Gajardo-Vidal, A

Green, DW

Lorca-Puls, DL

Price, CJ

English

UCL Discovery

Reply: Broca’s area: why was neurosurgery neglected for so long whenseeking to re-establish the scientific truth? and Where is the speechproduction area? Evidence from direct cortical electrical stimulation mappingDiego L. Lorca-Puls,1,2,† Andrea Gajardo-Vidal,1,3,† David W. Green4 and Cathy J. Price1†These authors contributed equally to this work.1 Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, London, UK2 Department of Speech, Language and Hearing Sciences, Faculty of Medicine, Universidad de Concepcion, Concepcion, Chile3 Faculty of Health Sciences, Universidad del Desarrollo, Concepcion, Chile4 Department of Experimental Psychology, University College London, London, UKCorrespondence to: Diego L. Lorca-Puls, PhDWellcome Centre for Human NeuroimagingUCL Queen Square Institute of Neurology, 12 Queen SquareLondon, WC1N 3AR, UKE-mail: d.puls@ucl.ac.ukCorrespondence may also be addressed to: Andrea Gajardo-Vidal, PhDE-mail: andrea.gajardo.11@ucl.ac.ukGajardo-Vidal et al.1 reported data from a sample of 134 strokepatients with relatively circumscribed damage to the left frontallobe. Contrary to the received view, mapping lesion to deficit usingan ecologically-valid measure of speech production (i.e. spontan-eous connected speech elicited with a picture description task)revealed that, irrespective of lesion extent, damage to Broca’s areadoes not contribute to long-term speech production outcome,whereas damage to the white matter in the vicinity of the anteriorpart of the arcuate fasciculus (AF) is strongly implicated. Ourresults therefore address a matter of critical clinical importance:understanding the causes of inter-patient variability in speech pro-duction outcome post-stroke.We welcome the opportunity to reply to two Letters to theEditor on our paper.2,3 Both Letters rely on a source of data differ-ent from ours: direct electrical stimulation (DES) and/or resectioncarried out during neurosurgical procedures on awake patients(e.g. with glioma). A key behavioural outcome measure in suchwork is the presence or absence of speech arrest (e.g. an inabilityto name a visually presented picture) following DES over a givencortical region. Inferences drawn from different clinical popula-tions and methodological approaches that converge on a com-mon scientific understanding (consilience) bolster confidence inthat understanding, and so we strongly endorse the contributionof research in neurosurgical patients to the existing body ofknowledge regarding the regions involved in speech production.Consilience is important because different methods have differ-ent strengths and weaknesses. For instance, the challenge for le-sion-deficit mapping research in stroke patients is to dissociatethe contribution of brain regions that are commonly damaged to-gether. In the case of DES, an observed behavioural effect is notnecessarily the consequence of direct stimulation of the targetedregion; it may instead reflect the contribution of stimulation thatspreads along white matter pathways into remote regions.4 In thecase of resection (and DES), the absence of a behavioural effectmight reflect functional reorganization that has occurred over-time prior to neurosurgery, due to an underlying neurologicalcondition (e.g. tumour or epilepsy). This contrasts with the sud-den onset of stroke where functional reorganization is notexpected to occur until after the insult.In what follows, we identify the main contentions of each Letterfirst and then address them one by one.Mandonnet and Duffau2 propose that prior data, acquired inpatients undergoing neurosurgery, already refute the relevance ofBroca’s area to persistent speech production impairments. Theyhighlight, for example, the work of Benzagmout et al.5 where focalresection of Broca’s area only resulted in transient speech produc-tion impairments. They also enjoin the community to understandthe apparent neglect of such data. We recognize the perpetuationof the myth of Broca’s area as the critical region for speech produc-tion, but challenge the decisiveness of current neurosurgical datawith respect to the research question we addressed. For example,the Benzamount et al.5 data may establish that damage to Broca’sarea is not sufficient to cause long-lasting speech productionimpairments, but they do not refute its necessity