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Functional connectivity reveals different brain networks underlying the idiopathic foreign accent syndrome

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Abstract

Foreign accent syndrome (FAS) is characterized by new onset speech that is perceived as foreign. Available data from acquired cases suggests focal brain damage in language and sensorimotor brain networks, but little remains known about abnormal functional connectivity in idiopathic cases of FAS without structural damage. Here, connectomic analyses were completed on three patients with idiopathic FAS to investigate unique functional connectivity abnormalities underlying accent change for the first time. Machine learning (ML)-based algorithms generated personalized brain connectomes based on a validated parcellation scheme from the Human Connectome Project (HCP). Diffusion tractography was performed on each patient to rule out structural fiber damage to the language system. Resting-state-fMRI was assessed with ML-based software to examine functional connectivity between individual parcellations within language and sensorimotor networks and subcortical structures. Functional connectivity matrices were created and compared against a dataset of 200 healthy subjects to identify abnormally connected parcellations. Three female patients (28–42 years) who presented with accent changes from Australian English to Irish (n = 2) or American English to British English (n = 1) demonstrated fully intact language system structural connectivity. All patients demonstrated functional connectivity anomalies within language and sensorimotor networks in numerous left frontal regions and between subcortical structures in one patient. Few commonalities in functional connectivity anomalies were identified between all three patients, specifically 3 internal-network parcellation pairs. No common inter-network functional connectivity anomalies were identified between all patients. The current study demonstrates specific language, and sensorimotor functional connectivity abnormalities can exist and be quantitatively shown in the absence of structural damage for future study.

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References

  1. Miller N, Lowit A, O’Sullivan H (2006) What makes acquired foreign accent syndrome foreign? J Neurolinguistics 19:385–409. https://doi.org/10.1016/j.jneuroling.2006.03.005

    Article  Google Scholar 

  2. Jonkers R, van der Scheer F, Gilbers D (2017) The common denominator in the perception of accents in cases with foreign accent syndrome. Aphasiology 31:1021–1043. https://doi.org/10.1080/02687038.2016.1232362

    Article  Google Scholar 

  3. Chang EF, Niziolek CA, Knight RT, Nagarajan SS, Houde JF (2013) Human cortical sensorimotor network underlying feedback control of vocal pitch. Proc Natl Acad Sci 110(7):2653–2658. https://doi.org/10.1073/pnas.1216827110

    Article  PubMed  PubMed Central  Google Scholar 

  4. Dichter BK, Breshears JD, Leonard MK, Chang EF (2018) The control of vocal pitch in human laryngeal motor cortex. Cell 174:21–31.e29. https://doi.org/10.1016/j.cell.2018.05.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Poologaindran A, Lowe SR, Sughrue ME (2020) The cortical organization of language: distilling human connectome insights for supratentorial neurosurgery. J Neurosurg 1-8. https://doi.org/10.3171/2020.5.JNS191281

  6. Saur D, Kreher BW, Schnell S, Kümmerer D, Kellmeyer P, Vry M-S, Umarova R, Musso M, Glauche V, Abel S, Huber W, Rijntjes M, Hennig J, Weiller C (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci 105:18035–18040. https://doi.org/10.1073/pnas.0805234105

    Article  PubMed  PubMed Central  Google Scholar 

  7. Tomasino B, Marin D, Maieron M, Ius T, Budai R, Fabbro F, Skrap M (2013) Foreign accent syndrome: a multimodal mapping study. Cortex 49:18–39. https://doi.org/10.1016/j.cortex.2011.10.007

    Article  PubMed  Google Scholar 

  8. Higashiyama Y, Hamada T, Saito A, Morihara K, Okamoto M, Kimura K, Joki H, Kishida H, Doi H, Ueda N, Takeuchi H, Tanaka F (2021) Neural mechanisms of foreign accent syndrome: lesion and network analysis. Neuroimage Clin 31:102760. https://doi.org/10.1016/j.nicl.2021.102760

    Article  PubMed  PubMed Central  Google Scholar 

  9. Glasser MF, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Ugurbil K, Andersson J, Beckmann CF, Jenkinson M, Smith SM, Van Essen DC (2016) A multi-modal parcellation of human cerebral cortex. Nature 536:171–178. https://doi.org/10.1038/nature18933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Berthier ML, Ruiz A, Massone MI, Starkstein SE, Leiguarda RC (1991) Foreign accent syndrome: behavioural and anatomical findings in recovered and non-recovered patients. Aphasiology 5:129–147. https://doi.org/10.1080/02687039108249478

