Right Hemisphere Grey Matter Volume and Language Functions in Stroke Aphasia

Sladjana Lukic, Elena Barbieri, Xue Wang, David Caplan, Swathi Kiran, Brenda Rapp, Todd B Parrish, Cynthia K Thompson, Sladjana Lukic, Elena Barbieri, Xue Wang, David Caplan, Swathi Kiran, Brenda Rapp, Todd B Parrish, Cynthia K Thompson

Abstract

The role of the right hemisphere (RH) in recovery from aphasia is incompletely understood. The present study quantified RH grey matter (GM) volume in individuals with chronic stroke-induced aphasia and cognitively healthy people using voxel-based morphometry. We compared group differences in GM volume in the entire RH and in RH regions-of-interest. Given that lesion site is a critical source of heterogeneity associated with poststroke language ability, we used voxel-based lesion symptom mapping (VLSM) to examine the relation between lesion site and language performance in the aphasic participants. Finally, using results derived from the VLSM as a covariate, we evaluated the relation between GM volume in the RH and language ability across domains, including comprehension and production processes both at the word and sentence levels and across spoken and written modalities. Between-subject comparisons showed that GM volume in the RH SMA was reduced in the aphasic group compared to the healthy controls. We also found that, for the aphasic group, increased RH volume in the MTG and the SMA was associated with better language comprehension and production scores, respectively. These data suggest that the RH may support functions previously performed by LH regions and have important implications for understanding poststroke reorganization.

Figures

Figure 1
Figure 1
Lesion overlap map of 40 participants with aphasia, showing areas of overlap, from no overlap (blue) to maximum overlap (red; N = 29 participants).
Figure 2
Figure 2
Six right hemisphere regions of interest (ROIs), derived from VBM analysis, used to evaluate between-group differences in the grey matter volume. SMA = green, MTG = red, insula = blue, hippocampus = violet, postcentral = yellow, and pallidum = cyan.
Figure 3
Figure 3
VLSM maps showing left hemisphere regions that were significantly associated with language performance. Panels (a–c) display lesions correlated with comprehension measures: (a) spoken word comprehension, (b) word semantic association, and (c) sentence comprehension. All voxels shown in color survived a threshold of p < 0.05, based on cluster size and the permutation method. The color bar reflects the range of t values from minimum (red) to maximum (yellow).
Figure 4
Figure 4
VBM maps showing right hemisphere regions where GM volume was significantly associated with language performance. Panel (a) shows the relationship between RH gray matter volume and spoken word comprehension. Panels (b–e) display the relationship between RH gray matter volume and production measures: (b) spoken word production, (c) oral reading, (d) spelling-to-dictation, and (e) sentence production. All voxels shown in color survived a threshold of p < 0.05, cluster-level FWE corrected. The color bar reflects the range of t values from minimum (red) to maximum (yellow).

References

    1. Gainotti G. Contrasting opinions on the role of the right hemisphere in the recovery of language. A critical survey. Aphasiology. 2015;29(9):1020–1037. doi: 10.1080/02687038.2015.1027170.
    1. Kiran S. What is the nature of poststroke language recovery and reorganization? ISRN Neurology. 2012;2012:13. doi: 10.5402/2012/786872.786872
    1. Price C. J. A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage. 2012;62(2):816–847. doi: 10.1016/j.neuroimage.2012.04.062.
    1. Thompson C. K., den Ouden D. B. Neuroimaging and recovery of language in aphasia. Current Neurology and Neuroscience Reports. 2008;8(6):475–483. doi: 10.1007/s11910-008-0076-0.
    1. Thompson C. K., Kielar A. Neural bases of sentence processing: evidence from neurolinguistic and neuroimaging studies. In: Goldrick M., Ferreira V., Miozzo M., editors. The Oxford Handbook of Language Production. New York, NY, USA: Oxford University Press; 2014. pp. 47–69.
    1. Turkeltaub P. Brain stimulation and the role of the right hemisphere in aphasia recovery. Current Neurology and Neuroscience Reports. 2015;15(72):1–9. doi: 10.1007/s11910-015-0593-6.
    1. Watila M. M., Balarabe S. A. Factors predicting post-stroke aphasia recovery. Journal of the Neurological Sciences. 2015;352(1):12–18. doi: 10.1016/j.jns.2015.03.020.
