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Erschienen in: Brain Structure and Function 4/2013

01.07.2013 | Original Article

Superior temporal gyrus thickness correlates with cognitive performance in multiple sclerosis

verfasst von: Asaf Achiron, Joab Chapman, Sigal Tal, Eran Bercovich, Hararai Gil, Anat Achiron

Erschienen in: Brain Structure and Function | Ausgabe 4/2013

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Abstract

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.
Literatur
Zurück zum Zitat Achiron A, Gicquel S, Miron S, Faibel M (2002) Brain MRI lesion load quantification in multiple sclerosis: a comparison between automated multispectral and semi-automated thresholding computer-assisted techniques. Magn Reson Imaging 20:713–720PubMedCrossRef Achiron A, Gicquel S, Miron S, Faibel M (2002) Brain MRI lesion load quantification in multiple sclerosis: a comparison between automated multispectral and semi-automated thresholding computer-assisted techniques. Magn Reson Imaging 20:713–720PubMedCrossRef
Zurück zum Zitat Achiron A, Doniger GM, Harel Y, Appleboim-Gavish N, Lavie M, Simon ES (2007) Prolonged response times characterize cognitive performance in multiple sclerosis. Eur J Neurol 14:1102–1108PubMedCrossRef Achiron A, Doniger GM, Harel Y, Appleboim-Gavish N, Lavie M, Simon ES (2007) Prolonged response times characterize cognitive performance in multiple sclerosis. Eur J Neurol 14:1102–1108PubMedCrossRef
Zurück zum Zitat Amato MP, Bartolozzi ML, Zipoli V, Portaccio E, Mortilla M, Guidi L, Siracusa G, Sorbi S, Federico A, De Stefano N (2004) Neocortical volume decrease in relapsing–remitting MS patients with mild cognitive impairment. Neurology 63:89–93PubMedCrossRef Amato MP, Bartolozzi ML, Zipoli V, Portaccio E, Mortilla M, Guidi L, Siracusa G, Sorbi S, Federico A, De Stefano N (2004) Neocortical volume decrease in relapsing–remitting MS patients with mild cognitive impairment. Neurology 63:89–93PubMedCrossRef
Zurück zum Zitat Amato MP, Portaccio E, Goretti B, Zipoli V, Battaglini M, Bartolozzi ML, Stromillo ML, Guidi L, Siracusa G, Sorbi S, Federico A, De Stefano N (2007) Association of neocortical volume changes with cognitive deterioration in relapsing–remitting multiple sclerosis. Arch Neurol 64:1157–1161PubMedCrossRef Amato MP, Portaccio E, Goretti B, Zipoli V, Battaglini M, Bartolozzi ML, Stromillo ML, Guidi L, Siracusa G, Sorbi S, Federico A, De Stefano N (2007) Association of neocortical volume changes with cognitive deterioration in relapsing–remitting multiple sclerosis. Arch Neurol 64:1157–1161PubMedCrossRef
Zurück zum Zitat Anderson BJ, Eckburg PB, Relucio KI (2002) Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn Mem 9:1–9PubMedCrossRef Anderson BJ, Eckburg PB, Relucio KI (2002) Alterations in the thickness of motor cortical subregions after motor-skill learning and exercise. Learn Mem 9:1–9PubMedCrossRef
Zurück zum Zitat Audoin B, Ibarrola D (2005) Functional MRI study of PASAT in normal subjects. MAGMA 18:96–102PubMedCrossRef Audoin B, Ibarrola D (2005) Functional MRI study of PASAT in normal subjects. MAGMA 18:96–102PubMedCrossRef
Zurück zum Zitat Bozzali M, Cercignani M, Sormani MP, Comi G, Filippi M (2002) Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. AJNR Am J Neuroradiol 23:985–988PubMed Bozzali M, Cercignani M, Sormani MP, Comi G, Filippi M (2002) Quantification of brain gray matter damage in different MS phenotypes by use of diffusion tensor MR imaging. AJNR Am J Neuroradiol 23:985–988PubMed