    Article  Google Scholar 

  11. Luzzi S, Viticchi G, Piccirilli M, Fabi K, Pesallaccia M, Bartolini M, Provinciali L, Snowden JS (2008) Foreign accent syndrome as the initial sign of primary progressive aphasia. J Neurol Neurosurg Psychiatry 79:79–81. https://doi.org/10.1136/jnnp.2006.113365

    Article  CAS  PubMed  Google Scholar 

  12. Abel TJ, Hebb AO, Silbergeld DL (2009) Cortical stimulation mapping in a patient with foreign accent syndrome: case report. Clin Neurol Neurosurg 111:97–101. https://doi.org/10.1016/j.clineuro.2008.07.014

    Article  PubMed  Google Scholar 

  13. Keulen S, Mariën P, van Dun K, Bastiaanse R, Manto M, Verhoeven J (2017) The posterior fossa and foreign accent syndrome: report of two new cases and review of the literature. The Cerebellum 16:772–785. https://doi.org/10.1007/s12311-017-0849-6

    Article  PubMed  Google Scholar 

  14. Fridriksson J, Ryalls J, Rorden C, Morgan PS, George MS, Baylis GC (2005) Brain damage and cortical compensation in foreign accent syndrome. Neurocase 11:319–324. https://doi.org/10.1080/13554790591006302

    Article  PubMed  Google Scholar 

  15. Briggs RG, Allan PG, Poologaindran A, Dadario NB, Young IM, Ahsan SA, Teo C, Sughrue ME (2021) The frontal aslant tract and supplementary motor area syndrome: moving towards a connectomic initiation axis. Cancers 13(5):1116. https://doi.org/10.3390/cancers13051116

    Article  PubMed  PubMed Central  Google Scholar 

  16. Keulen S, Verhoeven J, De Witte E, De Page L, Bastiaanse R, Mariën P (2016) Foreign accent syndrome as a psychogenic disorder: a review. Front Hum Neurosci 10:168. https://doi.org/10.3389/fnhum.2016.00168

    Article  PubMed  PubMed Central  Google Scholar 

  17. Dadario NB, Brahimaj B, Yeung J, Sughrue ME (2021) Reducing the cognitive footprint of brain tumor surgery. Front Neurol 12:711646

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dadario NB, Sughrue ME (2022) Should neurosurgeons try to preserve non-traditional brain networks? A systematic review of the neuroscientific evidence. J Pers Med 12:587

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ren H, Zhu J, Su X, Chen S, Zeng S, Lan X, Zou L-Y, Sughrue ME, Guo Y (2020) Application of structural and functional connectome mismatch for classification and individualized therapy in Alzheimer disease. Front Public Health 8:584430–584430. https://doi.org/10.3389/fpubh.2020.584430

    Article  PubMed  PubMed Central  Google Scholar 

  20. Doyen S, Nicholas P, Poologaindran A, Crawford L, Young IM, Romero-Garcia R, Sughrue ME (2021) Connectivity-based parcellation of normal and anatomically distorted human cerebral cortex. Hum Brain Mapp 43(4):1358–1369

    Article  PubMed  PubMed Central  Google Scholar 

  21. Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37:90–101. https://doi.org/10.1016/j.neuroimage.2007.04.042

    Article  PubMed  Google Scholar 

  22. Briggs RG, Tanglay O, Dadario NB, Young IM, Fonseka RD, Hormovas J, Dhanaraj V, Lin YH, Kim SJ, Bouvette A, Chakraborty AR, Milligan TM, Abraham CJ, Anderson CD, O'Donoghue DL, Sughrue ME (2021) The unique fiber anatomy of middle temporal gyrus default mode connectivity. Oper Neurosurg 21:E8–E14. https://doi.org/10.1093/ons/opab109

    Article  Google Scholar 

  23. Moreno-Torres I, Berthier ML, Mar Cid M, Green C, Gutiérrez A, García-Casares N, Froudist Walsh S, Nabrozidis A, Sidorova J, Dávila G, Carnero-Pardo C (2013) Foreign accent syndrome: a multimodal evaluation in the search of neuroscience-driven treatments. Neuropsychologia 51:520–537. https://doi.org/10.1016/j.neuropsychologia.2012.11.010