    1. Fernandez B., Cardebat D., Demonet J., et al. Functional MRI follow-up study of language processes in healthy subjects and during recovery in a case of aphasia. Stroke. 2004;35(9):2171–2176. doi: 10.1161/01.STR.0000139323.76769.b0.
    1. Heiss W., Thiel A., Kessler J., Herholz K. Disturbance and recovery of language function: correlates in PET activation studies. NeuroImage. 2003;20(Supplement 1):S42–S49. doi: 10.1016/j.neuroimage.2003.09.005.
    1. Ino T., Tokumoto K., Usami K., Kimura T., Hashimoto Y., Fukuyama H. Longitudinal fMRI study of reading in a patient with letter-by-letter reading. Cortex. 2008;44(7):773–781. doi: 10.1016/j.cortex.2007.03.002.
    1. Karbe H., Herholz K., Halber M., Heiss W. D. Collateral inhibition of transcallosal activity facilitates functional brain asymmetry. Journal of Cerebral Blood Flow & Metabolism. 1998;18(10):1157–1161. doi: 10.1097/00004647-199810000-00012.
    1. Saur D., Lange R., Baumgaertner A., et al. Dynamics of language reorganization after stroke. Brain. 2006;129(6):1371–1384. doi: 10.1093/brain/awl090.
    1. Cao Y., Vikingstad E. M., George K. P., Johnson A. F., Welch K. M. A. Cortical language activation in stroke patients recovering from aphasia with functional MRI. Stroke. 1999;30(11):2331–2340. doi: 10.1161/01.STR.30.11.2331.
    1. Fridriksson J., Bonilha L., Baker J., Mosen D., Rorden C. Activity in preserved left hemisphere regions predicts anomia severity in aphasia. Cerebral Cortex. 2010;20(5):1013–1019. doi: 10.1093/cercor/bhp160.
    1. Blasi V., Young A. C., Tansy A. P., Petersen S. E., Snyder A. Z., Corbetta M. Word retrieval learning modulates right frontal cortex in patients with left frontal damage. Neuron. 2002;36(1):159–170. doi: 10.1016/S0896-6273(02)00936-4.
    1. Crinion J., Price C. J. Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. Brain. 2005;128(12):2858–2871. doi: 10.1093/brain/awh659.
    1. Crosson B., Moore A. B., McGregor K. M., et al. Regional changes in word-production laterality after a naming treatment designed to produce a rightward shift in frontal activity. Brain and Language. 2009;111(2):73–85. doi: 10.1016/j.bandl.2009.08.001.
    1. Musso M., Weiller C., Kiebel S., Müller S. P., Bülau P., Rijntjes M. Training-induced brain plasticity in aphasia. Brain. 1999;122(9):1781–1790. doi: 10.1093/brain/122.9.1781.
    1. Ohyama M., Senda M., Kitamura S., Ishii K., Mishina M., Terashi A. Role of the nondominant hemisphere and undamaged area during word repetition in poststroke aphasics. A PET activation study. Stroke. 1996;27(5):897–903. doi: 10.1161/01.STR.27.5.897.
    1. Perani D., Cappa S. F., Tettamanti M., et al. A fMRI study of word retrieval in aphasia. Brain and Language. 2003;85(3):357–368. doi: 10.1016/S0093-934X(02)00561-8.
    1. Wan C. Y., Zheng X., Marchina S., Norton A., Schlaug G. Intensive therapy induces contralateral white matter changes in chronic stroke patients with Broca’s aphasia. Brain and Language. 2014;136:1–7. doi: 10.1016/j.bandl.2014.03.011.
    1. Weiller C., Isensee C., Rijntjes M., et al. Recovery from Wernicke's aphasia: a positron emission tomographic study. Annals of Neurology. 1995;37(6):723–732. doi: 10.1002/ana.410370605.
    1. Winhuisin L., Thiel A., Schumacher B., et al. Role of the contralateral inferior frontal gyrus in recovery of language function in poststroke aphasia: a combined repetitive transcranial magnetic stimulation and positron emission tomography study. Stroke. 2005;36(8):1759–1763. doi: 10.1161/01.STR.0000174487.81126.ef.
    1. Turkeltaub P., Messing S., Norise C., Hamilton R. H. Are networks for residual language function and recovery consistent across aphasic patients? Neurology. 2011;76(20):1726–1734. doi: 10.1212/WNL.0b013e31821a44c1.