Zurück zum Zitat Brunet E, Sarfati Y, Hardy-Bayle MC, Decety J (2000) A PET investigation of the attribution of intentions with a nonverbal task. Neuroimage 11:157–166PubMedCrossRef Brunet E, Sarfati Y, Hardy-Bayle MC, Decety J (2000) A PET investigation of the attribution of intentions with a nonverbal task. Neuroimage 11:157–166PubMedCrossRef
Zurück zum Zitat Calabrese M, Atzori M, Bernardi V, Morra A, Romualdi C, Rinaldi L, McAuliffe MJ, Barachino L, Perini P, Fischl B, Battistin L, Gallo P (2007) Cortical atrophy is relevant in multiple sclerosis at clinical onset. J Neurol 254:1212–1220PubMedCrossRef Calabrese M, Atzori M, Bernardi V, Morra A, Romualdi C, Rinaldi L, McAuliffe MJ, Barachino L, Perini P, Fischl B, Battistin L, Gallo P (2007) Cortical atrophy is relevant in multiple sclerosis at clinical onset. J Neurol 254:1212–1220PubMedCrossRef
Zurück zum Zitat Calabrese M, Rinaldi F, Mattisi I, Grossi P, Favaretto A, Atzori M, Bernardi V, Barachino L, Romualdi C, Rinaldi L, Perini P, Gallo P (2010) Widespread cortical thinning characterizes patients with MS with mild cognitive impairment. Neurology 7:321–328CrossRef Calabrese M, Rinaldi F, Mattisi I, Grossi P, Favaretto A, Atzori M, Bernardi V, Barachino L, Romualdi C, Rinaldi L, Perini P, Gallo P (2010) Widespread cortical thinning characterizes patients with MS with mild cognitive impairment. Neurology 7:321–328CrossRef
Zurück zum Zitat Chard DT, Griffin CM, Rashid W, Davies GR, Altmann DR, Kapoor R, Barker GJ, Thompson AJ, Miller DH (2004) Progressive grey matter atrophy in clinically early relapsing–remitting multiple sclerosis. Mult Scler 10:387–391PubMedCrossRef Chard DT, Griffin CM, Rashid W, Davies GR, Altmann DR, Kapoor R, Barker GJ, Thompson AJ, Miller DH (2004) Progressive grey matter atrophy in clinically early relapsing–remitting multiple sclerosis. Mult Scler 10:387–391PubMedCrossRef
Zurück zum Zitat Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F, Zalc B, Lubetzki C (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 93:9887–9892PubMedCrossRef Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F, Zalc B, Lubetzki C (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 93:9887–9892PubMedCrossRef
Zurück zum Zitat Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A (2004) Neuroplasticity: changes in grey matter induced by training. Nature 427:311–312PubMedCrossRef Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A (2004) Neuroplasticity: changes in grey matter induced by training. Nature 427:311–312PubMedCrossRef
Zurück zum Zitat Ge Y, Grossman RI, Udupa JK, Babb JS, Kolson DL, McGowan JC (2001) Magnetization transfer ratio histogram analysis of gray matter in relapsing–remitting multiple sclerosis. AJNR Am J Neuroradiol 22:470–475PubMed Ge Y, Grossman RI, Udupa JK, Babb JS, Kolson DL, McGowan JC (2001) Magnetization transfer ratio histogram analysis of gray matter in relapsing–remitting multiple sclerosis. AJNR Am J Neuroradiol 22:470–475PubMed
Zurück zum Zitat Geurts JJ, Barkhof F (2008) Grey matter pathology in multiple sclerosis. Lancet Neurol 7:841–851PubMedCrossRef Geurts JJ, Barkhof F (2008) Grey matter pathology in multiple sclerosis. Lancet Neurol 7:841–851PubMedCrossRef
Zurück zum Zitat Geuze E, Westenberg HG, Heinecke A, de Kloet CS, Goebel R, Vermetten E (2008) Thinner prefrontal cortex in veterans with posttraumatic stress disorder. Neuroimage 41:675–681PubMedCrossRef Geuze E, Westenberg HG, Heinecke A, de Kloet CS, Goebel R, Vermetten E (2008) Thinner prefrontal cortex in veterans with posttraumatic stress disorder. Neuroimage 41:675–681PubMedCrossRef
