Superior temporal gyrus thickness correlates with cognitive performance in multiple sclerosis

Decreased cortical thickness that signifies gray matter pathology and its impact on cognitive performance is a research field with growing interest in relapsing–remitting multiple sclerosis (RRMS) and needs to be further elucidated. Using high-field 3.0 T MRI, three-dimensional T1-FSPGR (voxel size 1 × 1 × 1 mm) cortical thickness was measured in 82 regions in the left hemisphere (LH) and right hemisphere (RH) in 20 RRMS patients with low disease activity and in 20 age-matched healthy subjects that in parallel underwent comprehensive cognitive evaluation. The correlation between local cortical atrophy and cognitive performance was examined. We identified seven regions with cortical tissue loss that differed between RRMS and age-matched healthy controls. These regions were mainly located in the frontal and temporal lobes, specifically within the gyrus rectus, inferior frontal sulcus, orbital gyrus, parahippocampal gyrus, and superior temporal gyrus, with preferential left asymmetry. Increased cortical thickness was identified in two visual sensory regions, the LH inferior occipital gyrus, and the RH cuneus, implicating adaptive plasticity. Correlation analysis demonstrated that only the LH superior temporal gyrus thickness was associated with cognitive performance and its thickness correlated with motor skills (r = 0.65, p = 0.003), attention (r = 0.45, p = 0.042), and information processing speed (r = 0.50, p = 0.025). Our findings show that restricted cortical thinning occurs in RRMS patients with mild disease and that LH superior temporal gyrus atrophy is associated with cognitive dysfunction.

[1]  L Bozzao,et al.  SPECT, MRI and cognitive functions in multiple sclerosis. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[2]  F. Fazio,et al.  Relationship between corpus callosum atrophy and cerebral metabolic asymmetries in multiple sclerosis , 1992, Journal of the Neurological Sciences.

[3]  B. Stankoff,et al.  Induction of myelination in the central nervous system by electrical activity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Maguire,et al.  Differential modulation of a common memory retrieval network revealed by positron emission tomography , 1999, Hippocampus.

[5]  J. Decety,et al.  A PET Investigation of the Attribution of Intentions with a Nonverbal Task , 2000, NeuroImage.

[6]  J K Udupa,et al.  Magnetization transfer ratio histogram analysis of gray matter in relapsing-remitting multiple sclerosis. , 2001, AJNR. American journal of neuroradiology.

[7]  L. Krupp,et al.  Cognitive Dysfunction Lateralizes With NAA in Multiple Sclerosis , 2001, Applied neuropsychology.

[8]  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.

[9]  Massimo Filippi,et al.  Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. , 2002, AJNR. American journal of neuroradiology.

[10]  Ivanei E. Bramati,et al.  The Neural Correlates of Moral Sensitivity: A Functional Magnetic Resonance Imaging Investigation of Basic and Moral Emotions , 2002, The Journal of Neuroscience.

[11]  A. Achiron,et al.  Brain MRI lesion load quantification in multiple sclerosis: a comparison between automated multispectral and semi-automated thresholding computer-assisted techniques. , 2002, Magnetic resonance imaging.

[12]  B. J. Anderson,et al.  Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. , 2002, Learning & memory.

[13]  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.

[14]  A. Dale,et al.  Focal thinning of the cerebral cortex in multiple sclerosis. , 2003, Brain : a journal of neurology.

[15]  N. Uzunoglu,et al.  Working memory deficits in multiple sclerosis: a controlled study with auditory P600 correlates , 2003, Journal of neurology, neurosurgery, and psychiatry.

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

[17]  Massimo Filippi,et al.  Indirect evidence for early widespread gray matter involvement in relapsing–remitting multiple sclerosis , 2004, NeuroImage.

[18]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.

[19]  N. De Stefano,et al.  Neocortical volume decrease in relapsing–remitting MS patients with mild cognitive impairment , 2004, Neurology.

[20]  A J Thompson,et al.  Progressive grey matter atrophy in clinically early relapsing-remitting multiple sclerosis , 2003, Multiple sclerosis.

[21]  Roberto Mutani,et al.  Grey Matter Pathology in Multiple Sclerosis , 2005, Journal of neuropathology and experimental neurology.

[22]  A J Thompson,et al.  Gray and white matter volume changes in early RRMS , 2005, Neurology.

[23]  Rick M Dijkhuizen,et al.  Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. , 2006, Brain : a journal of neurology.

[24]  Alan C. Evans,et al.  A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom , 2006, NeuroImage.

[25]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[26]  Dieter Vaitl,et al.  Evidence for a direct association between cortical atrophy and cognitive impairment in relapsing–remitting MS , 2006, NeuroImage.

[27]  Chiara Romualdi,et al.  Cortical atrophy is relevant in multiple sclerosis at clinical onset , 2007, Journal of Neurology.

[28]  Bruno Alfano,et al.  Grey matter loss in relapsing–remitting multiple sclerosis: A voxel-based morphometry study , 2006, NeuroImage.

[29]  H. Haidar,et al.  Measurement of Cortical Thickness in 3D Brain MRI Data: Validation of the Laplacian Method , 2006, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[30]  Marco Battaglini,et al.  Association of neocortical volume changes with cognitive deterioration in relapsing-remitting multiple sclerosis. , 2007, Archives of neurology.

[31]  G. Doniger,et al.  Prolonged response times characterize cognitive performance in multiple sclerosis , 2007, European journal of neurology.

[32]  Rohit Bakshi,et al.  Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis , 2007, NeuroImage.

[33]  J. Price Definition of the Orbital Cortex in Relation to Specific Connections with Limbic and Visceral Structures and Other Cortical Regions , 2007, Annals of the New York Academy of Sciences.

[34]  Rainer Goebel,et al.  Thinner prefrontal cortex in veterans with posttraumatic stress disorder , 2008, NeuroImage.

[35]  Frederik Barkhof,et al.  Grey matter pathology in multiple sclerosis , 2008, The Lancet Neurology.

[36]  J. Kurtzke,et al.  Historical and Clinical Perspectives of the Expanded Disability Status Scale , 2008, Neuroepidemiology.

[37]  B. Pakkenberg,et al.  Neocortical glial cell numbers in human brains , 2008, Neurobiology of Aging.

[38]  A. Minagar,et al.  Evidence for gray matter pathology in multiple sclerosis: A neuroimaging approach , 2009, Journal of the Neurological Sciences.

[39]  R. Rudick,et al.  Gray-matter injury in multiple sclerosis. , 2009, New England Journal of Medicine.

[40]  Andra M. Smith,et al.  fMRI investigation of disinhibition in cognitively impaired patients with multiple sclerosis , 2009, Journal of Neurological Sciences.

[41]  M. Calabrese,et al.  Widespread cortical thinning characterizes patients with MS with mild cognitive impairment , 2010, Neurology.