Naming errors and dysfunctional tissue metrics predict language recovery after acute left hemisphere stroke

Erin L Meier, Shannon M Sheppard, Emily B Goldberg, Catherine R Head, Delaney M Ubellacker, Alexandra Walker, Argye E Hillis, Erin L Meier, Shannon M Sheppard, Emily B Goldberg, Catherine R Head, Delaney M Ubellacker, Alexandra Walker, Argye E Hillis

Abstract

Language recovery following acute left hemisphere (LH) stroke is notoriously difficult to predict. Global language measures (e.g., overall aphasia severity) and gross lesion metrics (e.g., size) provide incomplete recovery predictions. In this study, we test the hypothesis that the types of naming errors patients produce, combined with dysfunctional brain tissue metrics, can provide additional insight into recovery following acute LH stroke. One hundred forty-eight individuals who were hospitalized with a new LH stroke completed clinical neuroimaging and assessments of naming and global language skills. A subset of participants again completed language testing at subacute, early (5-7 months post-stroke), and late (≥11 months post-stroke) chronic phases. At each time point, we coded naming errors into four types (semantic, phonological, mixed and unrelated) and determined error type totals and proportions. Dysfunctional tissue measures included the percentage of damage to language network regions and hypoperfusion in vascular territories. A higher proportion of semantic errors was associated with better acute naming, but higher proportions of other error types was related to poorer accuracy. Naming and global language skills significantly improved over time , but naming error profiles did not change. Fewer acute unrelated errors and less damage to left angular gyrus resulted in optimal naming and language recovery by the final testing time point, yet patients with more acute errors and damage to left middle temporal gyrus demonstrated the greatest increases in language over time. These results illustrate that naming error profiles, particularly unrelated errors, add power to predictions of language recovery after stroke.

Keywords: Language; Left hemisphere stroke; Longitudinal; Naming errors; Recovery; Structural imaging.

Conflict of interest statement

None.

Copyright © 2020 Elsevier Ltd. All rights reserved.

Figures

Fig. 1
Fig. 1
Lesion overlap. Overlay of lesions across the sample of patients with error data at the acute stage and at least one later time point (n = 46).