Zurück zum Zitat Goldberg II, Harel M, Malach R (2006) When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 50:329–339PubMedCrossRef Goldberg II, Harel M, Malach R (2006) When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 50:329–339PubMedCrossRef
Zurück zum Zitat Haidar H, Soul JS (2006) Measurement of cortical thickness in 3D brain MRI data: validation of the Laplacian method. J Neuroimaging 16:146–153PubMedCrossRef Haidar H, Soul JS (2006) Measurement of cortical thickness in 3D brain MRI data: validation of the Laplacian method. J Neuroimaging 16:146–153PubMedCrossRef
Zurück zum Zitat Inglese M, Ge Y, Filippi M, Falini A, Grossman RI, Gonen O (2004) Indirect evidence for early widespread gray matter involvement in relapsing–remitting multiple sclerosis. Neuroimage 21:1825–1829PubMedCrossRef Inglese M, Ge Y, Filippi M, Falini A, Grossman RI, Gonen O (2004) Indirect evidence for early widespread gray matter involvement in relapsing–remitting multiple sclerosis. Neuroimage 21:1825–1829PubMedCrossRef
Zurück zum Zitat Kurtzke JF (2008) Historical and clinical perspectives of the expanded disability status scale. Neuroepidemiology 31:1–9PubMedCrossRef Kurtzke JF (2008) Historical and clinical perspectives of the expanded disability status scale. Neuroepidemiology 31:1–9PubMedCrossRef
Zurück zum Zitat Lee JK, Lee JM, Kim JS, Kim IY, Evans AC, Kim SI (2006) A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom. Neuroimage 31:572–584PubMedCrossRef Lee JK, Lee JM, Kim JS, Kim IY, Evans AC, Kim SI (2006) A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom. Neuroimage 31:572–584PubMedCrossRef
Zurück zum Zitat Maguire EA, Mummery CJ (1999) Differential modulation of a common memory retrieval network revealed by positron emission tomography. Hippocampus 9:54–61PubMedCrossRef Maguire EA, Mummery CJ (1999) Differential modulation of a common memory retrieval network revealed by positron emission tomography. Hippocampus 9:54–61PubMedCrossRef
Zurück zum Zitat Moll J, de Oliveira-Souza R, Eslinger PJ, Bramati IE, Mourão-Miranda J, Andreiuolo PA, Pessoa L (2002) The neural correlates of moral sensitivity: a functional magnetic resonance imaging investigation of basic and moral emotions. J Neurosci 22:2730–2736PubMed Moll J, de Oliveira-Souza R, Eslinger PJ, Bramati IE, Mourão-Miranda J, Andreiuolo PA, Pessoa L (2002) The neural correlates of moral sensitivity: a functional magnetic resonance imaging investigation of basic and moral emotions. J Neurosci 22:2730–2736PubMed
Zurück zum Zitat Morgen K, Sammer G, Courtney SM, Wolters T, Melchior H, Blecker CR, Oschmann P, Kaps M, Vaitl D (2006) Evidence for a direct association between cortical atrophy and cognitive impairment in relapsing–remitting MS. Neuroimage 30:891–898PubMedCrossRef Morgen K, Sammer G, Courtney SM, Wolters T, Melchior H, Blecker CR, Oschmann P, Kaps M, Vaitl D (2006) Evidence for a direct association between cortical atrophy and cognitive impairment in relapsing–remitting MS. Neuroimage 30:891–898PubMedCrossRef
Zurück zum Zitat Pan JW, Krupp LB, Elkins LE, Coyle PK (2001) Cognitive dysfunction lateralizes with NAA in multiple sclerosis. Appl Neuropsychol 8:155–160PubMedCrossRef Pan JW, Krupp LB, Elkins LE, Coyle PK (2001) Cognitive dysfunction lateralizes with NAA in multiple sclerosis. Appl Neuropsychol 8:155–160PubMedCrossRef
Zurück zum Zitat Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B (2008) Neocortical glial cell numbers in human brains. Neurobiol Aging 29:1754–1762PubMedCrossRef Pelvig DP, Pakkenberg H, Stark AK, Pakkenberg B (2008) Neocortical glial cell numbers in human brains. Neurobiol Aging 29:1754–1762PubMedCrossRef