    Article  PubMed  Google Scholar 

  24. Milton CK, Dhanaraj V, Young IA-O, Taylor HM, Nicholas PJ, Briggs RG, Bai MA-O, Fonseka RD, Hormovas J, Lin YH, Tanglay OA-O, Conner AK, Glenn CA, Teo C, Doyen S, Sughrue MA-O (2021) Parcellation-based anatomic model of the semantic network. Brain Behav 11(4):e02065

    Article  PubMed  PubMed Central  Google Scholar 

  25. Sandhu Z, Tanglay O, Young IM, Briggs RG, Bai MY, Larsen ML, Conner AK, Dhanaraj V, Lin Y-H, Hormovas J, Fonseka RD, Glenn CA, Sughrue ME (2021) Parcellation-based anatomic modeling of the default mode network. Brain Behav 11:e01976. https://doi.org/10.1002/brb3.1976

    Article  PubMed  Google Scholar 

  26. Akiki TJ, Abdallah CG (2019) Determining the hierarchical architecture of the human brain using subject-level clustering of functional networks. Sci Rep 9:19290. https://doi.org/10.1038/s41598-019-55738-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shahab QS, Young IM, Dadario NB, Tanglay O, Nicholas PJ, Lin Y-H, Fonseka RD, Yeung JT, Bai MY, Teo C (2022) A connectivity model of the anatomic substrates underlying Gerstmann syndrome. Brain commun 4(3):fcac140

    Article  PubMed  PubMed Central  Google Scholar 

  28. Dadario NB, Brahimaj B, Yeung J, Sughrue ME (2021) Reducing the cognitive footprint of brain tumor surgery. Front Neurol 12:711646. https://doi.org/10.3389/fneur.2021.711646

    Article  PubMed  Google Scholar 

  29. Dadario NB, Sughrue ME (2022) Should neurosurgeons try to preserve non-traditional brain networks? A systematic review of the neuroscientific evidence. J Pers Med 12(4):587. https://doi.org/10.3390/jpm12040587

    Article  PubMed  PubMed Central  Google Scholar 

  30. Berthier M, Dávila G, Moreno-Torres I, Beltrán-Corbellini Á, Santana-Moreno D, Torres-Prioris MJ, Massone MI, Cruces R, Roé Vellvé N, Thurnhofer-Hemsi K (2015) Loss of regional accent after damage to the speech production network. Front Hum Neurosci 9:610. https://doi.org/10.3389/fnhum.2015.00610

    Article  PubMed  PubMed Central  Google Scholar 

  31. Sakurai Y, Itoh K, Sai K, Lee S, Abe S, Terao Y, Mannen T (2015) Impaired laryngeal voice production in a patient with foreign accent syndrome. Neurocase 21:289–298. https://doi.org/10.1080/13554794.2014.892622

    Article  PubMed  Google Scholar 

  32. Chang EF, Kurteff G, Andrews JP, Briggs RG, Conner AK, Battiste JD, Sughrue ME (2020) Pure apraxia of speech after resection based in the posterior middle frontal gyrus. Neurosurgery 87:E383–E389. https://doi.org/10.1093/neuros/nyaa002

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hickok G, Houde J, Rong F (2011) Sensorimotor integration in speech processing: computational basis and neural organization. Neuron 69:407–422. https://doi.org/10.1016/j.neuron.2011.01.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Sheets JR, Briggs RG, Young IM, Bai MY, Lin YH, Poologaindran A, Conner AK, O'Neal CM, Baker CM, Glenn CA, Sughrue ME (2021) Parcellation-based modeling of the supplementary motor area. J Neurol Sci 421:117322. https://doi.org/10.1016/j.jns.2021.117322

    Article  PubMed  Google Scholar 

  35. Kumral E, Evyapan D, Balkir K (1999) Acute caudate vascular lesions. Stroke 30:100–108. https://doi.org/10.1161/01.STR.30.1.100

    Article  CAS  PubMed  Google Scholar 

  36. Berthier ML, Roé-Vellvé N, Moreno-Torres I, Falcon C, Thurnhofer-Hemsi K, Paredes-Pacheco J, Torres-Prioris MJ, De-Torres I, Alfaro F, Gutiérrez-Cardo AL, Baquero M, Ruiz-Cruces R, Dávila G (2016) Mild developmental foreign accent syndrome and psychiatric comorbidity: altered white matter integrity in speech and emotion regulation networks. Front Hum Neurosci 10:399. https://doi.org/10.3389/fnhum.2016.00399

