Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes

Background: The simplistic approaches to language circuits are continuously challenged by new findings in brain structure and connectivity. The posterior middle frontal gyrus and area 55b (pFMG/area55b), in particular, has gained a renewed interest in the overall language network.Methods: This is a...

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Main Authors: Sally Rosario Hazem, Mariam Awan, Jose Pedro Lavrador, Sabina Patel, Hilary Margaret Wren, Oeslle Lucena, Carla Semedo, Hassna Irzan, Andrew Melbourne, Sebastien Ourselin, Jonathan Shapey, Ahilan Kailaya-Vasan, Richard Gullan, Keyoumars Ashkan, Ranjeev Bhangoo, Francesco Vergani
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Neurology
Subjects:
DTI
TMS
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2021.646075/full
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author Sally Rosario Hazem
Sally Rosario Hazem
Mariam Awan
Mariam Awan
Jose Pedro Lavrador
Jose Pedro Lavrador
Sabina Patel
Sabina Patel
Hilary Margaret Wren
Oeslle Lucena
Carla Semedo
Carla Semedo
Hassna Irzan
Hassna Irzan
Andrew Melbourne
Andrew Melbourne
Sebastien Ourselin
Jonathan Shapey
Jonathan Shapey
Jonathan Shapey
Ahilan Kailaya-Vasan
Ahilan Kailaya-Vasan
Richard Gullan
Keyoumars Ashkan
Keyoumars Ashkan
Ranjeev Bhangoo
Ranjeev Bhangoo
Francesco Vergani
Francesco Vergani
spellingShingle Sally Rosario Hazem
Sally Rosario Hazem
Mariam Awan
Mariam Awan
Jose Pedro Lavrador
Jose Pedro Lavrador
Sabina Patel
Sabina Patel
Hilary Margaret Wren
Oeslle Lucena
Carla Semedo
Carla Semedo
Hassna Irzan
Hassna Irzan
Andrew Melbourne
Andrew Melbourne
Sebastien Ourselin
Jonathan Shapey
Jonathan Shapey
Jonathan Shapey
Ahilan Kailaya-Vasan
Ahilan Kailaya-Vasan
Richard Gullan
Keyoumars Ashkan
Keyoumars Ashkan
Ranjeev Bhangoo
Ranjeev Bhangoo
Francesco Vergani
Francesco Vergani
Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
Frontiers in Neurology
area 55b
language mapping
speech arrest
perioperative mapping
DTI
TMS
author_facet Sally Rosario Hazem
Sally Rosario Hazem
Mariam Awan
Mariam Awan
Jose Pedro Lavrador
Jose Pedro Lavrador
Sabina Patel
Sabina Patel
Hilary Margaret Wren
Oeslle Lucena
Carla Semedo
Carla Semedo
Hassna Irzan
Hassna Irzan
Andrew Melbourne
Andrew Melbourne
Sebastien Ourselin
Jonathan Shapey
Jonathan Shapey
Jonathan Shapey
Ahilan Kailaya-Vasan
Ahilan Kailaya-Vasan
Richard Gullan
Keyoumars Ashkan
Keyoumars Ashkan
Ranjeev Bhangoo
Ranjeev Bhangoo
Francesco Vergani
Francesco Vergani
author_sort Sally Rosario Hazem
title Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
title_short Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
title_full Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
title_fullStr Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
title_full_unstemmed Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language Outcomes
title_sort middle frontal gyrus and area 55b: perioperative mapping and language outcomes
publisher Frontiers Media S.A.
series Frontiers in Neurology
issn 1664-2295
publishDate 2021-03-01
description Background: The simplistic approaches to language circuits are continuously challenged by new findings in brain structure and connectivity. The posterior middle frontal gyrus and area 55b (pFMG/area55b), in particular, has gained a renewed interest in the overall language network.Methods: This is a retrospective single-center cohort study of patients who have undergone awake craniotomy for tumor resection. Navigated transcranial magnetic simulation (nTMS), tractography, and intraoperative findings were correlated with language outcomes.Results: Sixty-five awake craniotomies were performed between 2012 and 2020, and 24 patients were included. nTMS elicited 42 positive responses, 76.2% in the inferior frontal gyrus (IFG), and hesitation was the most common error (71.4%). In the pMFG/area55b, there were seven positive errors (five hesitations and two phonemic errors). This area had the highest positive predictive value (43.0%), negative predictive value (98.3%), sensitivity (50.0%), and specificity (99.0%) among all the frontal gyri. Intraoperatively, there were 33 cortical positive responses—two (6.0%) in the superior frontal gyrus (SFG), 15 (45.5%) in the MFG, and 16 (48.5%) in the IFG. A total of 29 subcortical positive responses were elicited−21 in the deep IFG–MFG gyri and eight in the deep SFG–MFG gyri. The most common errors identified were speech arrest at the cortical level (20 responses−13 in the IFG and seven in the MFG) and anomia at the subcortical level (nine patients—eight in the deep IFG–MFG and one in the deep MFG–SFG). Moreover, 83.3% of patients had a transitory deterioration of language after surgery, mainly in the expressive component (p = 0.03). An increased number of gyri with intraoperative positive responses were related with better preoperative (p = 0.037) and worse postoperative (p = 0.029) outcomes. The involvement of the SFG–MFG subcortical area was related with worse language outcomes (p = 0.037). Positive nTMS mapping in the IFG was associated with a better preoperative language outcome (p = 0.017), relating to a better performance in the expressive component, while positive mapping in the MFG was related to a worse preoperative receptive component of language (p = 0.031).Conclusion: This case series suggests that the posterior middle frontal gyrus, including area 55b, is an important integration cortical hub for both dorsal and ventral streams of language.