Zurück zum Zitat Pozzilli C, Passafiume D, Bernardi S, Pantano P, Incoccia C, Bastianello S, Bozzao L, Lenzi GL, Fieschi C (1991) SPECT, MRI and cognitive functions in multiple sclerosis. J Neurol Neurosurg Psychiatry 54:110–115PubMedCrossRef Pozzilli C, Passafiume D, Bernardi S, Pantano P, Incoccia C, Bastianello S, Bozzao L, Lenzi GL, Fieschi C (1991) SPECT, MRI and cognitive functions in multiple sclerosis. J Neurol Neurosurg Psychiatry 54:110–115PubMedCrossRef
Zurück zum Zitat Pozzilli C, Fieschi C, Perani D, Paulesu E, Comi G, Bastianello S, Bernardi S, Bettinardi V, Bozzao L, Canal N (1992) Relationship between corpus callosum atrophy and cerebral metabolic asymmetries in multiple sclerosis. J Neurol Sci 112:51–57PubMedCrossRef Pozzilli C, Fieschi C, Perani D, Paulesu E, Comi G, Bastianello S, Bernardi S, Bettinardi V, Bozzao L, Canal N (1992) Relationship between corpus callosum atrophy and cerebral metabolic asymmetries in multiple sclerosis. J Neurol Sci 112:51–57PubMedCrossRef
Zurück zum Zitat Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54–71PubMedCrossRef Price JL (2007) Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann N Y Acad Sci 1121:54–71PubMedCrossRef
Zurück zum Zitat Prinster A, Quarantelli M, Orefice G, Lanzillo R, Brunetti A, Mollica C, Salvatore E, Morra VB, Coppola G, Vacca G, Alfano B, Salvatore M (2006) Grey matter loss in relapsing–remitting multiple sclerosis: a voxel-based morphometry study. Neuroimage 29:859–867PubMedCrossRef Prinster A, Quarantelli M, Orefice G, Lanzillo R, Brunetti A, Mollica C, Salvatore E, Morra VB, Coppola G, Vacca G, Alfano B, Salvatore M (2006) Grey matter loss in relapsing–remitting multiple sclerosis: a voxel-based morphometry study. Neuroimage 29:859–867PubMedCrossRef
Zurück zum Zitat Rocca MA, Pagani E, Ghezzi A, Falini A, Zaffaroni M, Colombo B, Scotti G, Comi G, Filippi M (2003) Functional cortical changes in patients with multiple sclerosis and nonspecific findings on conventional magnetic resonance imaging scans of the brain. Neuroimage 19:826–836PubMedCrossRef Rocca MA, Pagani E, Ghezzi A, Falini A, Zaffaroni M, Colombo B, Scotti G, Comi G, Filippi M (2003) Functional cortical changes in patients with multiple sclerosis and nonspecific findings on conventional magnetic resonance imaging scans of the brain. Neuroimage 19:826–836PubMedCrossRef
Zurück zum Zitat Rudick RA, Trapp BD (2009) Gray-matter injury in multiple sclerosis. N Engl J Med 361:1505–1506PubMedCrossRef Rudick RA, Trapp BD (2009) Gray-matter injury in multiple sclerosis. N Engl J Med 361:1505–1506PubMedCrossRef
Zurück zum Zitat Sailer M, Fischl B, Salat D, Tempelmann C, Schönfeld MA, Busa E, Bodammer N, Heinze HJ, Dale A (2003) Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126:1734–1744PubMedCrossRef Sailer M, Fischl B, Salat D, Tempelmann C, Schönfeld MA, Busa E, Bodammer N, Heinze HJ, Dale A (2003) Focal thinning of the cerebral cortex in multiple sclerosis. Brain 126:1734–1744PubMedCrossRef
Zurück zum Zitat Schaechter JD, Moore CI, Connell BD, Rosen BR, Dijkhuizen RM (2006) Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. Brain 129:2722–2733PubMedCrossRef Schaechter JD, Moore CI, Connell BD, Rosen BR, Dijkhuizen RM (2006) Structural and functional plasticity in the somatosensory cortex of chronic stroke patients. Brain 129:2722–2733PubMedCrossRef