    Article  PubMed  PubMed Central  Google Scholar 

  37. Keulen S, Verhoeven J, De Page L, Jonkers R, Bastiaanse R, Mariën P (2016) Psychogenic foreign accent syndrome: a new case. Front Hum Neurosci 10:143. https://doi.org/10.3389/fnhum.2016.00143

    Article  PubMed  PubMed Central  Google Scholar 

  38. Poulin S, Macoir J, Paquet N, Fossard M, Gagnon L (2007) Psychogenic or neurogenic origin of agrammatism and foreign accent syndrome in a bipolar patient: a case report. Ann Gen Psychiatry 6:1. https://doi.org/10.1186/1744-859X-6-1

    Article  PubMed  Google Scholar 

  39. Espay AJ, Aybek S, Carson A, Edwards MJ, Goldstein LH, Hallett M, LaFaver K, LaFrance WC Jr, Lang AE, Nicholson T, Nielsen G, Reuber M, Voon V, Stone J, Morgante F (2018) Current concepts in diagnosis and treatment of functional neurological disorders. JAMA Neurol 75:1132–1141. https://doi.org/10.1001/jamaneurol.2018.1264

    Article  PubMed  PubMed Central  Google Scholar 

  40. Weber S, Heim S, Richiardi J, Van De Ville D, Serranova T, Jech R, Marapin RS, Tijssen MAJ, Aybek S (2022) Multi-centre classification of functional neurological disorders based on resting-state functional connectivity. Neuroimage Clin 35:103090. https://doi.org/10.1016/j.nicl.2022.103090

    Article  PubMed  PubMed Central  Google Scholar 

  41. Young IM, Dadario NB, Tanglay O, Chen E, Cook B, Taylor HM, Crawford L, Yeung JT, Nicholas PJ, Doyen S, Sughrue ME (2023) Connectivity model of the anatomic substrates and network abnormalities in major depressive disorder: a coordinate meta-analysis of resting-state functional connectivity. J Affect Disord 11:100478. https://doi.org/10.1016/j.jadr.2023.100478

    Article  Google Scholar 

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Author information

Authors and Affiliations

  1. Robert Wood Johnson Medical School, Rutgers University, New Brunswick, NJ, USA

    Nicholas B. Dadario

  2. Department of Neurosurgery, University of South Florida, Tampa, FL, USA

    Keaton Piper

  3. Omniscient Neurotechnology, Sydney, New South Wales, Australia

    Isabella M Young

  4. Department of Neurosurgery, West Virginia University, Martinsburg, WV, USA

    Jonathan H. Sherman

  5. Centre for Minimally Invasive Neurosurgery, Prince of Wales Private Hospital, Suite 3, Level 7 Barker St, Randwick, New South Wales, 2031, Australia

    Michael E. Sughrue

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  1. Nicholas B. Dadario
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  3. Isabella M Young
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  4. Jonathan H. Sherman
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  5. Michael E. Sughrue
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Contributions

Conceptualization: Michael Sughrue and Jonathan Sherman; methodology: Michael Sughrue; formal analysis and investigation: Michael Sughrue, Isabella Young, and Nicholas Dadario; writing — original draft preparation: Nicholas Dadario; writing — review and editing: Nicholas Dadario, Keaton Piper, Isabella Young, Jonathan Sherman, and Michael Sughrue; resources: Michael Sughrue and Jonathan Sherman; supervision: Michael Sughrue; figures and tables; Keaton Piper and Nicholas Dadario

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Correspondence to Michael E. Sughrue.

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All patients provided informed consent to study participation and image publication.

Conflict of interest

Michael Sughrue is the Chief Medical Officer and co-founder of Omniscient Neurotechnology. Isabella Young is an employee of Omniscient Neurotechnology. Products related to this company were only discussed as needed for statistical analyses in the current paper using the Quicktome software. No other authors report any conflict of interest.

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Supplementary file 1

Supplementary material have been provided detailing expanded methodology and results on recently reported coordinates for acquired cases of foreign accent syndrome in comparison with results presented in the current manuscript. (DOCX 38 kb)

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Dadario, N.B., Piper, K., Young, I.M. et al. Functional connectivity reveals different brain networks underlying the idiopathic foreign accent syndrome. Neurol Sci 44, 3087–3097 (2023). https://doi.org/10.1007/s10072-023-06762-4

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  • DOI: https://doi.org/10.1007/s10072-023-06762-4

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