References

    1. Basso A., Corno M., Marangolo P. Evolution of oral and written confrontation naming errors in aphasia. A retrospective study on vascular patients. J. Clin. Exp. Neuropsychol. 1996;18(1):77–87. doi: 10.1080/01688639608408264.
    1. Beaulieu C., De Crespigny A., Tong D.C., Moseley M.E., Albers G.W., Marks M.P. Longitudinal magnetic resonance imaging study of perfusion and diffusion in stroke: evolution of lesion volume and correlation with clinical outcome. Ann. Neurol. 1999;46(4):568–578. doi: 10.1002/1531-8249(199910)46:4<568::AID-ANA4>;2-R.
    1. Benjamin E.J., Muntner P., Alonso A., Bittencourt M.S., Callaway C.W., Carson A.P., Chamberlain A.M., Chang A.R., Cheng S., Das S.R., Delling F.N., Djousse L., Elkind M.S.V., Ferguson J.F., Fornage M., Jordan L.C., Khan S.S., Kissela B.M., Knutson K.L. … on behalf of the American heart association council on epidemiology and prevention statistics committee and stroke statistics subcommittee. Heart disease and stroke statistics—2019 update: A report from the American Heart Association. Circulation. 2019;139(10) doi: 10.1161/CIR.0000000000000659.
    1. Binder J.R., Desai R.H. The neurobiology of semantic memory. Trends Cognit. Sci. 2011;15(11):527–536. doi: 10.1016/j.tics.2011.10.001.
    1. Binder J.R., Desai R.H., Graves W.W., Conant L.L. Where Is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebr. Cortex. 2009;19(12):2767–2796. doi: 10.1093/cercor/bhp055.
    1. Bonilha L., Gleichgerrcht E., Nesland T., Rorden C., Fridriksson J. Success of anomia treatment in aphasia is associated with preserved architecture of global and left temporal lobe structural networks. Neurorehabilitation Neural Repair. 2016;30(3):266–279.
    1. Breier J.I., Juranek J., Papanicolaou A.C. Changes in maps of language function and the integrity of the arcuate fasciculus after therapy for chronic aphasia. Neurocase. 2011;17(6):506–517. doi: 10.1080/13554794.2010.547505.
    1. Brett M., Anton J., Valabregue R., Poline J.B. Region of interest analysis using the MarsBar toolbox for. SPM. 2002;99(2):S497. 16.
    1. Brookshire R.H., Nicholas L.E. Relationship of word frequency in printed materials and judgements of word frequency in daily life to Boston Naming Test of performance of aphasic adults. Clinical Aphasiology. 1995;23:107–119.
    1. Capitani E., Laiacona M. A method for studying the evolution of naming error types in the recovery of acute aphasia: a single-patient and single-stimulus approach. Neuropsychologia. 2004;42(5):613–623. doi: 10.1016/j.neuropsychologia.2003.10.006.
    1. Caramazza A., Hillis A.E. Where do semantic errors come from? Cortex. 1990;26(1):95–122. doi: 10.1016/S0010-9452(13)80077-9.
    1. Catani M., Thiebaut de Schotten M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex. 2008;44(8):1105–1132. doi: 10.1016/j.cortex.2008.05.004.
    1. Chen Q., Middleton E., Mirman D. Words fail: lesion-symptom mapping of errors of omission in post-stroke aphasia. J. Neuropsychol. 2019;13(2):183–197. doi: 10.1111/jnp.12148.
    1. Connor L.T., Spiro A., Obler L.K., Albert M.L. Change in object naming ability during adulthood. J. Gerontol. B Psychol. Sci. Soc. Sci. 2004;59(5):P203–P209. doi: 10.1093/geronb/59.5.P203.
    1. Crary M.A., Kertesz A. Evolving error profiles during aphasia syndrome remission. Aphasiology. 1988;2(1):67–77. doi: 10.1080/02687038808248888.
    1. Davey J., Cornelissen P.L., Thompson H.E., Sonkusare S., Hallam G., Smallwood J., Jefferies E. Automatic and controlled semantic retrieval: TMS reveals distinct contributions of posterior middle temporal gyrus and angular gyrus. J. Neurosci. 2015;35(46):15230–15239. doi: 10.1523/JNEUROSCI.4705-14.2015.