    1. Breier J. I., Maher L. M., Novak B., Papanicolau A. C. Functional imaging before and after constraint-induced language therapy for aphasia using magnetoencephalography. Neurocase. 2006;12(6):322–331. doi: 10.1080/13554790601126054.
    1. Elkana O., Frost R., Kramer U., Ben-Bashat D., Schweiger A. Cerebral language reorganization in the chronic stage of recovery: a longitudinal fMRI study. Cortex. 2013;49(1):71–81. doi: 10.1016/j.cortex.2011.09.001.
    1. Fridriksson J., Morrow-Odom L., Moser D., Fridriksson A., Baylis G. Neural recruitment associated with anomia treatment in aphasia. NeuroImage. 2006;32(3):1402–1412. doi: 10.1016/j.neuroimage.2006.04.194.
    1. Fridriksson J., Moser D., Bonilha L., et al. Neural correlates of phonological and semantic-based anomia treatment in aphasia. Neuropsychologia. 2007;45(8):1812–1822. doi: 10.1016/j.neuropsychologia.2006.12.017.
    1. Kiran S., Meier E. L., Kapse K. J., Glynn P. A. Changes in task-based effective connectivity in language networks following rehabilitation in post-stroke patients with aphasia. Frontiers in Human Neuroscience. 2015;9:p. 316. doi: 10.3389/fnhum.2015.00316.
    1. Meinzer M., Obleser J., Flaisch T., Eulitz C., Rockstroh B. Recovery from aphasia as a function of language therapy in an early bilingual patient demonstrated by fMRI. Neuropsychologia. 2007;45(6):1247–1256. doi: 10.1016/j.neuropsychologia.2006.10.003.
    1. Thompson C. K., den Ouden D. B., Bonakdarpour B., Garibaldi K., Parrish T. B. Neural plasticity and treatment-induced recovery of sentence processing in agrammatism. Neuropsychologia. 2010;48(11):3211–3227. doi: 10.1016/j.neuropsychologia.2010.06.036.
    1. Raboyeau G., De Boissezon X., Marie N., et al. Right hemisphere activation in recovery from aphasia lesion effect or function recruitment? Neurology. 2008;70(4):290–298. doi: 10.1212/01.wnl.0000287115.85956.87.
    1. Abel S., Weiller C., Huber W., Willmes K. Neural underpinnings for model-oriented therapy of aphasic word production. Neuropsychologia. 2014;57:154–165. doi: 10.1016/j.neuropsychologia.2014.03.010.
    1. Gold B. T., Kertesz A. Right hemisphere semantic processing of visual words in an aphasic patient: an fMRI study. Brain and Language. 2000;73(3):456–465. doi: 10.1006/brln.2000.2317.
    1. Thompson C. K., Riley E. A., Den Ouden D. B., Meltzer-Asscher A., Lukic S. Training verb argument structure production in agrammatic aphasia: behavioral and neural recovery patterns. Cortex. 2013;49(9):2358–2376. doi: 10.1016/j.cortex.2013.02.003.
    1. Allendorfer J. B., Kissela B. M., Holland S. K., Szaflarski J. P. Different patterns of language activation in post-stroke aphasia are detected by overt and covert versions of the verb generation task. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research. 2012;18(3):CR135–CR137.
    1. Postman-Caucheteux W., Birn R., Pursley R., et al. Single-trial fMRI shows contralesional activity linked to overt naming errors in chronic aphasic patients. Journal of Cognitive Neuroscience. 2010;22(6):1299–1318. doi: 10.1162/jocn.2009.21261.
    1. Barwood C., Murdoch B., Whelan B., et al. Improved language performance subsequent to low-frequency rTMS in patients with chronic non-fluent aphasia post-stroke. European Journal of Neurology. 2010;18(7):935–943. doi: 10.1111/j.1468-1331.2010.03284.x.
    1. Hamilton R., Chrysikou E., Coslett H. B. Mechanisms of aphasia recovery after stroke and the role of noninvasive brain stimulation. Brain and Language. 2011;118(1-2):40–50. doi: 10.1016/j.bandl.2011.02.005.
    1. Martin P. I., Naeser M. A., Ho M., et al. Overt naming fMRI pre- and post-TMS: two nonfluent aphasia patients, with and without improved naming post-TMS. Brain and Language. 2009;111(1):20–35. doi: 10.1016/j.bandl.2009.07.007.