Zurück zum Zitat Sfagos C, Papageorgiou CC, Kosma KK, Kodopadelis E, Uzunoglu NK, Vassilopoulos D, Rabavilas AD (2003) Working memory deficits in multiple sclerosis: a controlled study with auditory P600 correlates. J Neurol Neurosurg Psychiatry 74:1231–1235PubMedCrossRef Sfagos C, Papageorgiou CC, Kosma KK, Kodopadelis E, Uzunoglu NK, Vassilopoulos D, Rabavilas AD (2003) Working memory deficits in multiple sclerosis: a controlled study with auditory P600 correlates. J Neurol Neurosurg Psychiatry 74:1231–1235PubMedCrossRef
Zurück zum Zitat Smith AM, Walker LA, Freedman MS, DeMeulemeester C, Hogan MJ, Cameron I (2009) fMRI investigation of disinhibition in cognitively impaired patients with multiple sclerosis. J Neurol Sci 281:58–63PubMedCrossRef Smith AM, Walker LA, Freedman MS, DeMeulemeester C, Hogan MJ, Cameron I (2009) fMRI investigation of disinhibition in cognitively impaired patients with multiple sclerosis. J Neurol Sci 281:58–63PubMedCrossRef
Zurück zum Zitat Staffen W, Mair A, Zauner H, Unterrainer J, Niederhofer H, Kutzelnigg A, Ritter S, Golaszewski S, Iglseder B, Ladurner G (2002) Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. Brain 125:1275–1282PubMedCrossRef Staffen W, Mair A, Zauner H, Unterrainer J, Niederhofer H, Kutzelnigg A, Ritter S, Golaszewski S, Iglseder B, Ladurner G (2002) Cognitive function and fMRI in patients with multiple sclerosis: evidence for compensatory cortical activation during an attention task. Brain 125:1275–1282PubMedCrossRef
Zurück zum Zitat Tekok-Kilic A, Benedict RH, Weinstock-Guttman B, Dwyer MG, Carone D, Srinivasaraghavan B, Yella V, Abdelrahman N, Munschauer F, Bakshi R, Zivadinov R (2007) Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage 36:1294–1300PubMedCrossRef Tekok-Kilic A, Benedict RH, Weinstock-Guttman B, Dwyer MG, Carone D, Srinivasaraghavan B, Yella V, Abdelrahman N, Munschauer F, Bakshi R, Zivadinov R (2007) Independent contributions of cortical gray matter atrophy and ventricle enlargement for predicting neuropsychological impairment in multiple sclerosis. Neuroimage 36:1294–1300PubMedCrossRef
Zurück zum Zitat Tiberio M, Chard DT, Altmann DR, Davies G, Griffin CM, Rashid W, Sastre-Garriga J, Thompson AJ, Miller DH (2005) Gray and white matter volume changes in early RRMS: a 2-year longitudinal study. Neurology 64:1001–1007PubMedCrossRef Tiberio M, Chard DT, Altmann DR, Davies G, Griffin CM, Rashid W, Sastre-Garriga J, Thompson AJ, Miller DH (2005) Gray and white matter volume changes in early RRMS: a 2-year longitudinal study. Neurology 64:1001–1007PubMedCrossRef
Zurück zum Zitat Vercellino M, Plano F, Votta B, Mutani R, Giordana MT, Cavalla P (2005) Grey matter pathology in multiple sclerosis. J Neuropathol Exp Neurol 64:1101–1107PubMedCrossRef Vercellino M, Plano F, Votta B, Mutani R, Giordana MT, Cavalla P (2005) Grey matter pathology in multiple sclerosis. J Neuropathol Exp Neurol 64:1101–1107PubMedCrossRef
Zurück zum Zitat Zivadinov R, Minagar A (2009) Evidence for gray matter pathology in multiple sclerosis: a neuroimaging approach. J Neurol Sci 282:1–4PubMedCrossRef Zivadinov R, Minagar A (2009) Evidence for gray matter pathology in multiple sclerosis: a neuroimaging approach. J Neurol Sci 282:1–4PubMedCrossRef
Metadaten
Titel
Superior temporal gyrus thickness correlates with cognitive performance in multiple sclerosis
verfasst von
Asaf Achiron
Joab Chapman
Sigal Tal
Eran Bercovich
Hararai Gil
Anat Achiron
Publikationsdatum
01.07.2013
Verlag
Springer-Verlag
Erschienen in
Brain Structure and Function / Ausgabe 4/2013
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-012-0440-3

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