The Neural Basis of Successful Word Reading in Aphasia

Abstract Understanding the neural basis of recovery from stroke is a major research goal. Many functional neuroimaging studies have identified changes in brain activity in people with aphasia, but it is unclear whether these changes truly support successful performance or merely reflect increased task difficulty. We addressed this problem by examining differences in brain activity associated with correct and incorrect responses on an overt reading task. On the basis of previous proposals that semantic retrieval can assist pronunciation of written words, we hypothesized that recruitment of semantic areas would be greater on successful trials. Participants were 21 patients with left-hemisphere stroke with phonologic retrieval deficits. They read words aloud during an event-related fMRI paradigm. BOLD signals obtained during correct and incorrect trials were contrasted to highlight brain activity specific to successful trials. Successful word reading was associated with higher BOLD signal in the left angular gyrus. In contrast, BOLD signal in bilateral posterior inferior frontal cortex, SMA, and anterior cingulate cortex was greater on incorrect trials. These data show for the first time the brain regions where neural activity is correlated specifically with successful performance in people with aphasia. The angular gyrus is a key node in the semantic network, consistent with the hypothesis that additional recruitment of the semantic system contributes to successful word production when phonologic retrieval is impaired. Higher activity in other brain regions during incorrect trials likely reflects secondary engagement of attention, working memory, and error monitoring processes when phonologic retrieval is unsuccessful.

[1]  James L. McClelland,et al.  Understanding normal and impaired word reading: computational principles in quasi-regular domains. , 1996, Psychological review.

[2]  Margaret A. Naeser,et al.  TMS suppression of right pars triangularis, but not pars opercularis, improves naming in aphasia , 2011, Brain and Language.

[3]  A. Friederici,et al.  The role of the right inferior frontal gyrus in the processing of non-local dependencies in music , 2016 .

[4]  Michael J Cortese,et al.  Imageability ratings for 3,000 monosyllabic words , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[5]  Michael C. Doyle,et al.  Effects of frequency on visual word recognition tasks: where are they? , 1989, Journal of experimental psychology. General.

[6]  Cathy J Price,et al.  The latest on functional imaging studies of aphasic stroke , 2005, Current opinion in neurology.

[7]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[8]  Jeffrey R. Binder,et al.  Some neurophysiological constraints on models of word naming , 2005, NeuroImage.

[9]  Julius Fridriksson,et al.  Cortical mapping of naming errors in aphasia , 2009, Human brain mapping.

[10]  Roy H. Hamilton,et al.  Mechanisms of aphasia recovery after stroke and the role of noninvasive brain stimulation , 2011, Brain and Language.

[11]  Colin Humphries,et al.  Anatomy is strategy: Skilled reading differences associated with structural connectivity differences in the reading network , 2014, Brain and Language.

[12]  Mark S. Seidenberg,et al.  Semantic effects in single-word naming. , 1995, Journal of experimental psychology. Learning, memory, and cognition.

[13]  C. Thompson,et al.  Erratum: The role of semantic complexity in treatment of naming deficits: Training semantic categories in fluent aphasia by controlling exemplar typicality (Journal of Speech, Language, and Hearing Research (June 2003) 46: (608-622)) , 2003 .

[14]  B. Douglas Ward,et al.  Deconvolution Analysis of FMRI Time Series Data , 2006 .

[15]  F. Molteni,et al.  The anatomical foundations of acquired reading disorders: A neuropsychological verification of the dual-route model of reading , 2014, Brain and Language.

[16]  Maya L. Henry,et al.  Phonological dyslexia and dysgraphia: Cognitive mechanisms and neural substrates , 2009, Cortex.

[17]  M. Corbetta,et al.  Neural correlates of recovery from aphasia after damage to left inferior frontal cortex , 2000, Neurology.

[18]  J. Hodges,et al.  Non-verbal semantic impairment in semantic dementia , 2000, Neuropsychologia.

[19]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[20]  J. Smallwood,et al.  The restless mind. , 2006, Psychological bulletin.

[21]  Emily B. Myers,et al.  An event-related fMRI investigation of phonological-lexical competition , 2004, Brain and Language.

[22]  Thomas J. Grabowski,et al.  The Left Posterior Superior Temporal Gyrus Participates Specifically in Accessing Lexical Phonology , 2008, Journal of Cognitive Neuroscience.

[23]  B. Miller,et al.  The neural basis of surface dyslexia in semantic dementia. , 2009, Brain : a journal of neurology.

[24]  Harold Goodglass,et al.  Overt propositional speech in chronic nonfluent aphasia studied with the dynamic susceptibility contrast fMRI method , 2004, NeuroImage.

[25]  Michael J Cortese,et al.  Visual word recognition of single-syllable words. , 2004, Journal of experimental psychology. General.

[26]  Rebecca Saxe,et al.  Contributions of episodic retrieval and mentalizing to autobiographical thought: Evidence from functional neuroimaging, resting-state connectivity, and fMRI meta-analyses , 2014, NeuroImage.

[27]  J. A. Frost,et al.  Conceptual Processing during the Conscious Resting State: A Functional MRI Study , 1999, Journal of Cognitive Neuroscience.

[28]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[29]  Benjamin Naumann,et al.  Mental Representations A Dual Coding Approach , 2016 .

[30]  A. Woollams,et al.  Imageability and ambiguity effects in speeded naming: convergence and divergence. , 2005, Journal of experimental psychology. Learning, memory, and cognition.

[31]  C. Coelho,et al.  Semantic feature analysis as a treatment for aphasic dysnomia: A replication , 2000 .

