Lesion-symptom mapping of language impairments in people with brain tumours: The influence of linguistic stimuli.


Journal

Journal of neuropsychology
ISSN: 1748-6653
Titre abrégé: J Neuropsychol
Pays: England
ID NLM: 101468753

Informations de publication

Date de publication:
06 2023
Historique:
revised: 18 12 2022
received: 20 10 2022
accepted: 22 12 2022
medline: 9 6 2023
pubmed: 19 1 2023
entrez: 18 1 2023
Statut: ppublish

Résumé

People with tumours in specific brain sites might face difficulties in tasks with different linguistic material. Previous lesion-symptom mapping studies (VLSM) demonstrated that people with tumours in posterior temporal regions have more severe linguistic impairments. However, to the best of our knowledge, preoperative performance and lesion location on tasks with different linguistic stimuli have not been examined. In the present study, we performed VLSM on 52 people with left gliomas to examine whether tumour distribution differs depending on the tasks of the Aachen Aphasia Test. The VLSM analysis revealed that single-word production (e.g. object naming) was associated with the inferior parietal lobe and that compound and sentence production were additionally associated with posterior temporal gyri. Word repetition was affected in people with tumours in inferior parietal areas, whereas sentence repetition was the only task to be associated with frontal regions. Subcortically, word and sentence production were found to be affected in people with tumours reaching the arcuate fasciculus, and compound production was primarily associated with tumours affecting the inferior longitudinal and inferior fronto-occipital fasciculus. Our work shows that tasks with linguistic stimuli other than single-word naming (e.g. compound and sentence production) relate to additional cortical and subcortical brain areas. At a clinical level, we show that tasks that target the same processes (e.g. repetition) can have different neural correlates depending on the linguistic stimuli used. Also, we highlight the importance of left temporoparietal areas.

Identifiants

pubmed: 36651346
doi: 10.1111/jnp.12305
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

400-416

Informations de copyright

© 2023 The Authors. Journal of Neuropsychology published by John Wiley & Sons Ltd on behalf of The British Psychological Society.

Références

Alves, J., Cardoso, M., Morgado, M., Witte, E. D., Hall, A., & Jesus, L. M. T. (2021). Language assessment in awake brain surgery: The Portuguese adaptation of the Dutch linguistic intraoperative protocol (DuLIP). Clinical Linguistics & Phonetics, 35, 1113-1131. https://doi.org/10.1080/02699206.2020.1868022
Banerjee, P., Leu, K., Harris, R. J., Cloughesy, T. F., Lai, A., Nghiemphu, P. L., Pope, W. B., Bookheimer, S. Y., & Ellingson, B. M. (2015). Association between lesion location and language function in adult glioma using voxel-based lesion-symptom mapping. NeuroImage: Clinical, 9, 617-624. https://doi.org/10.1016/j.nicl.2015.10.010
Bates, E., Wilson, S. M., Saygin, A. P., Dick, F., Sereno, M. I., Knight, R. T., & Dronkers, N. F. (2003). Voxel-based lesion-symptom mapping. Nature Neuroscience, 6(5), 3-450. https://doi.org/10.1038/nn1050
Benzagmout, M., Gatignol, P., & Duffau, H. (2007). Resection of World Health Organization grade II gliomas involving Broca's area: Methodological and functional considerations. Neurosurgery, 61(4), 741-753. https://doi.org/10.1227/01.NEU.0000298902.69473.77
Bilotta, F., Stazi, E., Titi, L., Lalli, D., Delfini, R., Santoro, A., & Rosa, G. (2014). Diagnostic work up for language testing in patients undergoing awake craniotomy for brain lesions in language areas. British Journal of Neurosurgery, 28(3), 363-367. https://doi.org/10.3109/02688697.2013.854313
Brownsett, S. L. E., Ramajoo, K., Copland, D., McMahon, K. L., Robinson, G., Drummond, K., Jeffree, R. L., Olson, S., Ong, B., & De Zubicaray, G. (2019). Language deficits following dominant hemisphere tumour resection are significantly underestimated by syndrome-based aphasia assessments. Aphasiology, 33(10), 1163-1181. https://doi.org/10.1080/02687038.2019.1614760
Caramazza, A., & Miceli, G. (1991). Selective impairment of thematic role assignment in sentence processing. Brain and Language, 41(3), 402-436. https://doi.org/10.1016/0093-934X(91)90164-V
Catani, M., & de Schotten, M. T. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex, 44(8), 1105-1132. https://doi.org/10.1016/j.cortex.2008.05.004
Chang, E. F., Raygor, K. P., & Berger, M. S. (2015). Contemporary model of language organization: An overview for neurosurgeons. Journal of Neurosurgery, 122(2), 250-261. https://doi.org/10.3171/2014.10.JNS132647
Corina, D. P., Gibson, E. K., Martin, R., Poliakov, A., Brinkley, J., & Ojemann, G. A. (2005). Dissociation of action and object naming: Evidence from cortical stimulation mapping. Human Brain Mapping, 24(1), 1-10. https://doi.org/10.1002/hbm.20063
Davie, G. L., Hutcheson, K. A., Barringer, D. A., Weinberg, J. S., & Lewin, J. S. (2009). Aphasia in patients after brain tumour resection. Aphasiology, 23(9), 1196-1206. https://doi.org/10.1080/02687030802436900
De Witte, E., Satoer, D., Robert, E., Colle, H., Verheyen, S., Visch-Brink, E., & Mariën, P. (2015). The Dutch linguistic intraoperative protocol: A valid linguistic approach to awake brain surgery. Brain and Language, 140, 35-48. https://doi.org/10.1016/j.bandl.2014.10.011
Dronkers, N. F. (1996). A new brain region for coordinating speech articulation. Nature, 384(6605), 159-161. https://doi.org/10.1038/384159a0
Duffau, H. (2005). New insights into the anatomo-functional connectivity of the semantic system: A study using cortico-subcortical electrostimulations. Brain, 128(4), 797-810. https://doi.org/10.1093/brain/awh423
Duffau, H. (2009). A personal consecutive series of surgically treated 51 cases of insular WHO grade II glioma: Advances and limitations: Clinical article. Journal of Neurosurgery, 110(4), 696-708. https://doi.org/10.3171/2008.8.JNS08741
Duffau, H. (2014). The huge plastic potential of adult brain and the role of connectomics: New insights provided by serial mappings in glioma surgery. Cortex, 58, 325-337. https://doi.org/10.1016/j.cortex.2013.08.005
Duffau, H., Mandonnet, E., & Taillandier, L. (2008). Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with grade II glioma in the left dominant hemisphere. Journal of Neurosurgery, 109, 461-471. https://doi.org/10.3171/JNS/2008/109/9/0461
Eickhoff, S. B., Heim, S., Zilles, K., & Amunts, K. (2009). A systems perspective on the effective connectivity of overt speech production. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 367(1896), 2399-2421. https://doi.org/10.1098/rsta.2008.0287
Fekonja, L., Wang, Z., Bährend, I., Rosenstock, T., Rösler, J., Wallmeroth, L., Vajkoczy, P., & Picht, T. (2019). Manual for clinical language tractography. Acta Neurochirurgica, 161(6), 1125-1137. https://doi.org/10.1007/s00701-019-03899-0
Fekonja, L. S., Wang, Z., Doppelbauer, L., Vajkoczy, P., Picht, T., Pulvermüller, F., & Dreyer, F. R. (2021). Lesion-symptom mapping of language impairments in patients suffering from left perisylvian gliomas. Cortex, 144, 1-14. https://doi.org/10.1016/j.cortex.2021.08.002
Forgács, B., Bohrn, I., Baudewig, J., Hofmann, M. J., Pléh, C., & Jacobs, A. M. (2012). Neural correlates of combinatorial semantic processing of literal and figurative noun noun compound words. NeuroImage, 63(3), 1432-1442. https://doi.org/10.1016/j.neuroimage.2012.07.029
Fridriksson, J., den Ouden, D.-B., Hillis, A. E., Hickok, G., Rorden, C., Basilakos, A., Yourganov, G., & Bonilha, L. (2018). Anatomy of aphasia revisited. Brain, 141(3), 848-862. https://doi.org/10.1093/brain/awx363
Fridriksson, J., Fillmore, P., Guo, D., & Rorden, C. (2015). Chronic Broca's aphasia is caused by damage to Broca's and Wernicke's areas. Cerebral Cortex, 25(12), 4689-4696. https://doi.org/10.1093/cercor/bhu152
Friederici, A. D. (2011). The brain basis of language processing: From structure to function. Physiological Reviews, 91(4), 1357-1392. https://doi.org/10.1152/physrev.00006.2011
Friederici, A. D. (2018). The neural basis for human syntax: Broca's area and beyond. Current Opinion in Behavioral Sciences, 21, 88-92. https://doi.org/10.1016/j.cobeha.2018.03.004
Friederici, A. D., Rüschemeyer, S.-A., Hahne, A., & Fiebach, C. J. (2003). The role of left inferior frontal and superior temporal cortex in sentence comprehension: Localizing syntactic and semantic processes. Cerebral Cortex, 13(2), 170-177. https://doi.org/10.1093/cercor/13.2.170
Gajardo-Vidal, A., Lorca-Puls, D. L., Team, P., Warner, H., Pshdary, B., Crinion, J. T., Leff, A. P., Hope, T. M. H., Geva, S., Seghier, M. L., Green, D. W., Bowman, H., & Price, C. J. (2021). Damage to Broca's area does not contribute to long-term speech production outcome after stroke. Brain, 144(3), 817-832. https://doi.org/10.1093/brain/awaa460
Graves, W. W., Binder, J. R., Desai, R. H., Conant, L. L., & Seidenberg, M. S. (2010). Neural correlates of implicit and explicit combinatorial semantic processing. NeuroImage, 53(2), 638-646. https://doi.org/10.1016/j.neuroimage.2010.06.055
Havas, V., Gabarrós, A., Juncadella, M., Rifa-Ros, X., Plans, G., Acebes, J. J., de Diego Balaguer, R., & Rodríguez-Fornells, A. (2015). Electrical stimulation mapping of nouns and verbs in Broca's area. Brain and Language, 145-146, 53-63. https://doi.org/10.1016/j.bandl.2015.04.005
Hickok, G., Houde, J., & Rong, F. (2011). Sensorimotor integration in speech processing: Computational basis and neural organization. Neuron, 69(3), 407-422. https://doi.org/10.1016/j.neuron.2011.01.019
Hillis, A. E. (2007). Language and the frontal cortex. In B. L. Miller & J. L. Cummings (Eds.), The human frontal lobes: Functions and disorders (pp. 306-316). Guilford Press.
Huber, W., Poeck, K., & Willems, K. (1984). The Aachen aphasia test. Advanced Neurology, 42, 291-303.
Ivanova, M. V., Zhong, A., Turken, A., Baldo, J. V., & Dronkers, N. F. (2021). Functional contributions of the arcuate fasciculus to language processing. Frontiers in Human Neuroscience, 15, 672665. https://doi.org/10.3389/fnhum.2021.672665
Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W., & Smith, S. M. (2012). FSL. Neuroimage, 62(2), 782-790. https://doi.org/10.1016/j.neuroimage.2011.09.015
Kessler, J., Calabrese, P., & Kalbe, E. (2000). DemTect: A new screening instrument for supporting diagnosis of dementia. Neurbiology of Aging, 21, 30. https://doi.org/10.1016/S0197-4580(00)82813-4
Lauro, L. J. R., Reis, J., Cohen, L. G., Cecchetto, C., & Papagno, C. (2010). A case for the involvement of phonological loop in sentence comprehension. Neuropsychologia, 48(14), 4003-4011. https://doi.org/10.1016/j.neuropsychologia.2010.10.019
Lee, M., & Thompson, C. K. (2004). Agrammatic aphasic production and comprehension of unaccusative verbs in sentence contexts. Journal of Neurolinguistics, 17(4), 315-330. https://doi.org/10.1016/S0911-6044(03)00062-9
Mandonnet, E., & Duffau, H. (2021). Broca's area: Why was neurosurgery neglected for so long when seeking to re-establish the scientific truth? Brain, awab195, e60. https://doi.org/10.1093/brain/awab195
Matchin, W., Basilakos, A., Stark, B. C., den Ouden, D.-B., Fridriksson, J., & Hickok, G. (2020). Agrammatism and Paragrammatism: A cortical double dissociation revealed by lesion-symptom mapping. Neurobiology of Language, 1(2), 208-225. https://doi.org/10.1162/nol_a_00010
Matchin, W., & Hickok, G. (2020). The cortical organization of Syntax. Cerebral Cortex, 30(3), 1481-1498. https://doi.org/10.1093/cercor/bhz180
Miceli, G., Caltagirone, C., Gainotti, G., Masullo, C., Silveri, M. C., & Villa, G. (1981). Influence of age, sex, literacy and pathologic lesion on incidence, severity and type of aphasia. Acta Neurologica Scandinavica, 64(5), 370-382. https://doi.org/10.1111/j.1600-0404.1981.tb04416.x
Miceli, G., Silveri, M. C., Villa, G., & Caramazza, A. (1984). On the basis for the Agrammatic's difficulty in producing Main verbs. Cortex, 20(2), 207-220. https://doi.org/10.1016/S0010-9452(84)80038-6
Mirman, D., Landrigan, J.-F., Kokolis, S., Verillo, S., Ferrara, C., & Pustina, D. (2018). Corrections for multiple comparisons in voxel-based lesion-symptom mapping. Neuropsychologia, 115, 112-123. https://doi.org/10.1016/j.neuropsychologia.2017.08.025
Mohr, J. P., Pessin, M. S., Finkelstein, S., Funkenstein, H. H., Duncan, G. W., & Davis, K. R. (1978). Broca aphasia: Pathologic and clinical. Neurology, 28(4), 311. https://doi.org/10.1212/WNL.28.4.311
Mooijman, S., Bos, L. S., De Witte, E., Vincent, A., Visch-Brink, E., & Satoer, D. (2021). Language processing in glioma patients: Speed or accuracy as a sensitive measure? Aphasiology, 36(12), 1467-1491. https://doi.org/10.1080/02687038.2021.1970099
Oh, A., Duerden, E. G., & Pang, E. W. (2014). The role of the insula in speech and language processing. Brain and Language, 135, 96-103. https://doi.org/10.1016/j.bandl.2014.06.003
Ohlerth, A.-K., Valentin, A., Vergani, F., Ashkan, K., & Bastiaanse, R. (2020). The verb and noun test for peri-operative testing (VAN-POP): Standardized language tests for navigated transcranial magnetic stimulation and direct electrical stimulation. Acta Neurochirurgica, 162(2), 397-406. https://doi.org/10.1007/s00701-019-04159-x
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97-113. https://doi.org/10.1016/0028-3932(71)90067-4
Ouden, D., Malyutina, S., Basilakos, A., Bonilha, L., Gleichgerrcht, E., Yourganov, G., Hillis, A. E., Hickok, G., Rorden, C., & Fridriksson, J. (2019). Cortical and structural-connectivity damage correlated with impaired syntactic processing in aphasia. Human Brain Mapping, 40(7), 2153-2173. https://doi.org/10.1002/hbm.24514
Rofes, A., Mandonnet, E., Godden, J., Baron, M. H., Colle, H., Darlix, A., de Aguiar, V., Duffau, H., Herbet, G., Klein, M., Lubrano, V., Martino, J., Mathew, R., Miceli, G., Moritz-Gasser, S., Pallud, J., Papagno, C., Rech, F., Robert, E., … Wager, M. (2017). Survey on current cognitive practices within the European low-grade glioma network: Towards a European assessment protocol. Acta Neurochirurgica, 159(7), 1167-1178. https://doi.org/10.1007/s00701-017-3192-2
Rofes, A., Spena, G., Talacchi, A., Santini, B., Miozzo, A., & Miceli, G. (2017). Mapping nouns and finite verbs in left hemisphere tumors: A direct electrical stimulation study. Neurocase, 23(2), 105-113. https://doi.org/10.1080/13554794.2017.1307418
Rofes, A., Talacchi, A., Santini, B., Pinna, G., Nickels, L., Bastiaanse, R., & Miceli, G. (2018). Language in individuals with left hemisphere tumors: Is spontaneous speech analysis comparable to formal testing? Journal of Clinical and Experimental Neuropsychology, 40(7), 722-732. https://doi.org/10.1080/13803395.2018.1426734
Rorden, C., & Brett, M. (2001). Stereotaxic display of brain lesions. Behavioural Neurology, 12, 191-200. https://doi.org/10.1155/2000/421719
Satoer, D., De Witte, E., Bulté, B., Bastiaanse, R., Smits, M., Vincent, A., Mariën, P., & Visch-Brink, E. (2022). Dutch diagnostic instrument for mild aphasia (DIMA): Standardisation and a first clinical application in two brain tumour patients. Clinical Linguistics & Phonetics, 36, 929-953. https://doi.org/10.1080/02699206.2021.1992797
Satoer, D., Vincent, A., Smits, M., Dirven, C., & Visch-Brink, E. (2013). Spontaneous speech of patients with gliomas in eloquent areas before and early after surgery. Acta Neurochirurgica, 155(4), 685-692. https://doi.org/10.1007/s00701-013-1638-8
Semenza, C., De Pellegrin, S., Battel, I., Garzon, M., Meneghello, F., & Chiarelli, V. (2011). Compounds in different aphasia categories: A study on picture naming. Journal of Clinical and Experimental Neuropsychology, 33(10), 1099-1107. https://doi.org/10.1080/13803395.2011.603691
Semenza, C., & Mondini, S. (2010). Compound words in neuropsychology. In S. Olsen (Ed.), New Impulses in Word-Formation (pp. 331 - 348). Buske.
Sierpowska, J., Gabarrós, A., Fernandez-Coello, A., Camins, À., Castañer, S., Juncadella, M., Morís, J., & Rodríguez-Fornells, A. (2017). Words are not enough: Nonword repetition as an indicator of arcuate fasciculus integrity during brain tumor resection. Journal of Neurosurgery, 126(2), 435-445. https://doi.org/10.3171/2016.2.JNS151592
Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143-155. https://doi.org/10.1002/hbm.10062
Thompson, C. K., Faroqi-Shah, Y., & Lee, J. (2015). Models of sentence production. In The handbook of adult language disorders (pp. 344-370). Psychology Press.
Tomasino, B., Tronchin, G., Marin, D., Maieron, M., Fabbro, F., Cubelli, R., Skrap, M., & Luzzatti, C. (2019). Noun-verb naming dissociation in neurosurgical patients. Aphasiology, 33(12), 1418-1440. https://doi.org/10.1080/02687038.2018.1542658
Tremblay, P., & Dick, A. S. (2016). Broca and Wernicke are dead, or moving past the classic model of language neurobiology. Brain and Language, 162, 60-71. https://doi.org/10.1016/j.bandl.2016.08.004
Tuncer, M. S., Salvati, L. F., Grittner, U., Hardt, J., Schilling, R., Bährend, I., Silva, L. L., Fekonja, L. S., Faust, K., Vajkoczy, P., Rosenstock, T., & Picht, T. (2021). Towards a tractography-based risk stratification model for language area associated gliomas. NeuroImage: Clinical, 29, 102541. https://doi.org/10.1016/j.nicl.2020.102541
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15(1), 273-289. https://doi.org/10.1006/nimg.2001.0978
Vanier, M., & Caplan, D. (1989). Chapter 3. CT-scan correlates of agrammatism. In L. Menn, L. K. Obler, G. Miceli, & M. O'Connor (Eds.), Agrammatic aphasia (pp. 37-114). John Benjamins Publishing Company. https://doi.org/10.1075/z.39.09van
Vigneau, M., Beaucousin, V., Hervé, P. Y., Duffau, H., Crivello, F., Houdé, O., Mazoyer, B., & Tzourio-Mazoyer, N. (2006). Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing. NeuroImage, 30(4), 1414-1432. https://doi.org/10.1016/j.neuroimage.2005.11.002
Whittle, I. R., Pringle, A.-M., & Taylor, R. (1998). Effects of resective surgery for left-sided intracranial tumours on language function: A prospective study. The Lancet, 351(9108), 1014-1018. https://doi.org/10.1016/S0140-6736(97)08295-0
Xu, J., Kemeny, S., Park, G., Frattali, C., & Braun, A. (2005). Language in context: Emergent features of word, sentence, and narrative comprehension. NeuroImage, 25(3), 1002-1015. https://doi.org/10.1016/j.neuroimage.2004.12.013
Yushkevich, P. A., & Gerig, G. (2017). ITK-SNAP: An intractive medical image segmentation tool to meet the need for expert-guided segmentation of complex medical images. IEEE Pulse, 8(4), 54-57. https://doi.org/10.1109/MPUL.2017.2701493
Yushkevich, P. A., Piven, J., Hazlett, H. C., Smith, R. G., Ho, S., Gee, J. C., & Gerig, G. (2006). User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. NeuroImage, 31(3), 1116-1128. https://doi.org/10.1016/j.neuroimage.2006.01.015