    1. DeLeon J., Gottesman R.F., Kleinman J.T., Newhart M., Davis C., Heidler-Gary J., Lee A., Hillis A.E. Neural regions essential for distinct cognitive processes underlying picture naming. Brain. 2007;130(5):1408–1422. doi: 10.1093/brain/awm011.
    1. Dell G.S., O’Seaghdha P.G. Stages of lexical access in language production. Cognition. 1992;42(1–3):287–314.
    1. Dell G.S., Schwartz M.F., Martin N., Saffran E.M., Gagnon D.A. Lexical access in aphasic and nonaphasic speakers. Psychol. Rev. 1997;104(4):801–838.
    1. Dell Gary S., Lawler E.N., Harris H.D., Gordon J.K. Models of errors of omission in aphasic naming. Cogn. Neuropsychol. 2004;21(2–4):125–145. doi: 10.1080/02643290342000320.
    1. Engelter S.T., Gostynski M., Papa S., Frei M., Born C., Ajdacic-Gross V., Gutzwiller F., Lyrer P.A. Epidemiology of aphasia attributable to first ischemic stroke: incidence, severity, fluency, etiology, and thrombolysis. Stroke. 2006;37(6):1379–1384. doi: 10.1161/01.STR.0000221815.64093.8c.
    1. Faria A.V., Joel S.E., Zhang Y., Oishi K., van Zjil P.C.M., Miller M.I., Pekar J.J., Mori S. Atlas-based analysis of resting-state functional connectivity: evaluation for reproducibility and multi-modal anatomy–function correlation studies. Neuroimage. 2012;61(3):613–621. doi: 10.1016/j.neuroimage.2012.03.078.
    1. Fisher N.J., Tierney M.C., Snow G.W., Szalai J.P. Odd/even short forms of the Boston Naming Test: preliminary geriatric norms. Clin. Neuropsychol. 1999;13(3):359–364. doi: 10.1076/clin.13.3.359.1742.
    1. Flowers H.L., Skoretz S.A., Silver F.L., Rochon E., Fang J., Flamand-Roze C., Martino R. Poststroke aphasia frequency, recovery, and outcomes: a systematic review and meta-analysis. Arch. Phys. Med. Rehabil. 2016;97(12):2188–2201. doi: 10.1016/j.apmr.2016.03.006. e8.
    1. Foygel D., Dell G.S. Models of impaired lexical access in speech production. J. Mem. Lang. 2000;43(2):182–216. doi: 10.1006/jmla.2000.2716.
    1. Fridriksson J. Preservation and modulation of specific left hemisphere regions is vital for treated recovery from anomia in stroke. J. Neurosci. 2010;30(35):11558–11564. doi: 10.1523/JNEUROSCI.2227-10.2010.
    1. Fridriksson J., den Ouden D.-B., Hillis A.E., Hickok G., Rorden C., Basilakos A., Yourganov G., Bonilha L. Anatomy of aphasia revisited. Brain. 2018;141(3):848–862. doi: 10.1093/brain/awx363.
    1. Goodglass H., Kaplan E., Barresi B. third ed. Lippincott Williams & Wilkins; 2001. BDAE-3: Boston Diagnostic Aphasia Examination.
    1. Goodglass H., Wingfield A., editors. Anomia: Neuroanatomical and Cognitive Correlates. Academic Press; 1997.
    1. Griffis J.C., Nenert R., Allendorfer J.B., Szaflarski J.P. Damage to white matter bottlenecks contributes to language impairments after left hemispheric stroke. Neuroimage: Clinical. 2017;14:552–565. doi: 10.1016/j.nicl.2017.02.019.
    1. Griffis J.C., Nenert R., Allendorfer J.B., Szaflarski J.P. Linking left hemispheric tissue preservation to fMRI language task activation in chronic stroke patients. Cortex. 2017;96:1–18. doi: 10.1016/j.cortex.2017.08.031.
    1. Grima R., Franklin S. Usefulness of investigating error profiles in diagnosis of naming impairments. Int. J. Lang. Commun. Disord. 2017;52(2):214–226. doi: 10.1111/1460-6984.12266.
    1. Hillis A.E., Gold L., Kannan V., Cloutman L., Kleinman J.T., Newhart M., Heidler-Gary J., Davis C., Aldrich E., Llinas R., Gottesman R.F. Site of the ischemic penumbra as a predictor of potential for recovery of functions. Neurology. 2008;71(3):184–189. doi: 10.1212/01.wnl.0000317091.17339.98.
    1. Hillis A.E., Kleinman J.T., Newhart M., Heidler-Gary J., Gottesman R., Barker P.B., Aldrich E., Llinas R., Wityk R., Chaudhry P. Restoring cerebral blood flow reveals neural regions critical for naming. J. Neurosci. 2006;26(31):8069–8073. doi: 10.1523/JNEUROSCI.2088-06.2006.