in combinationwith surrounding regions (including the underlying white matter),which was the focus of our work.Advance access publication May 12, 2021VC The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), whichpermits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.doi:10.1093/brain/awab177 BRAIN 2021: 144; 1–3 | e62Downloaded from https://academic.oup.com/brain/article/144/7/e62/6274639 by Catherine Sharp user on 18 October 2021Zhao et al.,3 based on their work with glioma patients, offer con-vergent evidence that the anterior segment of AF is essential andconclude that this region is the speech production area. We repriseour arguments about the anterior part of AF for the sake of clarity,but strongly contest the localizationist notion that the anterior seg-ment of AF is the speech production area. We emphasize, instead,the critical importance of understanding the network of regionsinvolved in speech production.Madonnet and Duffau2 set their comments in an historical con-text. We also set our findings from stroke patients in this context.For example, our results refine the influential work of Mohr et al.6These authors were the first to systematically show that relativelyfocal damage to Broca’s area typically causes an initial mutism thatrapidly evolves into mild speech production impairments or com-pletely resolves over time. Moreover, Mohr et al.6 showed that thesevere and persistent speech production impairments originallydescribed by Paul Broca are associated with far more extensivedamage that involves Broca’s area and neighbouring brain regions.These findings led to the long-held belief that persistent speechproduction impairments after damage in and around Broca’s areaare caused by the combination of damage to Broca’s area andneighbouring regions. We showed, however, that damage toBroca’s area does not contribute to long-term speech productionoutcome, irrespective of the extent of the lesion. Therefore,our study’s findings complement and extend those of Benzagmoutet al.5DES (and resection) data provide evidence for the role of a cor-tical region or white matter tract in speech production and we citedpertinent work, and reviews of the topic, in our paper. Speech ar-rest, however, does not allow immediate inference to the long-term consequences of damage to an area. Moreover, the evidencefor speech arrest with DES of Broca’s area has been inconsistent.We placed most weight on data from Tate et al.7 involving a largesample of 165 neurosurgical patients that indicated only rareinstances of speech arrest. But still, as a community we need to ac-knowledge methodological factors associated with the use of DES.For instance, the absence of an effect may arise because stimula-tion intensity is insufficient,8 because of prior functional reorgan-ization in response to tumour infiltration/epileptic foci, or becausethe task assessing speech arrest (e.g. picture naming) is not sensi-tive enough to the function of the region (e.g. sentence generation).If damage to Broca’s area does not contribute to long-lastingspeech production impairments, what may explain such impair-ments in stroke survivors with damage in and around Broca’sarea? Prior DES/resection data leave this question open. Our analy-ses indicated a causal role for co-occurring white matter damage inthe vicinity of the anterior part of AF and established that such anoutcome is not a consequence of the disconnection of Broca’s area.In brief, we found that the speech production abilities of patientswith direct damage to Broca’s area and relative sparing of the whitematter in the vicinity of the anterior part of AF were, on average,within the normal range and significantly better than those ofpatients with the contrasting pattern of damage (i.e. to the whitematter in the vicinity of the anterior part of AF with relative spar-ing of Broca’s area). Thus, our data establish that damage toBroca’s area is neither necessary nor sufficient to cause persistentspeech production impairments.Interestingly, Zhao et al.3 report DES data on 18 glioma patientsbearing on the role of the anterior and long segments of AF inspeech production. In our study, we noted high collinearity in thedegree of damage to these two segments, which precluded us fromdissociating their effects. Zhao et al.3 report a dissociation: thefrontal end points of the anterior segment are more consistent