord and brain in amyotrophic lateral sclerosis patients. J Neurol Neurosurg Psychiatry. 2009;80:53–5.
   Google Scholar
• Cardenas-Blanco A, Machts J, Acosta-Cabronero J, Kaufmann J, Abdulla S, Kollewe K, et al. Central white matter degeneration in bulbar-and limb-onset amyotrophic lateral sclerosis. J Neurol. 2014;261:1961–7.
   Google Scholar
• Menke RA, Körner S, Filippini N, Douaud G, Knight S, Talbot K, et al. Widespread grey matter pathology dominates the longitudinal cerebral MRI and clinical landscape of amyotrophic lateral sclerosis. Brain. 2014;137:2546–55.
   Google Scholar
• Roccatagliata L, Bonzano L, Mancardi G, Canepa C, Caponnetto C. Detection of motor cortex thinning and corticospinal tract involvement by quantitative MRI in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2009;10:47–52.
   Google Scholar
• Chen Z, Liu M, Ma L. Gray matter volume changes over the whole brain in the bulbar-and spinal-onset amyotrophic lateral sclerosis: a voxel-based morphometry study. Chin Med Sci J. 2018;33:20–8.
   Google Scholar
• Verstraete E, Veldink JH, Hendrikse J, Schelhaas HJ, van den Heuvel MP, van den Berg LH. Structural MRI reveals cortical thinning in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2012;83:383–8.
   Google Scholar
• Allison KM, Yunusova Y, Campbell TF, Wang J, Berry JD, Green JR. The diagnostic utility of patient-report and speech-language pathologists’ ratings for detecting the early onset of bulbar symptoms due to ALS. Amyotroph Lateral Scler Frontotemp Degener. 2017;18:358–66.
   Google Scholar
• Fuertinger S, Horwitz B, Simonyan K. The functional connectome of speech control. PLoS Biol. 2015;13:e1002209.
   Google Scholar
• Zhu L, Fan Y, Zou Q, Wang J, Gao J-H, Niu Z. Temporal reliability and lateralization of the resting-state language network. PLoS One. 2014;9:e85880.
   Google Scholar
• Tyler LK, Marslen-Wilson W. Fronto-temporal brain systems supporting spoken language comprehension. Philos Trans R Soc Lond B Biol Sci. 2008;363:1037–54.
   Google Scholar
• Dronkers NF, Wilkins DP, Van Valin RD, Jr Redfern BB, Jaeger JJ. Lesion analysis of the brain areas involved in language comprehension. Cognition. 2004;92:145–77.
   Google Scholar
• Vassal F, Schneider F, Boutet C, Jean B, Sontheimer A, Lemaire J-J. Combined DTI tractography and functional MRI study of the language connectome in healthy volunteers: extensive mapping of white matter fascicles and cortical activations. PLoS One. 2016;11:e0152614.
   Google Scholar
• Bohland JW, Guenther FH. An fMRI investigation of syllable sequence production. Neuroimage. 2006;32:821–41.
   Google Scholar
• Hickok G, Okada K, Serences JT. Area Spt in the human planum temporale supports sensory-motor integration for speech processing. J Neurophysiol. 2009;101:2725–32.
   Google Scholar
• Guenther FH, Vladusich T. A neural theory of speech acquisition and production. J Neurolinguistics. 2012;25:408–22.
   Google Scholar
• Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007;8:393.
   Google Scholar
• Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1:293–9.
   Google Scholar
• Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53:695–9.
   Google Scholar
• Gillingham SM, Yunusova Y, Ganda A, Rogaeva E, Black S, Stuss D, et al. Assessing cognitive functioning in ALS: A focus on frontal lobe processes. Amyotroph Lateral Scler Frontotemp Degener. 2017;18:182–92.
   Google Scholar
• Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, et al. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci. 1999;169:13–21.
   Google Scholar
• Rong P, Yunusova Y, Wang J, Green JR. Predicting early bulbar decline in amyotrophic lateral sclerosis: a speech subsystem approach. Behav Neurol. 2015;2015:1.
