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Published in: Journal of Neurology 5/2015

01-05-2015 | Original Communication

Ocular motor measures of cognitive dysfunction in multiple sclerosis II: working memory

Authors: Meaghan Clough, Laura Mitchell, Lynette Millist, Nathaniel Lizak, Shin Beh, Teresa C. Frohman, Elliot M. Frohman, Owen B. White, Joanne Fielding

Published in: Journal of Neurology | Issue 5/2015

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Abstract

Our companion paper documents pervasive inhibitory deficits in multiple sclerosis (MS) using ocular motor (OM) measures. Here we investigated the utility of an OM working memory (WMem) task in characterising WMem deficits in these patients as a function of disease status and disease duration. 22 patients with CIS, 22 early clinically definite MS patients (CDMS: <7 years of diagnosis), 22 late CDMS patients (>7 years from diagnosis), and 22 healthy controls participated. All participants completed the ocular motor WMem task, the paced auditory serial addition test (PASAT), and the symbol digit modalities test (SDMT). Clinical disability was characterised in CDMS patients using the Expanded Disability Severity Scale (EDSS). WMem performance was measured as proportion of errors (WMem errors), saccade latency, and relative sensitivity to WMem loading (WMem effect), an indicator of WMem capacity. All patient groups performed more WMem errors than controls with proportion of WMem errors, and degree of WMem effect increasing with increasing disease duration. A larger WMem effect, reflecting poorer WMem capacity, corresponded to poorer performance on neuropsychological measures, and a higher disability score for CDMS patients with the longest disease duration; an observation that suggests wider implication of WMem executive processes with advancing disease. Conspicuously, performance decrements on standard neuropsychological testing did not similarly increase commensurate with disease duration. The ocular motor WMem task appears to meaningfully dissociate WMem deficit from healthy individuals as well as a function of increasing disease duration. Potentially, this task represents a highly informative and objective method by which to ascertain progressive WMem changes from the earliest inception of MS.
Literature
1.
go back to reference Baddeley AD (1986) Working memory. Clarendon Press, Oxford Baddeley AD (1986) Working memory. Clarendon Press, Oxford
2.
3.
go back to reference Miyake A, Shah P (1999) Models of working memory: mechanisms of active maintenance and executive control. Cambridge University Press, New YorkCrossRef Miyake A, Shah P (1999) Models of working memory: mechanisms of active maintenance and executive control. Cambridge University Press, New YorkCrossRef
5.
go back to reference Amato MP, Ponziani G, Siracusa G, Sorbi S (2001) Cognitive dysfunction in early-onset multiple sclerosis—a reappraisal after 10 years. Arch Neurol 58(10):1602–1606CrossRefPubMed Amato MP, Ponziani G, Siracusa G, Sorbi S (2001) Cognitive dysfunction in early-onset multiple sclerosis—a reappraisal after 10 years. Arch Neurol 58(10):1602–1606CrossRefPubMed
6.
go back to reference Anhoque CF, Aires Domingues SC, Teixira AL, Domingues RB (2010) Cognitive impairment in clinically isolated syndrome. Demetia Neuropsychol 4(2):86–90 Anhoque CF, Aires Domingues SC, Teixira AL, Domingues RB (2010) Cognitive impairment in clinically isolated syndrome. Demetia Neuropsychol 4(2):86–90
7.
go back to reference Bobholz JA, Roo SM (2003) Cognitive dysfunction in multiple sclerosis: a review of recent developments. Curr Opin Neurol 16:283–288CrossRefPubMed Bobholz JA, Roo SM (2003) Cognitive dysfunction in multiple sclerosis: a review of recent developments. Curr Opin Neurol 16:283–288CrossRefPubMed
8.
