Semin Hear 2012; 33(03): 283-294
DOI: 10.1055/s-0032-1315727
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Magnetic Resonance Imaging Correlates of Dichotic Listening Performance in Multiple Sclerosis

Yosef A. Berlow
1   Advanced Imaging Research Center
2   Department of Behavioral Neuroscience
,
James Pollaro
1   Advanced Imaging Research Center
,
Christine Krisky
1   Advanced Imaging Research Center
,
John Grinstead
1   Advanced Imaging Research Center
8   Siemens Medical Solutions, USA Inc., Malverne, Pennsylvania
,
Mathew Snodgrass
1   Advanced Imaging Research Center
,
Keith Kohout
1   Advanced Imaging Research Center
,
M. Samantha Lewis
6   National Center for Rehabilitative Auditory Research (NCRAR)
8   Siemens Medical Solutions, USA Inc., Malverne, Pennsylvania
,
Debra Wilmington
6   National Center for Rehabilitative Auditory Research (NCRAR)
8   Siemens Medical Solutions, USA Inc., Malverne, Pennsylvania
,
Michele Hutter
6   National Center for Rehabilitative Auditory Research (NCRAR)
,
Linda Casiana
6   National Center for Rehabilitative Auditory Research (NCRAR)
,
Mary Fitzpatrick
6   National Center for Rehabilitative Auditory Research (NCRAR)
8   Siemens Medical Solutions, USA Inc., Malverne, Pennsylvania
,
David J. Lilly
6   National Center for Rehabilitative Auditory Research (NCRAR)
,
Stephen Fausti
6   National Center for Rehabilitative Auditory Research (NCRAR)
7   Neurology Service, Portland VA Medical Center, Portland, Oregon
,
Robert Folmer
6   National Center for Rehabilitative Auditory Research (NCRAR)
8   Siemens Medical Solutions, USA Inc., Malverne, Pennsylvania
,
Dennis Bourdette
7   Neurology Service, Portland VA Medical Center, Portland, Oregon
4   Department of Neurology, Oregon Health & Science University
,
William D. Rooney
1   Advanced Imaging Research Center
2   Department of Behavioral Neuroscience
5   Department of Biomedical Engineering, Oregon Health & Science University
› Author Affiliations
Further Information

Publication History

Publication Date:
31 July 2012 (online)

Abstract

Multiple sclerosis (MS) pathology can cause disruptions in central auditory processing. Here, we applied quantitative magnetic resonance imaging (MRI) techniques to investigate the impact of global neurodegenerative processes on dichotic listening performance in MS. We studied 28 subjects with clinically definite MS and 26 healthy controls using 3T MRI and a dichotic digits task (DDT) performed in the scanner. Subjects with MS displayed increased white matter lesions, prolonged water proton longitudinal relaxation time constants in normal appearing white matter, reduced gray matter volumes, and reduced corpus callosum areas compared with controls. No group differences were found for any of the DDT performance measures. In subjects with MS, corpus callosum area was strongly correlated with DDT performance. This relationship remained present after controlling for other measures of neuropathology, suggesting that callosal atrophy directly impacts dichotic listening performance in MS.

