Working memory representation in atypical language dominance

One of the most important factors controlling material specific processing in the human brain is language dominance, i.e. hemispheric specialization in semantic processes. Although previous studies have shown that lateralized long‐term memory processes in the medial temporal lobes are modified in subjects with atypical (right) language dominance, the effect of language dominance on the neural basis of working memory (WM) has remained unknown. Here, we used functional MRI (fMRI) to study the impact of language dominance on the neural representation of WM. We conducted an n‐back task in three different load conditions and with both verbal and nonverbal (spatial) material in matched groups of left and right language dominant subjects. This approach allowed us to investigate regions showing significant interactions between language dominance and material. Overall, right dominant subjects showed an increased inter‐individual variability of WM‐related activations. Verbal WM involved more pronounced activation of the left fusiform cortex in left dominant subjects and of the right inferior parietal lobule in the right dominant group. Spatial WM, on the other hand, induced activation of right hemispheric regions in left dominant subjects, but no specific activations in right dominant subjects. Taken together, these findings indicate that the neural basis of verbal WM processes depends on language dominance and is more mutable in right dominant subjects. The increased variability in right dominant subjects strongly suggests that a standard network of material‐dependent WM processes exists in left dominant subjects, and that right dominant subjects use variable alternative networks. Hum Brain Mapp, 2009. © 2008 Wiley‐Liss, Inc.

[1]  J. A. Frost,et al.  Determination of language dominance using functional MRI: A comparison with the Wada test , 2011, Neurology.

[2]  E. Smith,et al.  Neuroimaging studies of working memory: A meta-analysis , 2010 .

[3]  J. Binder,et al.  A comparison of five fMRI protocols for mapping speech comprehension systems , 2008, Epilepsia.

[4]  E. T. Possing,et al.  Functional MRI and Wada studies in patients with interhemispheric dissociation of language functions , 2008, Epilepsy & Behavior.

[5]  Bernd Weber,et al.  Strongly lateralized activation in language fMRI of atypical dominant patients—Implications for presurgical work-up , 2008, Epilepsy Research.

[6]  Yaakov Stern,et al.  A common neural network for cognitive reserve in verbal and object working memory in young but not old. , 2008, Cerebral cortex.

[7]  Rene Vohn,et al.  The subcortical role of language processing. High level linguistic features such as ambiguity-resolution and the human brain; an fMRI study , 2008, NeuroImage.

[8]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[9]  A. Kersting,et al.  Functional anatomy of visuo-spatial working memory during mental rotation is influenced by sex, menstrual cycle, and sex steroid hormones , 2007, Neuropsychologia.

[10]  Klaus Fliessbach,et al.  Material-specific memory processing is related to language dominance , 2007, NeuroImage.

[11]  Henrik Walter,et al.  Working memory dysfunction in schizophrenia compared to healthy controls and patients with depression: Evidence from event-related fMRI , 2007, NeuroImage.

[12]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[13]  T. Goldberg,et al.  Dissociating the effects of Sternberg working memory demands in prefrontal cortex , 2007, Psychiatry Research: Neuroimaging.

[14]  Yang Dan,et al.  Experience-Dependent Plasticity in Adult Visual Cortex , 2006, Neuron.

[15]  Jeffrey R. Binder,et al.  Tuning of the human left fusiform gyrus to sublexical orthographic structure , 2006, NeuroImage.

[16]  N. Kanwisher,et al.  Domain specificity in visual cortex. , 2006, Cerebral cortex.

[17]  Eugen Trinka,et al.  Language Lateralization in Temporal Lobe Epilepsy: A Comparison between fMRI and the Wada Test , 2006, Epilepsia.

[18]  Leila Reddy,et al.  Coding of visual objects in the ventral stream , 2006, Current Opinion in Neurobiology.

[19]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

[20]  R. Knight,et al.  The functional neuroanatomy of working memory: Contributions of human brain lesion studies , 2006, Neuroscience.

[21]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[22]  Bradley R. Postle,et al.  Distraction-spanning sustained activity during delayed recognition of locations , 2006, NeuroImage.

[23]  Colin Humphries,et al.  Syntactic and Semantic Modulation of Neural Activity during Auditory Sentence Comprehension , 2006, Journal of Cognitive Neuroscience.

[24]  Evan Fletcher,et al.  White Matter Changes Compromise Prefrontal Cortex Function in Healthy Elderly Individuals , 2006, Journal of Cognitive Neuroscience.

[25]  Guillén Fernández,et al.  Left hippocampal pathology is associated with atypical language lateralization in patients with focal epilepsy. , 2006, Brain : a journal of neurology.

[26]  J. M. Watson,et al.  Evaluating functional MRI procedures for assessing hemispheric language dominance in neurosurgical patients , 2005, Neuroradiology.

[27]  Christian Büchel,et al.  The functional and temporal characteristics of top-down modulation in visual selection. , 2005, Cerebral cortex.

[28]  Richard Levy,et al.  Cognitive control and brain resources in major depression: An fMRI study using the n-back task , 2005, NeuroImage.

[29]  A. Jansen,et al.  Crossed cerebro–cerebellar language dominance , 2005, Human brain mapping.

[30]  John D E Gabrieli,et al.  The role of the prefrontal cortex in the maintenance of verbal working memory: an event-related FMRI analysis. , 2005, Neuropsychology.

[31]  T. Pasternak,et al.  Working memory in primate sensory systems , 2005, Nature Reviews Neuroscience.

[32]  Bertrand Audoin,et al.  Modulation of effective connectivity inside the working memory network in patients at the earliest stage of multiple sclerosis , 2005, NeuroImage.

[33]  Asaid Khateb,et al.  Variability of fMRI activation during a phonological and semantic language task in healthy subjects , 2004, Human brain mapping.

[34]  J Jonides,et al.  The where and how of attention-based rehearsal in spatial working memory. , 2004, Brain research. Cognitive brain research.

[35]  M. D’Esposito,et al.  Category-specific modulation of inferior temporal activity during working memory encoding and maintenance. , 2004, Brain research. Cognitive brain research.

[36]  Julie A Fiez,et al.  Functional dissociations within the inferior parietal cortex in verbal working memory , 2004, NeuroImage.

[37]  F Crivello,et al.  Interindividual variability in the hemispheric organization for speech , 2004, NeuroImage.

[38]  Sterling C. Johnson,et al.  Functional MRI and Wada Determination of Language Lateralization: A Case of Crossed Dominance , 2004, Epilepsia.

[39]  Rainer Goebel,et al.  Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network , 2003, NeuroImage.

[40]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[41]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[42]  G. J. M. Rutten,et al.  fMRI-Determined Language Lateralization in Patients with Unilateral or Mixed Language Dominance According to the Wada Test , 2002, NeuroImage.

[43]  R. Malach,et al.  The topography of high-order human object areas , 2002, Trends in Cognitive Sciences.

[44]  Guillén Fernández,et al.  Language Mapping in Less Than 15 Minutes: Real-Time Functional MRI during Routine Clinical Investigation , 2001, NeuroImage.

[45]  N. F. Ramsey,et al.  Combined Analysis of Language Tasks in fMRI Improves Assessment of Hemispheric Dominance for Language Functions in Individual Subjects , 2001, NeuroImage.

[46]  R. Coppola,et al.  Specific versus Nonspecific Brain Activity in a Parametric N-Back Task , 2000, NeuroImage.

[47]  E. Ringelstein,et al.  Handedness and hemispheric language dominance in healthy humans. , 2000, Brain : a journal of neurology.

[48]  D Y von Cramon,et al.  What have Klingon letters and faces in common? An fMRI study on content‐specific working memory systems , 2000, Human brain mapping.

[49]  D Le Bihan,et al.  Functional MR evaluation of temporal and frontal language dominance compared with the Wada test , 2000, Neurology.

[50]  M Deppe,et al.  Assessment of Hemispheric Language Lateralization: A Comparison between fMRI and fTCD , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[51]  J. Gore,et al.  An Event-Related fMRI Study of Implicit Phrase-Level Syntactic and Semantic Processing , 1999, NeuroImage.

[52]  Edward E. Smith,et al.  Rehearsal in Spatial Working Memory: Evidence From Neuroimaging , 1999 .

[53]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[54]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[55]  J. Desmond,et al.  Load-Dependent Roles of Frontal Brain Regions in the Maintenance of Working Memory , 1999, NeuroImage.

[56]  K. Kiehl,et al.  Neural pathways involved in the processing of concrete and abstract words , 1999, Human brain mapping.

[57]  Edward E. Smith,et al.  The Role of Parietal Cortex in Verbal Working Memory , 1998, The Journal of Neuroscience.

[58]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[59]  M Deppe,et al.  Noninvasive determination of language lateralization by functional transcranial Doppler sonography: a comparison with the Wada test. , 1998, Stroke.

[60]  C. E. Elger,et al.  Patterns of Language Dominance in Focal Left and Right Hemisphere Epilepsies: Relation to MRI Findings, EEG, Sex, and Age at Onset of Epilepsy , 1997, Brain and Cognition.

[61]  Edward E. Smith,et al.  A Parametric Study of Prefrontal Cortex Involvement in Human Working Memory , 1996, NeuroImage.

[62]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[63]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[64]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[65]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

[66]  T. Allison,et al.  Human extrastriate visual cortex and the perception of faces, words, numbers, and colors. , 1994, Cerebral cortex.

[67]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[68]  P. Grobstein Analysis of Visual Behavior, David J. Ingle, Melvyn A. Goodale, Richard J.W. Mansfield (Eds.). MIT press, Cambridge, MA and London (1982), 834 , 1983 .

[69]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[70]  Jason W. Brown,et al.  Lateralization and language representation , 1976, Neurology.