    1. Naeser M., Martin P., Nicholas M., et al. Improved picture naming in chronic aphasia after TMS to part of right Broca’s area: an open-protocol study. Brain and Language. 2005;93(1):95–105. doi: 10.1016/j.bandl.2004.08.004.
    1. Chieffo R., Ferrari F., Battista P., et al. Excitatory deep transcranial magnetic stimulation with H-coil over the right homologous Broca’s region improves naming in chronic post-stroke aphasia. Neurorehabilitation and Neural Repair. 2014;28(3):291–298. doi: 10.1177/1545968313508471.
    1. Hartwigsen G., Saur D., Price C. J., Ulmer S., Baumgaertner A., Siebner H. R. Perturbation of the left inferior frontal gyrus triggers adaptive plasticity in the right homologous area during speech production. PNAS. 2013;110(41):16402–16407. doi: 10.1073/pnas.1310190110.
    1. Kakuda W., Abo M., Kaito N., Watanabe M., Senoo A. Functional MRI-based therapeutic rTMS strategy for aphasic stroke patients: a case series pilot study. International Journal of Neuroscience. 2010;120(1):60–66. doi: 10.3109/00207450903445628.
    1. Geranmayeh F., Brownsett S. L., Wise R. J. Task-induced brain activity in aphasic stroke patients: what is driving recovery? Brain. 2014;137(10):2632–2648. doi: 10.1093/brain/awu163.
    1. van Oers C. A., Vink M., van Zandvoort M. J., et al. Contribution of the left and right inferior frontal gyrus in recovery from aphasia. A functional MRI study in stroke patients with preserved hemodynamic responsiveness. NeuroImage. 2010;49(1):885–893. doi: 10.1016/j.neuroimage.2009.08.057.
    1. Baumgaertner A., Hartwigsen G., Siebner H. R. Right-hemispheric processing of non-linguistic word features: implications for mapping language recovery after stroke. Human Brain Mapping. 2013;34(6):1293–1305. doi: 10.1002/hbm.21512.
    1. Fein G., McGillivray S., Finn P. Older adults make less advantageous decisions than younger adults: cognitive and psychological correlates. Journal of the International Neuropsychological Society. 2007;13(3):480–489. doi: 10.1017/S135561770707052X.
    1. Mungas D., Reed B. R., Jagust W. J., et al. Volumetric MRI predicts rate of cognitive decline related to AD and cerebrovascular disease. Neurology. 2002;59(6):867–873. doi: 10.1212/WNL.59.6.867.
    1. Zhang J., Meng L., Qin W., Liu N., Shi F. D., Yu C. Structural damage and functional reorganization in ipsilesional m1 in well-recovered patients with subcortical stroke. Stroke. 2014;45(3):788–793. doi: 10.1161/STROKEAHA.113.003425.
    1. Gauthier L. V., Taub E., Mark V. W., Barghi A., Uswatte G. Atrophy of spared gray matter tissue predicts poorer motor recovery and rehabilitation response in chronic stroke. Stroke. 2012;43(2):453–457. doi: 10.1161/STROKEAHA.111.633255.
    1. Schaechter J. D., Moore C. I., Connell B. D., Rosen B. R., Dijkhuizen R. N. Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. Brain. 2006;129(10):2722–2733. doi: 10.1093/brain/awl214.
    1. Stebbins G. T., Nyenhuis D. L., Wang C., et al. Gray matter atrophy in patients with ischemic stroke with cognitive impairment. Stroke. 2008;39(3):785–793. doi: 10.1161/STROKEAHA.107.507392.
    1. Ashburner J., Friston K. J. Voxel-based morphometry—the methods. NeuroImage. 2000;11(6 Pt 1):805–821. doi: 10.1006/nimg.2000.0582.
    1. Bates E., Wilson S. M., Saygin A. P., et al. Voxel-based lesion–symptom mapping. Nature Neuroscience. 2003;6(5):448–450. doi: 10.1038/nn1050.
    1. Xing S., Lacey E. H., Skipper-Kallal L. M., et al. Right hemisphere grey matter structure and language outcomes in chronic left hemisphere stroke. Brain. 2016;139(1):227–241. doi: 10.1093/brain/awv323.