[32]  Maria Luisa Gorno-Tempini,et al.  Distinct neural substrates for semantic knowledge and naming in the temporoparietal network. , 2012, Cerebral cortex.

[33]  Ana Inés Ansaldo,et al.  Therapy-induced neuroplasticity in chronic aphasia , 2012, Neuropsychologia.

[34]  T. Robbins,et al.  Inhibition and the right inferior frontal cortex: one decade on , 2014, Trends in Cognitive Sciences.

[35]  R. Hamilton,et al.  Patterns of neural activity predict picture-naming performance of a patient with chronic aphasia , 2017, Neuropsychologia.

[36]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Matthew H. Davis,et al.  Interpreting response time effects in functional imaging studies , 2014, NeuroImage.

[38]  A. Hillis Can shift to the right be a good thing? , 2005, Annals of neurology.

[39]  Hans Knutsson,et al.  Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates , 2016, Proceedings of the National Academy of Sciences.

[40]  R. C. Marshall,et al.  Using semantic feature analysis to improve contextual discourse in adults with aphasia. , 2008, American journal of speech-language pathology.

[41]  Cynthia K Thompson,et al.  The role of semantic complexity in treatment of naming deficits: training semantic categories in fluent aphasia by controlling exemplar typicality. , 2003, Journal of speech, language, and hearing research : JSLHR.

[42]  Michael S. Beauchamp,et al.  A new method for improving functional-to-structural MRI alignment using local Pearson correlation , 2009, NeuroImage.

[43]  Julius Fridriksson,et al.  Preservation and Modulation of Specific Left Hemisphere Regions is Vital for Treated Recovery from Anomia in Stroke , 2010, The Journal of Neuroscience.

[44]  Allen R. Braun,et al.  Single-trial fMRI Shows Contralesional Activity Linked to Overt Naming Errors in Chronic Aphasic Patients , 2010, Journal of Cognitive Neuroscience.

[45]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[46]  Russell A. Poldrack,et al.  Decomposing Decision Components in the Stop-signal Task: A Model-based Approach to Individual Differences in Inhibitory Control , 2014, Journal of Cognitive Neuroscience.

[47]  Roy H. Hamilton,et al.  The right hemisphere is not unitary in its role in aphasia recovery , 2012, Cortex.

[48]  M. Boyle Semantic feature analysis treatment for anomia in two fluent aphasia syndromes. , 2004, American journal of speech-language pathology.

[49]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[50]  Jacquie Kurland,et al.  Overt naming fMRI pre- and post-TMS: Two nonfluent aphasia patients, with and without improved naming post-TMS , 2007, Brain and Language.

[51]  H. Karbe,et al.  Differential capacity of left and right hemispheric areas for compensation of poststroke aphasia , 1999, Annals of neurology.

[52]  F. Pulvermüller,et al.  Hemispheric contributions to language reorganisation: An MEG study of neuroplasticity in chronic post stroke aphasia , 2016, Neuropsychologia.

[53]  Julius Fridriksson,et al.  Left hemisphere plasticity and aphasia recovery , 2012, NeuroImage.

[54]  Cynthia K. Thompson,et al.  Neuroimaging and recovery of language in aphasia , 2008, Current neurology and neuroscience reports.

[55]  Colin Humphries,et al.  Lesion localization of speech comprehension deficits in chronic aphasia , 2017, Neurology.

[56]  M. Rosenberg,et al.  In the zone or zoning out? Tracking behavioral and neural fluctuations during sustained attention. , 2013, Cerebral cortex.

[57]  Keith D. White,et al.  Functional MRI of Language in Aphasia: A Review of the Literature and the Methodological Challenges , 2007, Neuropsychology Review.

[58]  Kristina M. Visscher,et al.  The neural bases of momentary lapses in attention , 2006, Nature Neuroscience.

[59]  Jonas Obleser,et al.  Brain regions essential for improved lexical access in an aged aphasic patient: a case report , 2006, BMC neurology.

[60]  John Duncan,et al.  The role of the right inferior frontal gyrus: inhibition and attentional control , 2010, NeuroImage.

[61]  R. Nathan Spreng,et al.  Patterns of Brain Activity Supporting Autobiographical Memory, Prospection, and Theory of Mind, and Their Relationship to the Default Mode Network , 2010, Journal of Cognitive Neuroscience.

[62]  G. Gainotti Contrasting opinions on the role of the right hemisphere in the recovery of language. A critical survey , 2015 .

[63]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[64]  J. Andrews-Hanna,et al.  The brain's default network: Anatomy, function, and consequence of disruption , 2009 .

[65]  Richard J. S. Wise,et al.  Task-induced brain activity in aphasic stroke patients: what is driving recovery? , 2014, Brain : a journal of neurology.

[66]  Jean K. Gordon,et al.  A Neural Signature of Phonological Access: Distinguishing the Effects of Word Frequency from Familiarity and Length in Overt Picture Naming , 2007, Journal of Cognitive Neuroscience.

[67]  William W. Graves,et al.  Neural Systems for Reading Aloud: A Multiparametric Approach , 2009, Cerebral cortex.

[68]  Jeffrey R. Binder,et al.  Interrupting the “stream of consciousness”: An fMRI investigation , 2006, NeuroImage.

[69]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[70]  Colin Humphries,et al.  Cerebral localization of impaired phonological retrieval during rhyme judgment , 2014, Annals of neurology.

[71]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[72]  David A. Medler,et al.  Distinct Brain Systems for Processing Concrete and Abstract Concepts , 2005, Journal of Cognitive Neuroscience.

[73]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[74]  Paul A. Taylor,et al.  FMRI Clustering in AFNI: False-Positive Rates Redux , 2017, Brain Connect..