    1. Hillis A.E., Beh Y.Y., Sebastian R., Breining B., Tippett D.C., Wright A., Saxena S., Rorden C., Bonilha L., Basilakos A., Yourganov G., Fridriksson J. Predicting recovery in acute poststroke aphasia. Ann. Neurol. 2018;83(3):612–622. doi: 10.1002/ana.25184.
    1. Hillis A.E., Caramazza A. The compositionality of lexical semantic representations: clues from semantic errors in object naming. Memory. 1995;3(3–4):333–358. doi: 10.1080/09658219508253156.
    1. Hillis A.E., Heidler J. Mechanisms of early aphasia recovery. Aphasiology. 2002;16(9):885–895. doi: 10.1080/0268703.
    1. Hillis A.E., Kane A., Tuffiash E., Ulatowski J.A., Barker P.B., Beauchamp N.J., Wityk R.J. Reperfusion of specific brain regions by raising blood pressure restores selective language functions in subacute stroke. Brain Lang. 2001;79(3):495–510. doi: 10.1006/brln.2001.2563.
    1. Hillis A.E., Wityk R.J., Tuffiash E., Beauchamp N.J., Jacobs M.A., Barker P.B., Selnes O.A. Hypoperfusion of Wernicke's area predicts severity of semantic deficit in acute stroke. Ann. Neurol. 2001;50(5):561–566. doi: 10.1002/ana.1265.
    1. Holland R., Johns S.L., Woollams A.M. The impact of phonological versus semantic repetition training on generalisation in chronic stroke aphasia reflects differences in dorsal pathway connectivity. Neuropsychol. Rehabil. 2016:1–20. doi: 10.1080/09602011.2016.1190384.
    1. Hosomi A., Nagakane Y., Yamada K., Kuriyama N., Mizuno T., Nishimura T., Nakagawa M. Assessment of arcuate fasciculus with diffusion-tensor tractography may predict the prognosis of aphasia in patients with left middle cerebral artery infarcts. Neuroradiology. 2009;51(9):549–555. doi: 10.1007/s00234-009-0534-7.
    1. Humphreys G.F., Lambon Ralph M.A. Fusion and fission of cognitive functions in the human parietal cortex. Cerebr. Cortex. 2015;25(10):3547–3560. doi: 10.1093/cercor/bhu198.
    1. Indefrey P., Levelt W.J.M. The spatial and temporal signatures of word production components. Cognition. 2004;92(1–2):101–144. doi: 10.1016/j.cognition.2002.06.001.
    1. Jang S.H., Lee H.D. Recovery of injured arcuate fasciculus in the dominant hemisphere in a patient with an intracerebral hemorrhage. Am. J. Phys. Med. Rehabil. 2014;93(12):e15–e18. doi: 10.1097/PHM.0000000000000202.
    1. Jefferies E., Baker S.S., Doran M., Ralph M.A.L. Refractory effects in stroke aphasia: a consequence of poor semantic control. Neuropsychologia. 2007;45(5):1065–1079. doi: 10.1016/j.neuropsychologia.2006.09.009.
    1. Jefferies E., Lambon Ralph M.A. Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. Brain. 2006;129(8):2132–2147. doi: 10.1093/brain/awl153.
    1. Jefferies E., Patterson K., Ralph M.A.L. Deficits of knowledge versus executive control in semantic cognition: insights from cued naming. Neuropsychologia. 2008;46(2):649–658. doi: 10.1016/j.neuropsychologia.2007.09.007.
    1. Kertesz A. Pearson; 2007. Western Aphasia Battery: Revised.
    1. Kim S.H., Jang S.H. Prediction of aphasia outcome using diffusion tensor tractography for arcuate fasciculus in stroke. Am. J. Neuroradiol. 2013;34(4):785–790. doi: 10.3174/ajnr.A3259.
    1. Kohn S.E., Smith K.L. Evolution of impaired access to the phonological lexicon. J. Neurolinguistics. 1994;8(4):267–288. doi: 10.1016/0911-6044(94)90013-2.
    1. Lambon Ralph M.A., Jefferies E., Patterson K., Rogers T.T. The neural and computational bases of semantic cognition. Nat. Rev. Neurosci. 2016;18(1):42–55. doi: 10.1038/nrn.2016.150.
    1. Lambon Ralph M.A., Moriarty L., Sage K. Anomia is simply a reflection of semantic and phonological impairments: evidence from a case-series study. Aphasiology. 2002;16(1–2):56–82. doi: 10.1080/02687040143000448.
    1. Laska A.C., Hellblom A., Murray V., Kahan T., Von Arbin M. Aphasia in acute stroke and relation to outcome. J. Intern. Med. 2001;249(5):413–422.
    1. Lazar R.M., Speizer A.E., Festa J.R., Krakauer J.W., Marshall R.S. Variability in language recovery after first-time stroke. J. Neurol. Neurosurg. Psychiatr. 2008;79(5):530–534. doi: 10.1136/jnnp.2007.122457.
    1. Lazar R.M., Boehme A.K. Aphasia as a predictor of stroke outcome. Curr. Neurol. Neurosci. Rep. 2017;17(11) doi: 10.1007/s11910-017-0797-z.
    1. Le Dorze G., Durocher J. The effects of age, educational level, and stimulus length on naming in normal subjects. J. Speech Lang. Pathol. Audiol. 1992;16(1):21–29.
    1. Le Dorze G., Nespoulous J.-L. Anomia in moderate aphasia: problems in accessing the lexical representation. Brain Lang. 1989;37(3):381–400. doi: 10.1016/0093-934X(89)90026-6.
    1. Levelt W.J., Roelofs A., Meyer A.S. A theory of lexical access in speech production. Behavioral and Brain Sciences. 1999;22(1):1–38.
    1. McKinnon E.T., Fridriksson J., Glenn G.R., Jensen J.H., Helpern J.A., Basilakos A., Rorden C., Shih A.Y., Spampinato M.V., Bonilha L. Structural plasticity of the ventral stream and aphasia recovery. Ann. Neurol. 2017;82(1):147–151. doi: 10.1002/ana.24983.
    1. Meier E.L., Johnson J.P., Pan Y., Kiran S. Brain Imaging and Behavior. 2019. The utility of lesion classification in predicting language and treatment outcomes in chronic stroke-induced aphasia.
    1. Mirman D., Britt A.E. What we talk about when we talk about access deficits. Phil. Trans. Biol. Sci. 2013;369(1634):20120388. doi: 10.1098/rstb.2012.0388. 20120388.
    1. Mitchum C.C., Ritgert B.A., Sandson J., Berndt R.S. The use of response analysis in confrontation naming. Aphasiology. 1990;4(3):261–279. doi: 10.1080/02687039008249079.
    1. Moerman C., Corluy R., Meersman W. Exploring the aphasiac's naming disturbances; A new approach using the neighbourhood limited classification method. Cortex. 1983;19(4):529–543. doi: 10.1016/S0010-9452(83)80034-3.
    1. Mori S., Oishi K., Jiang H., Jiang L., Li X., Akhter K., Hua K., Faria A.V., Mahmood A., Woods R., Toga A.W., Pike G.B., Neto P.R., Evans A., Zhang J., Huang H., Miller M.I., van Zijl P., Mazziotta J. Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage. 2008;40(2):570–582. doi: 10.1016/j.neuroimage.2007.12.035.
    1. Neils J., Baris J.M., Carter C., Dell’aira A.L., Nordloh S.J., Weiler E., Weisiger B. Effects of age, education, and living environment on Boston Naming Test performance. J. Speech Hear. Res. 1995;38(5):1143–1149. doi: 10.1044/jshr.3805.1143.
    1. Nicholas L.E., Brookshire R.H., Maclennan D.L., Schumacher J.G., Porrazzo S.A. Revised administration and scoring procedures for the Boston Naming test and norms for non-brain-damaged adults. Aphasiology. 1989;3(6):569–580. doi: 10.1080/02687038908249023.
    1. Noonan K.A., Jefferies E., Visser M., Lambon Ralph M.A. Going beyond inferior prefrontal involvement in semantic control: evidence for the additional contribution of dorsal angular gyrus and posterior middle temporal cortex. J. Cognit. Neurosci. 2013;25(11):1824–1850. doi: 10.1162/jocn_a_00442.
    1. Paolieri D., Marful A., Morales L., Bajo M.T. The modulating effect of education on semantic interference during healthy aging. PloS One. 2018;13(1) doi: 10.1371/journal.pone.0191656.
    1. Pedersen P.M., Vinter K., Olsen T.S. Aphasia after stroke: type, severity and prognosis. Cerebrovasc. Dis. 2003;17(1):35–43. doi: 10.1159/000073896.
    1. Plaut D.C. Double dissociation without modularity: evidence from connectionist neuropsychology. J. Clin. Exp. Neuropsychol. 1995;17(2):291–321. doi: 10.1080/01688639508405124.
    1. Plowman E., Hentz B., Ellis C. Post-stroke aphasia prognosis: a review of patient-related and stroke-related factors: aphasia prognosis. J. Eval. Clin. Pract. 2012;18(3):689–694. doi: 10.1111/j.1365-2753.2011.01650.x.