   Google Scholar
• Beck M, Giess R, Würffel W, Magnus T, Ochs G, Toyka KV. Comparison of maximal voluntary isometric contraction and Drachman's hand‐held dynamometry in evaluating patients with amyotrophic lateral sclerosis. Muscle Nerve. 1999;22:1265–70.
   Google Scholar
• Sevene TG, Berning J, Harris C, Climstein M, Adams KJ, DeBeliso M. Hand grip strength and gender: allometric normalization in older adults and implications for the NIOSH lifting equation. J Lifestyle Med. 2017;7:63.
   Google Scholar
• Kovacevic N, Lobaugh N, Bronskill M, Levine B, Feinstein A, Black S. A robust method for extraction and automatic segmentation of brain images. Neuroimage. 2002;17:1087–100.
   Google Scholar
• Levy-Cooperman N, Ramirez J, Lobaugh NJ, Black SE. Misclassified tissue volumes in Alzheimer disease patients with white matter hyperintensities importance of lesion segmentation procedures for volumetric analysis. Stroke. 2008;39:1134–41.
   Google Scholar
• Ramirez J, Gibson E, Quddus A, Lobaugh NJ, Feinstein A, Levine B, et al. Lesion Explorer: a comprehensive segmentation and parcellation package to obtain regional volumetrics for subcortical hyperintensities and intracranial tissue. Neuroimage. 2011;54:963–73.
   Google Scholar
• Ramirez J, Scott CJ, Black SE. A short-term scan-rescan reliability test measuring brain tissue and subcortical hyperintensity volumetrics obtained using the lesion explorer structural MRI processing pipeline. Brain Topogr. 2013;26:35–8.
   Google Scholar
• Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage. 2006;31:968–80.
   Google Scholar
• Salat DH, Greve DN, Pacheco JL, Quinn BT, Helmer KG, Buckner RL, et al. Regional white matter volume differences in nondemented aging and Alzheimer's disease. Neuroimage. 2009;44:1247–58.
   Google Scholar
• Agosta F, Canu E, Valsasina P, Riva N, Prelle A, Comi G, et al. Divergent brain network connectivity in amyotrophic lateral sclerosis. Neurobiol Aging.
   Google Scholar
• Chan F, Armstrong IT, Pari G, Riopelle RJ, Munoz DP. Deficits in saccadic eye-movement control in Parkinson's disease. Neuropsychologia. 2005;43:784–96.
   Google Scholar
• Grosskreutz J, Kaufmann J, Fradrich J, Dengler R, Heinze H, Peschel T. Widespread sensorimotor and frontal cortical atrophy in Amyotrophic lateral sclerosis. BMC Neurol. 2006;6:1–10.
   Google Scholar
• Kassubek J, Unrath A, Huppertz H, Lule D, Ethofer T, Sperfeld AD, et al. Global brain atrophy and corticospinal tract alterations in ALS, as investigated by voxel-based morphometry of 3-D MRI. Amyotroph Lateral Scler Other Motor Neuron Disord. 2005;6:213–20.
   Google Scholar
• Turner MR, Hammers A, Allsop J, Al-Chalabi A, Shaw CE, Brooks DJ, et al. Volumetric cortical loss in sporadic and familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2007;8:343–7.
   Google Scholar
• Verstraete E, van den Heuvel MP, Veldink JH, Blanken N, Mandl RC, Hulshoff Pol HE, et al. Motor Network Degeneration in Amyotrophic Lateral Sclerosis: A Structural and Functional Connectivity Study. PLoS One. 2010;5:e13664.
   Google Scholar
• Reuter M, Schmansky NJ, Rosas HD, Fischl B. Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage. 2012;61:1402–18.
   Google Scholar
• Dale AM, Fischl B, Sereno MI. Cortical surface-based analysis: I. Segmentation and surface reconstruction. Neuroimage. 1999;9:179–94.
   Google Scholar
• Fischl B, Dale AM. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA. 2000;97:11050–5.