    1. Kertesz A. Western Aphasia Battery (Revised) San Antonio: PsychCorp; 2007.
    1. Thompson C. K., Weintraub S. Northwestern Naming Battery (NNB) Evanston, IL: Northwestern University; 2014.
    1. Kay J., Lesser R., Coltheart M. Psycholinguistic assessments of language processing in aphasia (PALPA): an introduction. Aphasiology. 1996;10(2):159–180. doi: 10.1080/02687039608248403.
    1. Thompson C. K. Northwestern Assessment of Verbs and Sentences (NAVS) Evanston, IL: Northwestern University; 2012.
    1. Tustison N. J., Avants B. B., Cook P. A., et al. N4ITK: improved N3 bias correction. IEEE Transactions on Medical Imaging. 2010;29(6):1310–1320. doi: 10.1109/TMI.2010.2046908.
    1. Rorden C., Brett M. Stereotaxic display of brain lesions. Behavioural Neurology. 2000;12(4):191–200. doi: 10.1155/2000/421719.
    1. Alpert K., Kogan A., Parrish T., Marcus D., Wang L. The Northwestern University Neuroimaging Data Archive (NUNDA) NeuroImage. 2016;124, part B:1131–1136. doi: 10.1016/j.neuroimage.2015.05.060.
    1. Brett M., Anton J. L., Valabregue R., Poline J. B. Region of interest analysis using the MarsBar toolbox for SPM 99. NeuroImage. 2002;16(2):p. S497.
    1. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2015. URL
    1. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 1995;57(1):289–300.
    1. Cox R. W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research. 1996;29(3):162–173. doi: 10.1006/cbmr.1996.0014.
    1. Eklund A., Nichols T. E., Knutsson H. Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences. 2016;113(28):7900–7905. doi: 10.1073/pnas.1602413113.
    1. Hart J., Gordon B. Delineation of single-word semantic comprehension deficits in aphasia, with anatomical correlation. Annals of Neurology. 1990;27(3):226–231. doi: 10.1002/ana.410270303.
    1. Dronkers N. F., Wilkins D. P., Van Valin R. D., Redfern B. B., Jaeger J. J. Lesion analysis of the brain areas involved in language comprehension. Cognition. 2004;92(1):145–177. doi: 10.1016/j.cognition.2003.11.002.
    1. Booth J. R., Burman D. D., Meyer J. R., Gitelman D. R., Parrish T. B., Mesulam M. M. Modality independence of word comprehension. Human Brain Mapping. 2002;16(4):251–261. doi: 10.1002/hbm.10054.
    1. Tyler L. K., Marslen-Wilson W. D., Stamatakis E. A. Differentiating lexical form, meaning, and structure in the neural language system. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(23):8375–8380. doi: 10.1073/pnas.0408213102.
    1. Baker S. C., Frith C. D., Dolan R. J. The interaction between mood and cognitive function studied with PET. Psychological Medicine. 1997;27(3):565–578. doi: 10.1017/S0033291797004856.
    1. Berlingeri M., Crepaldi D., Roberti R., Scialfa G., Luzzatti C., Paulesu E. Nouns and verbs in the brain: grammatical class and task specific effects as revealed by fMRI. Cognitive Neuropsychology. 2008;25(4):528–558. doi: 10.1080/02643290701674943.
    1. Kemeny S., Ye F. Q., Birn R., Braun A. R. Comparison of continuous overt speech fMRI using BOLD and arterial spin labeling. Human Brain Mapping. 2005;24(3):173–183. doi: 10.1002/hbm.20078.
    1. Ardila A., Bernal B., Rosselli M. Participation of the insula in language revisited: a meta-analytic connectivity study. Journal of Neurolinguistics. 2014;29:31–41. doi: 10.1016/j.jneuroling.2014.02.001.
    1. Friederici A. D. Towards a neural basis of auditory sentence processing. Trends in Cognitive Sciences. 2002;6(2):78–84. doi: 10.1016/S1364-6613(00)01839-8.
    1. Rogalsky C., Hickok G. Selective attention to semantic and syntactic features modulates sentence processing networks in anterior temporal cortex. Cerebral Cortex. 2009;19(4):786–796. doi: 10.1093/cercor/bhn126.
    1. Friederici A. D., Kotz S. A., Scott S. K., Obleser J. Disentangling syntax and intelligibility in auditory language comprehension. Human Brain Mapping. 2010;31(3):448–457. doi: 10.1002/hbm.20878.