go back to reference DeSousa EA, Albert RH, Kalman B (2002) Cognitive impairments in multiple sclerosis: a review. Am J Alzheimers Dis Other Demen 17:23–29CrossRefPubMed DeSousa EA, Albert RH, Kalman B (2002) Cognitive impairments in multiple sclerosis: a review. Am J Alzheimers Dis Other Demen 17:23–29CrossRefPubMed
9.
go back to reference Feuillet L, Reuter F, Audoin B, Malikova I, Barrau K, Cherif AA, Pelletier J (2007) Early cognitive impairment in patients with clinically isolated syndrome suggestive of multiple sclerosis. Mult Scler 13(1):124–127. doi:10.1177/1352458506071196 CrossRefPubMed Feuillet L, Reuter F, Audoin B, Malikova I, Barrau K, Cherif AA, Pelletier J (2007) Early cognitive impairment in patients with clinically isolated syndrome suggestive of multiple sclerosis. Mult Scler 13(1):124–127. doi:10.​1177/​1352458506071196​ CrossRefPubMed
15.
go back to reference Jeter CB, Patei SS, Sereno AB (2011) Novel n-back spatial working memory task using eye movement response. Behav Res Methods 43:879–887CrossRefPubMed Jeter CB, Patei SS, Sereno AB (2011) Novel n-back spatial working memory task using eye movement response. Behav Res Methods 43:879–887CrossRefPubMed
16.
go back to reference Miller KM, Price CC, Okun MS, Montijo H, Bowers D (2009) Is the n-back task a valid neuropsychological measure for assessing working memory. Arch Clin Neuropsychol 24:711–717PubMedCentralCrossRefPubMed Miller KM, Price CC, Okun MS, Montijo H, Bowers D (2009) Is the n-back task a valid neuropsychological measure for assessing working memory. Arch Clin Neuropsychol 24:711–717PubMedCentralCrossRefPubMed
17.
go back to reference Nelson H, Willison J (1991) The revised national adult reading test–test manual. NFER-Nelson, Windsor Nelson H, Willison J (1991) The revised national adult reading test–test manual. NFER-Nelson, Windsor
18.
go back to reference Beck AT, Steer RA (1987) Manual for the revised Beck Depression Inventory. Psychological Corporation, San Antonio Beck AT, Steer RA (1987) Manual for the revised Beck Depression Inventory. Psychological Corporation, San Antonio
19.
go back to reference Rosti E, Hämäläinen P, Koivisto K, Hokkanen L (2007) PASAT in detecting cognitive impairment in relapsing-remitting MS. Appl Neuropsychol 14(2):101–112CrossRefPubMed Rosti E, Hämäläinen P, Koivisto K, Hokkanen L (2007) PASAT in detecting cognitive impairment in relapsing-remitting MS. Appl Neuropsychol 14(2):101–112CrossRefPubMed
20.
go back to reference Smith A (1973) Symbol digit modalities test. Western Psychological Services, Los Angeles Smith A (1973) Symbol digit modalities test. Western Psychological Services, Los Angeles
26.
go back to reference Silver MR, Grossberg S, Bullock D, Histed MH, Miller EK (2012) A neural model of sequential movement planning and control of eye movements: item-order-rank working memory and saccade selection by the supplementary eye fields. Neural Netw 26:29–58. doi:10.1016/J.Neunet.10.004 CrossRefPubMed Silver MR, Grossberg S, Bullock D, Histed MH, Miller EK (2012) A neural model of sequential movement planning and control of eye movements: item-order-rank working memory and saccade selection by the supplementary eye fields. Neural Netw 26:29–58. doi:10.​1016/​J.​Neunet.​10.​004 CrossRefPubMed
30.
go back to reference Duong M-VA, Audoin B, Boulanouar K, Ibarrola D, Malikova I, Confort-Gouny S, Celsis P, Pelletier J, Cozzone PJ, Ranjeva J-P (2005) Altered functional connectivity related to white matter changes inside the working memory network at the very early stage of MS. J Cereb Blood Flow Metab 25:1245–1253CrossRef Duong M-VA, Audoin B, Boulanouar K, Ibarrola D, Malikova I, Confort-Gouny S, Celsis P, Pelletier J, Cozzone PJ, Ranjeva J-P (2005) Altered functional connectivity related to white matter changes inside the working memory network at the very early stage of MS. J Cereb Blood Flow Metab 25:1245–1253CrossRef
31.
go back to reference Duong MVA, Boulanouar K, Audoin B, Treseras S, Ibarrola D, Malikova I, Confort-Gouny S, Celsis P, Pelletier J, Cozzone PJ, Ranjeva JP (2005) Modulation of effective connectivity inside the working memory network in patients at the earliest stage of multiple sclerosis. Neuroimage 24(2):533–538. doi:10.1016/J.Neuroimage.08.038 CrossRef Duong MVA, Boulanouar K, Audoin B, Treseras S, Ibarrola D, Malikova I, Confort-Gouny S, Celsis P, Pelletier J, Cozzone PJ, Ranjeva JP (2005) Modulation of effective connectivity inside the working memory network in patients at the earliest stage of multiple sclerosis. Neuroimage 24(2):533–538. doi:10.​1016/​J.​Neuroimage.​08.​038 CrossRef
32.
go back to reference Forn C, Rocca M, Valsasina P, Bosca I, Casanova B, Avila C, Filippi M (2011) A connectivity fMRI study of working memory in a cohort of patients with clinically isolated syndrome (CIS) suggestive of multiple sclerosis (MS). Neurology 76(9):A81–A82 Forn C, Rocca M, Valsasina P, Bosca I, Casanova B, Avila C, Filippi M (2011) A connectivity fMRI study of working memory in a cohort of patients with clinically isolated syndrome (CIS) suggestive of multiple sclerosis (MS). Neurology 76(9):A81–A82
33.
go back to reference Audoin B, Guye M, Reuter F, Duong MVA, Confort-Gouny S, Malikova I, Soulier E, Viout P, Cherif AA, Cozzone PJ, Pelletier J, Ranjeva JP (2007) Structure of WM bundles constituting the working memory system in early multiple sclerosis: a quantitative DTI tractography study. Neuroimage 36(4):1324–1330. doi:10.1016/J.Neuroimage.04.038 CrossRefPubMed Audoin B, Guye M, Reuter F, Duong MVA, Confort-Gouny S, Malikova I, Soulier E, Viout P, Cherif AA, Cozzone PJ, Pelletier J, Ranjeva JP (2007) Structure of WM bundles constituting the working memory system in early multiple sclerosis: a quantitative DTI tractography study. Neuroimage 36(4):1324–1330. doi:10.​1016/​J.​Neuroimage.​04.​038 CrossRefPubMed
35.
go back to reference Audoin B, Duong MV, Malikova I, Confort-Gouny S, Ibarrola D, Cozzone PJ, Pelletier J, Ranjeva JP (2006) Functional magnetic resonance imaging and cognition at the very early stage of MS. J Neurol Sci 245(1–2):87–91. doi:10.1016/J.Jns.08.026 CrossRefPubMed Audoin B, Duong MV, Malikova I, Confort-Gouny S, Ibarrola D, Cozzone PJ, Pelletier J, Ranjeva JP (2006) Functional magnetic resonance imaging and cognition at the very early stage of MS. J Neurol Sci 245(1–2):87–91. doi:10.​1016/​J.​Jns.​08.​026 CrossRefPubMed
36.
go back to reference Audoin B, Duong MV, Ranjeva JP, Ibarrola D, Malikova I, Confort-Gouny S, Soulier E, Viout P, Ali-Cherif A, Pelletier J, Cozzone PJ (2005) 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 24(3):216–228. doi:10.1002/hbm.20083 CrossRefPubMed Audoin B, Duong MV, Ranjeva JP, Ibarrola D, Malikova I, Confort-Gouny S, Soulier E, Viout P, Ali-Cherif A, Pelletier J, Cozzone PJ (2005) 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 24(3):216–228. doi:10.​1002/​hbm.​20083 CrossRefPubMed
37.
go back to reference Rocca MA, Falini A, Colombo B, Scotti G, Comi G, Filippi M (2002) Adaptive functional changes in the cerebral cortex of patients with nondisabling multiple sclerosis correlate with the extent of brain structural damage. Ann Neurol 51(3):330–339. doi:10.1002/ana.10120 CrossRefPubMed Rocca MA, Falini A, Colombo B, Scotti G, Comi G, Filippi M (2002) Adaptive functional changes in the cerebral cortex of patients with nondisabling multiple sclerosis correlate with the extent of brain structural damage. Ann Neurol 51(3):330–339. doi:10.​1002/​ana.​10120 CrossRefPubMed
Metadata
Title
Ocular motor measures of cognitive dysfunction in multiple sclerosis II: working memory
Authors
Meaghan Clough
Laura Mitchell
Lynette Millist
Nathaniel Lizak
Shin Beh
Teresa C. Frohman
Elliot M. Frohman
Owen B. White
Joanne Fielding
Publication date
01-05-2015
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 5/2015
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-015-7644-4

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