   Google Scholar
• Friederici AD. Pathways to language: fiber tracts in the human brain. Trends Cogn Sci (Regul Ed). 2009;13:175–81.
   Google Scholar
• Gordon PH, Cheng B, Salachas F, Pradat P-F, Bruneteau G, Corcia P, et al. Progression in ALS is not linear but is curvilinear. J Neurol. 2010;257:1713–7.
   Google Scholar
• Elamin M, Bede P, Byrne S, Jordan N, Gallagher L, Wynne B, et al. Cognitive changes predict functional decline in ALS: a population-based longitudinal study. Neurology. 2013;80:1590–7.
   Google Scholar
• Agosta F, Pagani E, Rocca M, Caputo D, Perini M, Salvi F, et al. Voxel‐based morphometry study of brain volumetry and diffusivity in amyotrophic lateral sclerosis patients with mild disability. Hum Brain Mapp. 2007;28:1430–8.
   Google Scholar
• Mezzapesa D, Ceccarelli A, Dicuonzo F, Carella A, De Caro M, Lopez M, et al. Whole-brain and regional brain atrophy in amyotrophic lateral sclerosis. Am J Neuroradiol. 2007;28:255–9.
   Google Scholar
• Canu E, Agosta F, Riva N, Sala S, Prelle A, Caputo D, et al. The topography of brain microstructural damage in amyotrophic lateral sclerosis assessed using diffusion tensor MR imaging. AJNR Am J Neuroradiol. 2011;32:1307–14.
   Google Scholar
• Ciccarelli O, Behrens TE, Johansen-Berg H, Talbot K, Orrell RW, Howard RS, et al. Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics. Hum Brain Mapp. 2009;30:615–24.
   Google Scholar
• Keil C, Prell T, Peschel T, Hartung V, Dengler R, Grosskreutz J. Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis. BMC Neurosci. 2012;13:1.
   Google Scholar
• Chang J, Lomen-Hoerth C, Murphy J, Henry R, Kramer J, Miller B, et al. A voxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology. 2005;65:75–80.
   Google Scholar
• Zatorre RJ, Evans AC, Meyer E, Gjedde A. Lateralization of phonetic and pitch discrimination in speech processing. Science. 1992;256:846–9.
   Google Scholar
• Lemaire J-J, Golby A, Wells WM, III, Pujol S, Tie Y, Rigolo L, et al. Extended Broca’s area in the connectome of language in adults: subcortical single-subject analysis using DTI tractography. Brain Topogr. 2013;26:428.
   Google Scholar
• Mazoyer B, Zago L, Jobard G, Crivello F, Joliot M, Perchey G, et al. Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness. PLoS One. 2014;9:e101165.
   Google Scholar
• Ferstl EC, Neumann J, Bogler C, Von Cramon DY. The extended language network: a meta‐analysis of neuroimaging studies on text comprehension. Hum Brain Mapp. 2008;29:581–93.
   Google Scholar
• Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP‐43 pathology in amyotrophic lateral sclerosis. Ann Neurol. 2013;74:20–38.
   Google Scholar
• Rose S, Pannek K, Bell C, Baumann F, Hutchinson N, Coulthard A, et al. Direct evidence of intra-and interhemispheric corticomotor network degeneration in amyotrophic lateral sclerosis: an automated MRI structural connectivity study. Neuroimage. 2012;59:2661–9.
   Google Scholar
• Tu S, Menke RA, Talbot K, Kiernan MC, Turner MR. Regional thalamic MRI as a marker of widespread cortical pathology and progressive frontotemporal involvement in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2018;89:1250–8.
   Google Scholar
• Braak H. On magnopyramidal temporal fields in the human brain – probable morphological counterparts of Wernicke's sensory speech region. Anat Embryol. 1978;152:141–69.
   Google Scholar
• Penhune V, Zatorre R, MacDonald J, Evans A. Interhemispheric anatomical differences in human primary auditory cortex: probabilistic mapping and volume measurement from magnetic resonance scans. Cereb Cortex. 1996;6:661–72.
   Google Scholar
• Kanai R, Lloyd H, Bueti D, Walsh V. Modality-independent role of the primary auditory cortex in time estimation. Exp Brain Res. 2011;209:465–71.
   Google Scholar
• Hyde KL, Peretz I, Zatorre RJ. Evidence for the role of the right auditory cortex in fine pitch resolution. Neuropsychologia. 2008;46:632–9.
   Google Scholar
• Scott SK, Johnsrude IS. The neuroanatomical and functional organization of speech perception. Trends Neurosci. 2003;26:100–7.
   Google Scholar
• Tourville JA, Reilly KJ, Guenther FH. Neural mechanisms underlying auditory feedback control of speech. Neuroimage. 2008;39:1429–43.
   Google Scholar
• Mohammadi B, Kollewe K, Samii A, Krampfl K, Dengler R, Münte TF. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp Neurol. 2009;217:147–53.
   Google Scholar
• Raggi A, Consonni M, Iannaccone S, Perani D, Zamboni M, Sferrazza B, et al. Auditory event-related potentials in non-demented patients with sporadic amyotrophic lateral sclerosis. Clin Neurophysiol. 2008;119:342–50.
   Google Scholar
• Saxon JA, Thompson JC, Jones M, Harris JM, Richardson AM, Langheinrich T, et al. Examining the language and behavioural profile in FTD and ALS-FTD. J Neurol Neurosurg Psychiatry. 2017;88:675–80.
   Google Scholar
• Ishaque A, Maani R, Satkunam J, Seres P, Mah D, Wilman AH, et al. Texture analysis to detect cerebral degeneration in amyotrophic lateral sclerosis. Can J Neurol Sci. 2018;45:533–9.
   Google Scholar
• Kalra S, Beaulieu C, Benatar M, Briemberg H, Dionne A, Dupre N, et al. The Canadian ALS neuroimaging consortium(CALSNIC). Neurology. 2019;92:P1.4-010.
   Google Scholar
• Bookheimer S. Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annu Rev Neurosci. 2002;25:151–88.
   Google Scholar
• Molnar-Szakacs I, Iacoboni M, Koski L, Mazziotta JC. Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation. Cereb Cortex. 2005;15:986–94.
   Google Scholar
• Bede P, Bokde AL, Byrne S, Elamin M, McLaughlin RL, Kenna K, et al. Multiparametric MRI study of ALS stratified for the C9orf72 genotype. Neurology. 2013;81:361–9.
   Google Scholar
• Westeneng H-J, Walhout R, Straathof M, Schmidt R, Hendrikse J, Veldink JH, et al. Widespread structural brain involvement in ALS is not limited to the C9orf72 repeat expansion. J Neurol Neurosurg Psychiatry. 2016;87:1354–60.
   Google Scholar
• Kwan JY, Meoded A, Danielian LE, Wu T, Floeter MK. Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis. NeuroImage: Clin. 2013;2:151–60.
   Google Scholar
• Brannen JH, Badie B, Moritz CH, Quigley M, Meyerand ME, Haughton VM. Reliability of functional MR imaging with word-generation tasks for mapping Broca's area. AJNR Am J Neuroradiol. 2001;22:1711–8.
   Google Scholar
• De Luca M, Beckmann C, De Stefano N, Matthews P, Smith SM. fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage. 2006;29:1359–67.
   Google Scholar
• Flinker A, Korzeniewska A, Shestyuk AY, Franaszczuk PJ, Dronkers NF, Knight RT, et al. Redefining the role of Broca's area in speech. Proc Natl Acad Sci USA. 2015;112:2871–5.
   Google Scholar
• Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM. The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage. 2010;50:1313–9.
   Google Scholar
• Heim S, Opitz B, Friederici AD. Distributed cortical networks for syntax processing: Broca’s area as the common denominator. Brain Lang. 2003;85:402–8.
   Google Scholar
• Zhou J, Gennatas ED, Kramer JH, Miller BL, Seeley WW. Predicting regional neurodegeneration from the healthy brain functional connectome. Neuron. 2012;73:1216–27.
   Google Scholar