ineliciting speech arrest. We look forward to a detailed report, assuch data would exemplify the value of consilience. In the mean-while, we remain cautious as their Letter suggests that they stimu-lated the frontal cortex where these two AF segments are thoughtto terminate based on tractography data (yielding indirect evi-dence), or perhaps stimulated the fibres directly after resection ofthe corresponding cortex (potentially conflating resection andstimulation effects).On their claim that the frontal termination of the anterior seg-ment of AF is the speech production area, we disagree with such alocalizationist position. In our paper, we stated that the long-last-ing detrimental effect of damage to the white matter in the vicinityof the anterior part of AF ‘may be the consequence of disruptedfunctional integration among the multiple regions in inferior front-al, inferior parietal and superior temporal cortices involved inthe sensorimotor control of speech production . . . irrespective ofwhether or not Broca’s area has been disconnected’.3 This is con-sistent with the results reported by Herbet et al.,9 based on DES andtumour resection data, suggesting that the compensatory potentialis generally high after cortical damage and low after white matterdamage (particularly for AF).Where is the speech production area? Our view is that no sucharea is discoverable by DES, or any other method for that matter,because no such area exists. Speech production results from thecoordinated activity of multiple brain regions, in which the networkconnectivity of AF may be salient.Data availabilityData availability is not applicable to this article as no new datawere created or analysed in this study.FundingThis work was funded by Wellcome (203147/Z/16/Z and 205103/Z/16/Z, C.J.P.), the Medical Research Council (MR/M023672/1, C.J.P.)and the Stroke Association (TSA 2014/02, C.J.P. and D.W.G.).Competing interestsThe authors report no competing interests.References1. Gajardo-Vidal A, Lorca-Puls DL, Team P, et al. Damage to Broca’sarea does not contribute to long-term speech production out-come after stroke. Brain. 2021;144(3):817–832.2. Mandonnet E, Duffau H. Broca’s area: why neurosurgery was solong time neglected to re-establish the scientific truth? Brain.2021;144(7):e60.3. Zhao Z, Liu Y, Zhang J, Lu J, Wu J. Where is the speech productionarea? Evidence from direct cortical electrical stimulation map-ping. Brain. 2021;144(7):e61.4. Matsumoto R, Nair DR, LaPresto E, et al. Functional connectivityin the human language system: A cortico-cortical evoked poten-tial study. Brain. 2004;127(Pt 10):2316–2330.5. Benzagmout M, Gatignol P, Duffau H. Resection of World HealthOrganization Grade II gliomas involving Broca’s area:Methodological and functional considerations. Neurosurgery.2007;61(4):741–752.6. Mohr JP, Pessin MS, Finkelstein S, Funkenstein HH, Duncan GW,Davis KR. Broca aphasia: Pathologic and clinical. Neurology. 1978;28(4):311–324.e62 | BRAIN 2021: 144; 1–3 Letter to the EditorDownloaded from https://academic.oup.com/brain/article/144/7/e62/6274639 by Catherine Sharp user on 18 October 20217. Tate MC, Herbet G, Moritz-Gasser S, Tate JE, Duffau H.Probabilistic map of critical functional regions of the human cere-bral cortex: Broca’s area revisited. Brain. 2014;137(Pt 10):2773–2782.8. Shimotake A, Matsumoto R, Ueno T, et al. Direct exploration ofthe role of the ventral anterior temporal lobe in semanticmemory: Cortical stimulation and local field potential: Evidencefrom subdural grid. Cereb Cortex. 2015;25(10):3802–3817.9. Herbet G, Maheu M, Costi E, Lafargue G, Duffau H. Mapping neu-roplastic potential in brain-damaged patients. Brain. 2016;139(3):829–844.Letter to the Editor BRAIN 2021: 144; 1–3 | e62Downloaded from https://academic.oup.com/brain/article/144/7/e62/6274639 by Catherine Sharp user on 18 October 2021

Reply: Broca’s area: why was neurosurgery neglected for so long when seeking to re-establish the scientific truth? and Where is the speech production area? Evidence from direct cortical electrical stimulation mapping

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Reply: Broca’s area: why was neurosurgery neglected for so long when seeking to re-establish the scientific truth? and Where is the speech production area? Evidence from direct cortical electrical stimulation mapping

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