topic area 55b
language mapping
speech arrest
perioperative mapping
DTI
TMS
url https://www.frontiersin.org/articles/10.3389/fneur.2021.646075/full
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spelling doaj-9e693a82478840318217aecb2ad1e3a82021-03-10T06:24:28ZengFrontiers Media S.A.Frontiers in Neurology1664-22952021-03-011210.3389/fneur.2021.646075646075Middle Frontal Gyrus and Area 55b: Perioperative Mapping and Language OutcomesSally Rosario Hazem0Sally Rosario Hazem1Mariam Awan2Mariam Awan3Jose Pedro Lavrador4Jose Pedro Lavrador5Sabina Patel6Sabina Patel7Hilary Margaret Wren8Oeslle Lucena9Carla Semedo10Carla Semedo11Hassna Irzan12Hassna Irzan13Andrew Melbourne14Andrew Melbourne15Sebastien Ourselin16Jonathan Shapey17Jonathan Shapey18Jonathan Shapey19Ahilan Kailaya-Vasan20Ahilan Kailaya-Vasan21Richard Gullan22Keyoumars Ashkan23Keyoumars Ashkan24Ranjeev Bhangoo25Ranjeev Bhangoo26Francesco Vergani27Francesco Vergani28Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomSchool of Biomedical Engineering and Imaging Sciences, King's College London, London, United KingdomSchool of Biomedical Engineering and Imaging Sciences, King's College London, London, United KingdomDepartment of Medical Physics and Biomedical Engineering, University College London, London, United KingdomSchool of Biomedical Engineering and Imaging Sciences, King's College London, London, United KingdomDepartment of Medical Physics and Biomedical Engineering, University College London, London, United KingdomSchool of Biomedical Engineering and Imaging Sciences, King's College London, London, United KingdomDepartment of Medical Physics and Biomedical Engineering, University College London, London, United KingdomSchool of Biomedical Engineering and Imaging Sciences, King's College London, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomSchool of Biomedical Engineering and Imaging Sciences, King's College London, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomDepartment of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomKing's Neuro Lab, Department of Neurosurgery, King's College Hospital National Health Service Foundation Trust, London, United KingdomBackground: The simplistic approaches to language circuits are continuously challenged by new findings in brain structure and connectivity. The posterior middle frontal gyrus and area 55b (pFMG/area55b), in particular, has gained a renewed interest in the overall language network.Methods: This is a retrospective single-center cohort study of patients who have undergone awake craniotomy for tumor resection. Navigated transcranial magnetic simulation (nTMS), tractography, and intraoperative findings were correlated with language outcomes.Results: Sixty-five awake craniotomies were performed between 2012 and 2020, and 24 patients were included. nTMS elicited 42 positive responses, 76.2% in the inferior frontal gyrus (IFG), and hesitation was the most common error (71.4%). In the pMFG/area55b, there were seven positive errors (five hesitations and two phonemic errors). This area had the highest positive predictive value (43.0%), negative predictive value (98.3%), sensitivity (50.0%), and specificity (99.0%) among all the frontal gyri. Intraoperatively, there were 33 cortical positive responses—two (6.0%) in the superior frontal gyrus (SFG), 15 (45.5%) in the MFG, and 16 (48.5%) in the IFG. A total of 29 subcortical positive responses were elicited−21 in the deep IFG–MFG gyri and eight in the deep SFG–MFG gyri. The most common errors identified were speech arrest at the cortical level (20 responses−13 in the IFG and seven in the MFG) and anomia at the subcortical level (nine patients—eight in the deep IFG–MFG and one in the deep MFG–SFG). Moreover, 83.3% of patients had a transitory deterioration of language after surgery, mainly in the expressive component (p = 0.03). An increased number of gyri with intraoperative positive responses were related with better preoperative (p = 0.037) and worse postoperative (p = 0.029) outcomes. The involvement of the SFG–MFG subcortical area was related with worse language outcomes (p = 0.037). Positive nTMS mapping in the IFG was associated with a better preoperative language outcome (p = 0.017), relating to a better performance in the expressive component, while positive mapping in the MFG was related to a worse preoperative receptive component of language (p = 0.031).Conclusion: This case series suggests that the posterior middle frontal gyrus, including area 55b, is an important integration cortical hub for both dorsal and ventral streams of language.https://www.frontiersin.org/articles/10.3389/fneur.2021.646075/fullarea 55blanguage mappingspeech arrestperioperative mappingDTITMS