Cortical reorganization during PASAT task in MS patients with preserved working memory functions

Cortical reorganization in multiple sclerosis (MS) is defined as a compensatory mechanism which requires MS patients to overactivate specific brain areas in order to perform the task as controls. To investigate this process with the Paced Auditory Serial Addition Test (PASAT) task, we selected 15 MS patients who performed the PASAT task within-normal limits and 10 healthy controls. Once selected, we used functional magnetic resonance imaging (fMRI) to investigate brain areas involved in PASAT performance in both groups. Results showed that the task activated the left frontal (BA6 and 9) and parietal cortex (BA7 and 40) in both groups, but MS patients showed a stronger activation in the left prefrontal cortex (BA9, 44 and 45) when compared with controls. These results confirmed those obtained post hoc by Audoin et al. [Audoin, B., Ibarrola, D., Ranjeva, J.P., Confort-Gouny, S., Malikova, I., Ali-Chérif, A.M., Pelletier, J., Cozzone, P., et al., 2003. Compensatory cortical activation observed by fMRI during cognitive task at the earliest stage of MS. Hum. Brain Mapp. 20, 51-58], and we interpreted this as showing true cortical reorganization.

[1]  Charles W. Mathias,et al.  Paced Visual Serial Addition Test: An Alternative Measure of Information Processing Speed , 2000 .

[2]  R. Bakshi,et al.  Frontal cortex atrophy predicts cognitive impairment in multiple sclerosis. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[3]  R W Cox,et al.  Magnetic field changes in the human brain due to swallowing or speaking , 1998, Magnetic resonance in medicine.

[4]  My-Van Au Duong,et al.  Altered Functional Connectivity Related to White Matter Changes inside the Working Memory Network at the Very Early Stage of MS , 2005, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[5]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[6]  Bertrand Audoin,et al.  Magnetic resonance study of the influence of tissue damage and cortical reorganization on PASAT performance at the earliest stage of multiple sclerosis , 2005, Human brain mapping.

[7]  D. Goodkin,et al.  Clinical and demographic predictors of cognitive performance in multiple sclerosis. Do diagnostic type, disease duration, and disability matter? , 1990, Archives of neurology.

[8]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[9]  Rohit Bakshi,et al.  Regional lobar atrophy predicts memory impairment in multiple sclerosis. , 2005, AJNR. American journal of neuroradiology.

[10]  R I Grossman,et al.  MR lesion load and cognitive function in patients with relapsing-remitting multiple sclerosis. , 1999, AJNR. American journal of neuroradiology.

[11]  J. Grafman,et al.  Plasticity and Rehabilitation , 2003 .

[12]  J. Kurtzke.  Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[13]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[14]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[15]  E Zarahn,et al.  Replication and further studies of neural mechanisms of spatial mnemonic processing in humans. , 2000, Brain research. Cognitive brain research.

[16]  D. Ibarrola,et al.  Functional MRI study of PASAT in normal subjects , 2005, Magnetic Resonance Materials in Physics, Biology and Medicine.

[17]  L A Fos,et al.  Paced Visual Serial Addition Test: An Alternative Measure of Information Processing Speed , 1999, Applied neuropsychology.

[18]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

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

[20]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[21]  P M Matthews,et al.  The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis , 2000, Annals of neurology.

[22]  S. Golaszewski,et al.  Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. , 2002, Brain : a journal of neurology.

[23]  P M Matthews,et al.  Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. , 2000, Brain : a journal of neurology.

[24]  A. Thompson,et al.  Cognitive function in primary progressive and transitional progressive multiple sclerosis: a controlled study with MRI correlates. , 1999, Brain : a journal of neurology.

[25]  Giuseppe Scotti,et al.  Functional cortical changes in patients with multiple sclerosis and nonspecific findings on conventional magnetic resonance imaging scans of the brain , 2003, NeuroImage.

[26]  D. Silberberg,et al.  New diagnostic criteria for multiple sclerosis: Guidelines for research protocols , 1983, Annals of neurology.

[27]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

[28]  Stephen M. Rao,et al.  Cognitive dysfunction in multiple sclerosis. , 1991, Neurology.

[29]  Caterina Mainero,et al.  fMRI evidence of brain reorganization during attention and memory tasks in multiple sclerosis , 2004, NeuroImage.

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

[31]  Guy Nagels,et al.  Paced visual serial addition test in multiple sclerosis , 2004, Clinical Neurology and Neurosurgery.

[32]  B M Bly,et al.  An Investigation of Working Memory Rehearsal in Multiple Sclerosis Using fMRI , 2003, Journal of clinical and experimental neuropsychology.

[33]  B. Postle,et al.  Functional neuroanatomical double dissociation of mnemonic and executive control processes contributing to working memory performance. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. D’Esposito,et al.  The Influence of Working-Memory Demand and Subject Performance on Prefrontal Cortical Activity , 2002, Journal of Cognitive Neuroscience.

[35]  M. Rausch,et al.  Analysis of Impairment Related Functional Architecture in MS Patients during Performance of Different Attention Tasks , 2003, Journal of Neurology.

[36]  A. Saykin,et al.  Brain activation patterns associated with working memory in relapsing-remitting MS , 2004, Neurology.

[37]  V. Haughton,et al.  Correlation of magnetic resonance imaging with neuropsychological testing in multiple sclerosis , 1989, Neurology.

[38]  J. Grafman,et al.  Relationship between frontal lobe lesions and Wisconsin Card Sorting Test performance in patients with multiple sclerosis , 1994, Neurology.

[39]  F Barkhof,et al.  MS Functional Composite , 2000, Neurology.

[40]  María Jesús Benedet,et al.  TAVEC: test de aprendizaje verbal España-Complutense : manual , 1998 .

[41]  Bertrand Audoin,et al.  Compensatory cortical activation observed by fMRI during a cognitive task at the earliest stage of multiple sclerosis , 2003, Human brain mapping.

[42]  G I de Zubicaray,et al.  The semantic interference effect in the picture‐word paradigm: An event‐related fMRI study employing overt responses , 2001, Human brain mapping.

[43]  G. McCarthy,et al.  The Influence of Memory Load Upon Delay-Interval Activity in a Working-Memory Task: An Event-Related Functional MRI Study , 2000, Journal of Cognitive Neuroscience.

[44]  J. Patton,et al.  Extended norms for the paced auditory serial addition task , 1991 .