    1. R Core Team . R Foundation for Statistical Computing; 2020. R: A Language and Environment for Statistical Computing.
    1. Rapp B., Goldrick M. Discreteness and interactivity in spoken word production. Psychol. Rev. 2000;107(3):460–499. doi: 10.1037/0033-295X.107.3.460.
    1. Reyes D., Hitomi E., Simpkins A., Lynch J., Hsia A., Benson R., Nadareishvili Z., Luby M., Latour L., Leigh R. Detection of perfusion deficits using FLAIR and GRE based vessel signs. Stroke. 2017;48(Suppl. l_1):ATP63. doi: 10.1161/str.48.suppl_1.tp63. ATP63.
    1. Rorden C., Bonilha L., Fridriksson J., Bender B., Karnath H.-O. Age-specific CT and MRI templates for spatial normalization. Neuroimage. 2012;61(4):957–965. doi: 10.1016/j.neuroimage.2012.03.020.
    1. Schlaug G., Marchina S., Norton A. Evidence for plasticity in white-matter tracts of patients with chronic Broca's aphasia undergoing intense intonation-based speech therapy. Ann. N. Y. Acad. Sci. 2009;1169(1):385–394. doi: 10.1111/j.1749-6632.2009.04587.x.
    1. Schuell H., Jenkins J.J. Reduction of vocabulary in aphasia. Brain. 1961;84(2):243–261. doi: 10.1093/brain/84.2.243.
    1. Schwartz M., Dell G., Martin N., Gahl S., Sobel P. A case-series test of the interactive two-step model of lexical access: evidence from picture naming. J. Mem. Lang. 2006;54(2):228–264. doi: 10.1016/j.jml.2005.10.001.
    1. Schwartz M.F., Brecher A. A model-driven analysis of severity, response characteristics, and partial recovery in aphasics' picture naming. Brain Lang. 2000;73(1):62–91. doi: 10.1006/brln.2000.2310.
    1. Seghier M.L. The angular gyrus multiple functions and multiple subdivisions. Neuroscientist. 2013;19(1):43–61.
    1. Sorensen A.G., Buonanno F.S., Gonzalez R.G., Schwamm L.H., Lev M.H., Huang-Hellinger F.R., Reese T.G., Weisskoff R.M., Davis T.L., Suwanwela N., Can U., Moreira J.A., Copen W.A., Look R.B., Finklestein S.P., Rosen B.R., Koroshetz W.J. Hyperacute stroke: evaluation with combined multisection diffusion-weighted and hemodynamically weighted echo-planar MR imaging. Radiology. 1996;199(2):391–401. doi: 10.1148/radiology.199.2.8668784.
    1. Staff R.T., Murray A.D., Deary I.J., Whalley L.J. What provides cerebral reserve? Brain. 2004;127(5):1191–1199. doi: 10.1093/brain/awh144.
    1. Tallberg I.M. The Boston naming test in Swedish: normative data. Brain Lang. 2005;94(1):19–31. doi: 10.1016/j.bandl.2004.11.004.
    1. van Hees S., McMahon K., Angwin A., de Zubicaray G., Read S., Copland D.A. Changes in white matter connectivity following therapy for anomia post stroke. Neurorehabilitation Neural Repair. 2014;28(4):325–334.
    1. Wade D.T., Hewer R.L., David R.M., Enderby P.M. Aphasia after stroke: natural history and associated deficits. J. Neurol. Neurosurg. Psychiatry. 1986;49(1):11–16.
    1. Watila M.M., Balarabe S.A. Factors predicting post-stroke aphasia recovery. J. Neurol. Sci. 2015;352(1–2):12–18. doi: 10.1016/j.jns.2015.03.020.
    1. Whitney C., Kirk M., O’Sullivan J., Lambon Ralph M.A., Jefferies E. Executive semantic processing Is underpinned by a large-scale neural network: revealing the contribution of left prefrontal, posterior temporal, and parietal cortex to controlled retrieval and selection using TMS. J. Cognit. Neurosci. 2012;24(1):133–147. doi: 10.1162/jocn_a_00123.
    1. Xu Y., He Y., Bi Y. A tri-network model of human semantic processing. Front. Psychol. 2017;8 doi: 10.3389/fpsyg.2017.01538.
    1. Xu Y., Lin Q., Han Z., He Y., Bi Y. Intrinsic functional network architecture of human semantic processing: modules and hubs. Neuroimage. 2016;132:542–555. doi: 10.1016/j.neuroimage.2016.03.004.

Source: PubMed

3
Suscribir