Auteurs

Effrosyni Ntemou (E)

International Doctorate for Approaches to Language and Brain (IDEALAB), University of Groningen, Groningen, The Netherlands.
International Doctorate for Approaches to Language and Brain (IDEALAB), University of Potsdam, Potsdam, Germany.
International Doctorate for Approaches to Language and Brain (IDEALAB), Newcastle University, Newcastle upon Tyne, UK.
International Doctorate for Approaches to Language and Brain (IDEALAB), Macquarie University, Sydney, New South Wales, Australia.
Centre for Language and Cognition Groningen (CLCG), University of Groningen, Groningen, The Netherlands.
Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Lena Rybka (L)

Centre for Language and Cognition Groningen (CLCG), University of Groningen, Groningen, The Netherlands.
Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Jocelyn Lubbers (J)

Centre for Language and Cognition Groningen (CLCG), University of Groningen, Groningen, The Netherlands.
Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Mehmet Salih Tuncer (MS)

Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Peter Vajkoczy (P)

Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Adrià Rofes (A)

Centre for Language and Cognition Groningen (CLCG), University of Groningen, Groningen, The Netherlands.

Thomas Picht (T)

Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.
Cluster of Excellence: "Matters of Activity. Image Space Material", Humboldt University, Berlin, Germany.

Katharina Faust (K)

Department of Neurosurgery, Charité - Universitätsmedizin Berlin, Berlin, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH