Abstract
Patients with phonologic alexia can be trained to read semantically impoverished words (e.g., functors) by pairing them with phonologically-related semantically rich words (e.g, nouns). What mechanisms underlie success in this cognitive re-training approach? Does the mechanism change if the skill is “overlearned”, i.e., practiced beyond criterion? We utilized fMRI pre- and post-treatment, and after overlearning, to assess treatment-related functional reorganization in a patient with phonologic alexia, 2 years post left temporoparietal stroke. Pre-treatment, there were no statistically significant differences in activation profiles across the sets of words. Post-treatment, accuracy on the two trained sets improved. Compared with untrained words, reading trained words recruited larger and more significant clusters of activation in the right hemisphere, including right inferior frontal and inferior parietal cortex. Post-overlearning, with near normal performance on overlearned words, predominant activation shifted to left hemisphere regions, including perilesional activation in superior parietal lobe, when reading overlearned vs. untrained words.
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Notes
Post-hoc analysis of a fourth pre-treatment baseline test revealed that YCR could read four words from each set of to-be-trained word lists (ITU and ITP). These words were therefore modeled as a nuisance variable in the following fMRI analyses.
References
Belin, P., Van Eeckhout, P., Zilbovicius, M., Remy, P. h., Francois, C., Guillaume, S., et al. (1996). Recovery from nonfluent aphasia after melodic intonation therapy: A PET study. Neurology, 47, 1504–1511.
Breier, J. I., Maher, L. M., Schmadeke, S., Hasan, K. M., & Papanicolaou, A. C. (2007). Changes in language-specific brain activation after therapy for aphasia using magnetoencephalography: A case study. Neurocase, 13, 169–177. doi:10.1080/13554790701448200.
Brett, M. (2003). The MNI brain and the Talairach atlas. [On-line], Available: http://www.mrc-cbu.cam.ac.uk/Imaging/mnispace.html.
Brett, M., Leff, A. P., Rorden, C., & Ashburner, J. (2001). Spatial normalization of brain images with focal lesions using cost function masking. NeuroImage, 14, 486–500.
Cappa, S. F., Perani, D., Grassi, F., Bressi, S., Alberoni, M., Franceschi, M., et al. (1997). A PET follow-up of recovery after stroke in acute aphasics. Brain and Language, 56, 55–67. doi:10.1006/brln.1997.1737.
Coltheart, M. (1981). Disorders of reading and their implications for models of normal reading. Visible Language, 15, 245–286.
Coltheart, M., Curtis, B., Atkins, P., & Haller, M. (1993). Models of reading aloud: Dual-route and parallel-distributed-processing approaches. Psychological Review, 100, 589–608. doi:10.1037/0033-295X.100.4.589.
Coltheart, M., Rastle, K., Perry, C., Langdon, R., & Ziegler, J. (2001). DRC: A dual route cascaded model of visual word recognition and reading aloud. Psychological Review, 108, 204–256. doi:10.1037/0033-295X.108.1.204.
Cornelissen, K., Laine, M., Tarkiainen, A., Jarvensivu, T., Martin, N., & Salmelin, R. (2003). Adult brain plasticity elicited by anomia treatment. Journal of Cognitive Neuroscience, 15, 444–461. doi:10.1162/089892903321593153.
DeLeon, J., Gottesman, R. F., Kleinman, J. T., Newhart, M., Davis, C., Heidler-Gary, J., et al. (2007). Neural regions essential for distinct cognitive processes underlying picture naming. Brain, 130, 1408–1422. doi:10.1093/brain/awm011.
de Partz, M. P. (1986). Re-education of a deep dyslexic patient: Rationale of the method and results. Cognitive Neuropsychology, 3, 149–177. doi:10.1080/02643298608252674.
Derouesne, J., & Beauvois, M. F. (1979). Phonological processing in reading: Data from alexia. Journal of Neurology, Neurosurgery and Psychiatry, 42, 1125–1132.
Eden, G. F., Joseph, J. E., Brown, H. E., Brown, C. P., & Zeffiro, T. A. (1999). Utilizing hemodynamic delay and dispersion to detect fMRI signal change without auditory interference: The behavior interleaved gradients technique. Magnetic Resonance in Medicine, 41, 13–20. doi:10.1002/(SICI)1522-2594(199901)41:1<13::AID-MRM4>3.0.CO;2-T.
Fernandez, B., Cardebat, D., Demonet, J. F., Joseph, P. A., Mazaux, J. M., Barat, M., et al. (2004). Functional MRI follow-up study of language processes in healthy subjects and during recovery in a case of aphasia. Stroke, 35, 2171–2176. doi:10.1161/01.STR.0000139323.76769.b0.
Friedman, R. B., & Lott, S. N. (2002). Is decreased maintenance of treatment effects in alexia a result of diminished capacity or deficient memory mechanisms? Brain and Language, 83, 133–136.
Friedman, R. B., Lott, S. N., & Sample, D. (1998). A reorganization approach to treating phonological alexia. Brain and Language, 65, 196–198.
Friedman, R. B., Sample, D., & Lott, S. N. (2002). The role of level of representation in the use of paired associate learning for rehabilitation of alexia. Neuropsychologia, 40, 223–234. doi:10.1016/S0028-3932(01)00098-7.
Gold, B. T., & Kertesz, A. (2000). Right hemisphere semantic processing of visual words in an aphasic patient: An fMRI study. Brain and Language, 73, 456–465. doi:10.1006/brln.2000.2317.
Goodglass, H., Kaplan, E., & Barresi, B. (2001). Boston Diagnostic Aphasia Examination (2nd ed.). Baltimore, MD: Lippincott, Williams and Williams.
Grabowski, T. J., Damasio, H., Eichhorn, G. R., & Tranel, D. (2003). Effects of gender on blood flow correlates of naming concrete entities. Neuroimage, 20, 940–954. doi:10.1016/S1053-8119(03)00284-2.
Heiss, W. D., Kessler, J., Thiel, A., Ghaemi, M., & Karbe, H. (1999). Differential capacity of left and right hemispheric areas for compensation of post-stroke aphasia. Annals of Neurology, 45, 430–438. doi:10.1002/1531-8249(199904)45:4<430::AID-ANA3>3.0.CO;2-P.
Hillis, A. E. (2006). The right place at the right time? Brain, 129, 1351–1353. doi:10.1093/brain/awl131.
Hillis, A. E. (1989). Efficacy and generalization of treatment for aphasic naming errors. Archives of Physical Medicine and Rehabilitation, 70, 632–636.
Jansen, A., Menke, R., Sommer, J., Forster, A. F., Bruchmann, S., Hempleman, J., et al. (2006). The assessment of hemispheric lateralization in functional MRI—Robustness and reproducibility. NeuroImage, 33, 204–217. doi:10.1016/j.neuroimage.2006.06.019.
Jobard, G., Crivello, F., & Tzourio-Mazoyer, N. (2003). Evaluation of the dual route theory of reading: A metanalysis of 35 neuroimaging studies. NeuroImage, 20, 693–712. doi:10.1016/S1053-8119(03)00343-4.
Kaplan, E., Goodglass, H., & Weintraub, S. (2001). The Boston naming test. Philadelphia: Lea and Febiger.
Kleim, J. A., Barbay, S., Cooper, N. R., Hogg, T. M., Reidel, C. N., Remple, M. S., et al. (2002). Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiology of Learning and Memory, 77, 63–77. doi:10.1006/nlme.2000.4004.
Kleim, J. A., & Jones, T. A. (2008). Principles of experience-dependent neural plasticity: Implications for rehabilitation after brain damage. Journal of Speech, Language, and Hearing Research, 51, S225–S239. doi:10.1044/1092-4388(2008/018).
Leger, A., Demonet, J.-F., Ruff, S., Aithamon, B., Touyeras, B., Puel, M., Boulanouar, K., & Cardebat, D. (2002). Neural substrates of spoken language rehabilitation in an aphasic patient: An fMRI study. NeuroImage, 17, 174–183.
Lott, N. S., Friedman, R. B., & Linebaugh, C. (1994). Rational and efficacy of a tactile–kinaesthetic treatment for alexia. Aphasiology, 8, 181–195. doi:10.1080/02687039408248650.
Marshall, J. C., & Newcombe, F. (1973). Patterns of paralexia: A psycholinguistic approach. Journal of Psycholinguistic Research, 2, 175–199. doi:10.1007/BF01067101.
McNeil, M. R., Doyle, P. J., Spencer, K., Jackson Goda, A., Flores, D., & Small, S. L. (1998). Effects of training multiple form classes on acquisition, generalization and maintenance of word retrieval in a single subject. Aphasiology, 12, 575–585. doi:10.1080/02687039808249559.
Meinzer, M., Flaisch, T., Obleser, J., Assadollahi, R., Djundja, D., Barthel, G., et al. (2006). Brain regions essential for improved lexical access in an aged aphasic patient: A case report. BMC Neurology, 6(28), 1–10.
Mesulam, M. M. (1990). Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Annals of Neurology, 28, 597–613. doi:10.1002/ana.410280502.
Mitchum, C. C., & Berndt, R. S. (1991). Diagnosis and treatment of the non-lexical route in acquired dyslexia: An illustration of the cognitive neuropsychological approach. Journal of Neurolinguistics, 6, 103–137. doi:10.1016/0911-6044(91)90003-2.
Monfils, M. H., Plautz, E. J., & Kleim, J. A. (2005). In search of the motor engram: Motor map plasticity as a mechanism for encoding motor experience. The Neuroscientist, 11, 471–483. doi:10.1177/1073858405278015.
Musso, M., Weiller, C., Kiebel, S., Muller, S. P., Bulau, P., & Rijntjes, M. (1999). Training-induced brain plasticity in aphasia. Brain, 122, 1781–1790. doi:10.1093/brain/122.9.1781.
Naeser, M. A., Martin, P. I., Baker, E. H., Hodge, S. M., Sczerzenie, S. E., Nicholas, M., et al. (2004). Overt propositional speech in chronic non-fluent aphasia studied with the dynamic susceptibility contrast fMRI method. Neuroimage, 22, 29–41. doi:10.1016/j.neuroimage.2003.11.016.
Nudo, R. J., & Friel, K. M. (1999). Cortical plasticity after stroke: Implications for rehabilitation. Revista de Neurologia, 155, 713–717.
Nudo, R. J., Milliken, G. W., Jenkins, W. M., & Merzenich, M. M. (1996). Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. Journal of Neuroscience, 16, 785–807.
Perani, D., Cappa, S. F., Tettamanti, M., Rosa, M., Scifo, P., Miozzo, A., et al. (2003). A fMRI study of word retrieval in aphasia. Brain and Language, 85, 357–368. doi:10.1016/S0093-934X(02)00561-8.
Price, C. J. (2000). The anatomy of language: Contributions from functional neuroimaging. Journal of Anatomy, 197, 335–359. doi:10.1046/j.1469-7580.2000.19730335.x.
Price, C. J., Gorno-Tempini, M. L., Graham, K. S., Biggio, N., Mechelli, A., Patterson, K., et al. (2003). Normal and pathological reading: Converging data from lesion and imaging studies. NeuroImage, 20, S30–S41. doi:10.1016/j.neuroimage.2003.09.012.
Pulvermuller, F., Hauk, O., Zohsel, K., Neininger, B., & Mohr, B. (2005). Therapy-related reorganization of language in both hemispheres of patients with chronic aphasia. NeuroImage, 28, 481–489. doi:10.1016/j.neuroimage.2005.06.038.
Raymer, A. M., Beeson, P., Holland, A., Kendal, D., Maher, L. M., et al. (2008). Translational research in aphasia: From neuroscience to neurorehabilitation. Journal of Speech, Language, and Hearing Research, 51, S259–S275. doi:10.1044/1092-4388(2008/020).
Rorden, C., & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioural Neurology, 12, 191–200.
Rosen, H. J., Peterson, S. E., Linenweber, M. R., Snyder, A. Z., White, D. A., Chapman, L., et al. (2000). Neural correlates of recovery from aphasia after damage to left inferior frontal cortex. Neurology, 55, 1883–1894.
Saur, D., Lange, R., Baumgaertner, A., Lange, R., Schraknepper, V., Willmes, K., et al. (2006). Dynamics of language reorganization after stroke. Brain, 129, 1371–1384. doi:10.1093/brain/awl090.
Small, S. L., Flores, D. K., & Noll, D. C. (1998). Different neural circuits subserve reading before and after therapy for acquired dyslexia. Brain and Language, 62, 298–308. doi:10.1006/brln.1998.1951.
Staudt, M., Grodd, W., Wildgruber, D., Erb, M., & Kraegeloh-Mann, I. (2001). The topography of right-hemispheric language dominance following early left-sided brain lesions. NeuroImage, 13, S844. doi:10.1016/S1053-8119(01)92186-X.
Thompson, C. K., Shapiro, L. P., Kiran, S., & Sobecks, J. (2003). The role of syntactic complexity in treatment of sentence deficits in agrammatic aphasia: The complexity account of treatment efficacy (CATE). Journal of Speech, Language and Hearing Research, 46, 591–607. doi:10.1044/1092-4388(2003/047).
Thulborn, K. R., Carpenter, P. A., & Just, M. A. (1999). Plasticity of language-related brain function during recovery from stroke. Stroke, 30, 749–754.
Vandenberghe, R., Price, C. J., et al. (1996). Semantic systems for words or pictures: Functional anatomy. Nature, 383, 254–256. doi:10.1038/383254a0.
Vitali, P., Abutalebia, J., Tettamanti, M., Danna, M., Ansaldo, A. I., Perani, D., et al. (2007). Training-induced brain remapping in chronic aphasia: A pilot study. Neurorehabilitation and Neural Repair, 21, 152–160. doi:10.1177/1545968306294735.
Wambaugh, J. L., Martinez, A. L., McNeil, M. R., & Rogers, M. A. (1999). Sound production treatment for apraxia of speech: Overgeneralization and maintenance effects. Aphasiology, 13, 821–837. doi:10.1080/026870399401902.
Warburton, E., Price, C. J., Swinburn, K., & Wise, R. J. (1999). Mechanisms of recovery from aphasia: Evidence from positron emission tomography studies. Journal of Neurology, Neurosurgery and Psychiatry, 66, 155–161.
Wilke, M., & Lidzba, K. (2007). LI-tool: A new toolbox to assess lateralization in functional MR-data. Journal of Neuroscience Methods, 163, 128–136. doi:10.1016/j.jneumeth.2007.01.026.
Wilke, M., & Schmithorst, V. J. (2006). A combined bootstrap/histogram approach for computing a lateralization index from neuroimaging data. NeuroImage, 33, 522–530. doi:10.1016/j.neuroimage.2006.07.010.
Acknowledgements
We are grateful to Nora Watson for acquisition of the behavioral data and to Elizabeth Lacey for editorial comments. We thank the two anonymous reviewers for their insightful and constructive criticism. This work was supported by NIH Grants R01 HD036019 and R01 DC007169 to the PI (RBF). Anne Sperling contributed to this research while a post-doctoral fellow at GUMC; she is now at the National Institute of Mental Health (NIMH). The views expressed in this article do not necessarily represent the views of the NIMH.
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Kurland, J., Cortes, C.R., Wilke, M. et al. Neural Mechanisms Underlying Learning Following Semantic Mediation Treatment in a Case of Phonologic Alexia. Brain Imaging and Behavior 2, 147–162 (2008). https://doi.org/10.1007/s11682-008-9027-2
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DOI: https://doi.org/10.1007/s11682-008-9027-2