 
  • References

  • 1 The National Multiple Sclerosis Society. About MS. Available at: www.nationalmssociety.org . Accessed February 12, 2012
  • 2 Raine CS. The Norton Lecture: a review of the oligodendrocyte in the multiple sclerosis lesion. J Neuroimmunol 1997; 77: 135-152
  • 3 Compston A. The 150th anniversary of the first depiction of the lesions of multiple sclerosis. J Neurol Neurosurg Psychiatry 1988; 51: 1249-1252
  • 4 Miron VE, Kuhlmann T, Antel JP. Cells of the oligodendroglial lineage, myelination, and remyelination. Biochim Biophys Acta 2011; 1812: 184-193
  • 5 Young IR, Hall AS, Pallis CA, Legg NJ, Bydder GM, Steiner RE. Nuclear magnetic resonance imaging of the brain in multiple sclerosis. Lancet 1981; 2: 1063-1066
  • 6 Grossman RI, Gonzalez-Scarano F, Atlas SW, Galetta S, Silberberg DH. Multiple sclerosis: gadolinium enhancement in MR imaging. Radiology 1986; 161: 721-725
  • 7 Goodkin DE, Rooney WD, Sloan R , et al. A serial study of new MS lesions and the white matter from which they arise. Neurology 1998; 51: 1689-1697
  • 8 Polman CH, Reingold SC, Edan G , et al. Diagnostic criteria for multiple sclerosis: 2005 revisions to the “McDonald Criteria”. Ann Neurol 2005; 58: 840-846
  • 9 Rudick R, Antel J, Confavreux C , et al. Recommendations from the National Multiple Sclerosis Society Clinical Outcomes Assessment Task Force. Ann Neurol 1997; 42: 379-382
  • 10 Ogawa S, Tank DW, Menon R , et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci U S A 1992; 89: 5951-5955
  • 11 Lee M, Reddy H, Johansen-Berg H , et al. The motor cortex shows adaptive functional changes to brain injury from multiple sclerosis. Ann Neurol 2000; 47: 606-613
  • 12 Reddy H, Narayanan S, Matthews PM , et al. Relating axonal injury to functional recovery in MS. Neurology 2000; 54: 236-239
  • 13 Rocca MA, Colombo B, Falini A , et al. Cortical adaptation in patients with MS: a cross-sectional functional MRI study of disease phenotypes. Lancet Neurol 2005; 4: 618-626
  • 14 Audoin B, Au Duong MV, Malikova I , et al. Functional magnetic resonance imaging and cognition at the very early stage of MS. J Neurol Sci 2006; 245: 87-91
  • 15 Audoin B, Au Duong MV, Ranjeva J-P , et al. Magnetic resonance study of the influence of tissue damage and cortical reorganization on PASAT performance at the earliest stage of multiple sclerosis. Hum Brain Mapp 2005; 24: 216-228
  • 16 Filippi M, Rocca MA. Cortical reorganisation in patients with MS. J Neurol Neurosurg Psychiatry 2004; 75: 1087-1089
  • 17 Bernal B, Altman NR. Auditory functional MR imaging. AJR Am J Roentgenol 2001; 176: 1009-1015
  • 18 Edmister WB, Talavage TM, Ledden PJ, Weisskoff RM. Improved auditory cortex imaging using clustered volume acquisitions. Hum Brain Mapp 1999; 7: 89-97
  • 19 Westerhausen R, Woerner W, Kreuder F, Schweiger E, Hugdahl K, Wittling W. The role of the corpus callosum in dichotic listening: a combined morphological and diffusion tensor imaging study. Neuropsychology 2006; 20: 272-279
  • 20 Musiek FE, Weihing J. Perspectives on dichotic listening and the corpus callosum. Brain Cogn 2011; 76: 225-232
  • 21 Levine RA, Gardner JC, Stufflebeam SM , et al. Binaural auditory processing in multiple sclerosis subjects. Hear Res 1993; 68: 59-72
  • 22 Coelho A, Ceranić B, Prasher D, Miller DH, Luxon LM. Auditory efferent function is affected in multiple sclerosis. Ear Hear 2007; 28: 593-604
  • 23 Pelletier J, Habib M, Lyon-Caen O, Salamon G, Poncet M, Khalil R. Functional and magnetic resonance imaging correlates of callosal involvement in multiple sclerosis. Arch Neurol 1993; 50: 1077-1082
  • 24 Rao SM, Bernardin L, Leo GJ, Ellington L, Ryan SB, Burg LS. Cerebral disconnection in multiple sclerosis. Relationship to atrophy of the corpus callosum. Arch Neurol 1989; 46: 918-920
  • 25 Gadea M, Marti-Bonmatí L, Arana E, Espert R, Casanova V, Pascual A. Dichotic listening and corpus callosum magnetic resonance imaging in relapsing-remitting multiple sclerosis with emphasis on sex differences. Neuropsychology 2002; 16: 275-281
  • 26 Reinvang I, Bakke SJ, Hugdahl K, Karlsen NR, Sundet K. Dichotic listening performance in relation to callosal area on the MRI scan. Neuropsychology 1994; 8: 445-450
  • 27 Barkhof FJ, Elton M, Lindeboom J , et al. Functional correlates of callosal atrophy in relapsing-remitting multiple sclerosis patients. A preliminary MRI study. J Neurol 1998; 245: 153-158
  • 28 Simon JH, Jacobs LD, Campion MK , et al; The Multiple Sclerosis Collaborative Research Group (MSCRG). A longitudinal study of brain atrophy in relapsing multiple sclerosis. Neurology 1999; 53: 139-148
  • 29 Dietemann JL, Beigelman C, Rumbach L , et al. Multiple sclerosis and corpus callosum atrophy: relationship of MRI findings to clinical data. Neuroradiology 1988; 30: 478-480
  • 30 Evangelou N, Konz D, Esiri MM, Smith S, Palace J, Matthews PM. Regional axonal loss in the corpus callosum correlates with cerebral white matter lesion volume and distribution in multiple sclerosis. Brain 2000; 123 (Pt 9) 1845-1849
  • 31 Lewis MS, Wilmington D, Hutter M , et al. Preliminary identification of central auditory processing screening tests for individuals with multiple sclerosis. Sem Hear 2012; 33: 261-273
  • 32 Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33: 1444-1452
  • 33 Grinstead JW, Rooney WD. Fast T1 mapping in human brain using inversion recovery EPI with GRAPPA at 3T and 7T. Proc. Int. Soc. Magn. Reson. Med. 2008; 16: 3084
  • 34 Smith SM. Fast robust automated brain extraction. Hum Brain Mapp 2002; 17: 143-155
  • 35 Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 2001; 20: 45-57
  • 36 Smith SM, Zhang Y, Jenkinson M , et al. Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. Neuroimage 2002; 17: 479-489
  • 37 Smith SM, Jenkinson M, Woolrich MW , et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23 (Suppl. 01) S208-S219
  • 38 Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal 2001; 5: 143-156
  • 39 Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002; 17: 825-841
  • 40 Quarantelli M, Ciarmiello A, Morra VB , et al. Brain tissue volume changes in relapsing-remitting multiple sclerosis: correlation with lesion load. Neuroimage 2003; 18: 360-366
  • 41 Fisher E, Lee JC, Nakamura K, Rudick RA. Gray matter atrophy in multiple sclerosis: a longitudinal study. Ann Neurol 2008; 64: 255-265
  • 42 Roosendaal SD, Bendfeldt K, Vrenken H , et al. Grey matter volume in a large cohort of MS patients: relation to MRI parameters and disability. Mult Scler 2011; 17: 1098-1106
  • 43 Paolillo A, Pozzilli C, Gasperini C , et al. Brain atrophy in relapsing-remitting multiple sclerosis: relationship with “black holes,” disease duration and clinical disability. J Neurol Sci 2000; 174: 85-91
  • 44 Sanfilipo MP, Benedict RHB, Sharma J, Weinstock-Guttman B, Bakshi R. The relationship between whole brain volume and disability in multiple sclerosis: a comparison of normalized gray vs. white matter with misclassification correction. Neuroimage 2005; 26: 1068-1077
  • 45 Vrenken H, Rombouts SARB, Pouwels PJW, Barkhof F. Voxel-based analysis of quantitative T1 maps demonstrates that multiple sclerosis acts throughout the normal-appearing white matter. AJNR Am J Neuroradiol 2006; 27: 868-874
  • 46 Lindeboom J, ter Horst R. Interhemispheric disconnection effects in multiple sclerosis. J Neurol Neurosurg Psychiatry 1988; 51: 1445-1447
  • 47 Pelletier J, Suchet L, Witjas T , et al. A longitudinal study of callosal atrophy and interhemispheric dysfunction in relapsing-remitting multiple sclerosis. Arch Neurol 2001; 58: 105-111
  • 48 Ortiz N, Reicherts M, Pegna AJ , et al. Interhemispheric transfer evaluation in multiple sclerosis. Swiss J Psychol 2000; 59: 150-158
  • 49 Prinster A, Quarantelli M, Orefice G , et al. Grey matter loss in relapsing-remitting multiple sclerosis: a voxel-based morphometry study. Neuroimage 2006; 29: 859-867