    1. Friederici A. D., Makuuchi M., Bahlmann J. The role of the posterior superior temporal cortex in sentence comprehension. Neuroreport. 2009;20(6):563–568. doi: 10.1097/WNR.0b013e3283297dee.
    1. Mack J. E., Meltzer-Asscher A., Barbieri E., Thompson C. K. Neural correlates of processing passive sentences. Brain Sciences. 2013;3(3):1198–1214. doi: 10.3390/brainsci3031198.
    1. Price C. J. The anatomy of language: a review of 100 fMRI studies published in 2009. Annals of the new York Academy of Sciences. 2010;119(1):62–88. doi: 10.1111/j.1749-6632.2010.05444.x.
    1. Caplan D., Michaud J., Hufford R. Mechanisms underlying syntactic comprehension deficits in vascular aphasia: new evidence from self-paced listening. Cognitive Neuropsychology. 2015;32(5):283–313. doi: 10.1080/02643294.2015.1058253.
    1. Lukic S., Bonakdarpour B., den Ouden D. B., Price C., Thompson C. K. Neural mechanisms of verb and sentence production: a lesion-deficit study. Procedia - Social and Behavioral Sciences. 2013;94:34–35. doi: 10.1016/j.sbspro.2013.09.014.
    1. Indefrey P., Levelt W. J. The spatial and temporal signatures of word production components. Cognition. 2004;92(1):101–144. doi: 10.1016/j.cognition.2002.06.001.
    1. Kawashima R., Okuda J., Umetsu A., et al. Human cerebellum plays an important role in memory-timed finger movement: an fMRI study. Journal of Neurophysiology. 2000;83(2):1079–1087.
    1. Bohland J. W., Guenther F. H. An fMRI investigation of syllable sequence production. NeuroImage. 2006;32(2):821–841. doi: 10.1016/j.neuroimage.2006.04.173.
    1. Loucks T. M., Poletto C. J., Simonyan K., Reynolds C. L., Ludlow C. L. Human brain activation during phonation and exhalation: common volitional control for two upper airway functions. NeuroImage. 2007;36(1):131–143. doi: 10.1016/j.neuroimage.2007.01.049.
    1. Alario F. X., Chainay H., Lehericy S., Cohen L. The role of the supplementary motor area (SMA) in word production. Brain Research. 2006;1076(1):129–143. doi: 10.1016/j.brainres.2005.11.104.
    1. Crosson B., Sadek J. R., Maron L., et al. Relative shift in activity from medial to lateral frontal cortex during internally versus externally guided word generation. Journal of Cognitive Neuroscience. 2001;13(2):272–283. doi: 10.1162/089892901564225.
    1. Dronkers N. F. A new brain region for coordinating speech articulation. Nature. 1996;384(6605):159–161. doi: 10.1038/384159a0.
    1. Shuren J. Insula and aphasia. Journal of Neurology. 1993;240(4):216–218. doi: 10.1007/BF00818707.
    1. Breitenstein C., Jansen A., Deppe M., et al. Hippocampus activity differentiates good from poor learners of a novel lexicon. NeuroImage. 2005;25(3):958–968. doi: 10.1016/j.neuroimage.2004.12.019.
    1. Maguire E. A., Frith C. D. The brain network associated with acquiring semantic knowledge. NeuroImage. 2004;22(1):171–178. doi: 10.1016/j.neuroimage.2003.12.036.
    1. Opitz B., Friederici A. D. Interactions of the hippocampal system and the prefrontal cortex in learning language-like rules. NeuroImage. 2003;19(4):1730–1737. doi: 10.1016/S1053-8119(03)00170-8.
    1. Meinzer M., Mohammadi S., Kugel H., et al. Integrity of the hippocampus and surrounding white matter is correlated with language training success in aphasia. NeuroImage. 2010;53(1):283–290. doi: 10.1016/j.neuroimage.2010.06.004.
    1. Menke R. A., Scholz J., Miller K. L., et al. MRI characteristics of the substantia nigra in Parkinson's disease: a combined quantitative T1 and DTI study. NeuroImage. 2009;47(2):435–441. doi: 10.1016/j.neuroimage.2009.05.017.
    1. Buckner R. L., Raichle M. E., Miezin F. M., Petersen S. E. Functional–anatomic studies of the recall of pictures and words from memory. The Journal of Neuroscience. 1996;16(19):6219–6235.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever