Abstract
OBJECTIVE—To explore functional corticocortical connections in multiple sclerosis by means of coherence of the EEG, and to evaluate their correlations with the degree of cognitive impairment and with brain lesion load assessed by MRI. METHODS—EEG coherence was studied from 28 patients with clinically definite multiple sclerosis. Ten minutes of resting EEG were recorded with 20 scalp electrodes, with binaural reference. FFT power and coherence were calculated in artifact free epochs of 1 second and compared with values from 22 control subjects of comparable age and sex distribution. Patients also underwent MRI (n=27) and neuropsychological examination (n=21). RESULTS—Compared with controls, patients with multiple sclerosis showed increased θ power in the frontotemporal-central regions (p<0.005). θ Band coherence was decreased between homologous areas (p<0.02). α Band coherence was decreased both in the local and long distance connections (p<0.0005). These findings were most striking both in patients with high MRI subcortical lesion load and in patients with cognitive involvement. A significant correlation was found between interhemispheric θ (p=0.02) and α (p=0.017) and anteroposterior α (p=0.013) coherence and subcortical MRI lesion load, but not with exclusively periventricular lesion load. CONCLUSIONS—These findings support the hypothesis that cognitive impairment in multiple sclerosis is mostly dependent on involvement of corticocortical connections related to demyelination and/or axonal loss within the white matter immediately underlying the cortex.
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- Amzica F., Steriade M. Disconnection of intracortical synaptic linkages disrupts synchronization of a slow oscillation. J Neurosci. 1995 Jun;15(6):4658–4677. doi: 10.1523/JNEUROSCI.15-06-04658.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beatty W. W., Goodkin D. E., Monson N., Beatty P. A. Cognitive disturbances in patients with relapsing remitting multiple sclerosis. Arch Neurol. 1989 Oct;46(10):1113–1119. doi: 10.1001/archneur.1989.00520460103020. [DOI] [PubMed] [Google Scholar]
- Beatty W. W. Memory and "frontal lobe" dysfunction in multiple sclerosis. J Neurol Sci. 1993 Apr;115 (Suppl):S38–S41. doi: 10.1016/0022-510x(93)90207-f. [DOI] [PubMed] [Google Scholar]
- Biggins C. A., Fein G., Raz J., Amir A. Artifactually high coherences result from using spherical spline computation of scalp current density. Electroencephalogr Clin Neurophysiol. 1991 Nov;79(5):413–419. doi: 10.1016/0013-4694(91)90206-j. [DOI] [PubMed] [Google Scholar]
- Busk J., Galbraith G. C. EEG correlates of visual-motor practice in man. Electroencephalogr Clin Neurophysiol. 1975 Apr;38(4):415–422. doi: 10.1016/0013-4694(75)90265-5. [DOI] [PubMed] [Google Scholar]
- Colon E., Hommes O. R., de Weerd J. P. Relation between EEG and disability scores in multiple sclerosis. Clin Neurol Neurosurg. 1981;83(3):163–168. doi: 10.1016/0303-8467(81)90018-4. [DOI] [PubMed] [Google Scholar]
- Comi G., Filippi M., Martinelli V., Campi A., Rodegher M., Alberoni M., Sirabian G., Canal N. Brain MRI correlates of cognitive impairment in primary and secondary progressive multiple sclerosis. J Neurol Sci. 1995 Oct;132(2):222–227. doi: 10.1016/0022-510x(95)00168-2. [DOI] [PubMed] [Google Scholar]
- Contreras D., Destexhe A., Sejnowski T. J., Steriade M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science. 1996 Nov 1;274(5288):771–774. doi: 10.1126/science.274.5288.771. [DOI] [PubMed] [Google Scholar]
- Corsi-Cabrera M., Trías G., Guevara M. A., Haro R., Hernández A. EEG interhemispheric correlation after callosotomy: one case study. Percept Mot Skills. 1995 Apr;80(2):504–506. doi: 10.2466/pms.1995.80.2.504. [DOI] [PubMed] [Google Scholar]
- Damian M. S., Schilling G., Bachmann G., Simon C., Stöppler S., Dorndorf W. White matter lesions and cognitive deficits: relevance of lesion pattern? Acta Neurol Scand. 1994 Dec;90(6):430–436. doi: 10.1111/j.1600-0404.1994.tb02753.x. [DOI] [PubMed] [Google Scholar]
- Duckrow R. B., Spencer S. S. Regional coherence and the transfer of ictal activity during seizure onset in the medial temporal lobe. Electroencephalogr Clin Neurophysiol. 1992 Jun;82(6):415–422. doi: 10.1016/0013-4694(92)90046-k. [DOI] [PubMed] [Google Scholar]
- Dunkin J. J., Leuchter A. F., Newton T. F., Cook I. A. Reduced EEG coherence in dementia: state or trait marker? Biol Psychiatry. 1994 Jun 1;35(11):870–879. doi: 10.1016/0006-3223(94)90023-x. [DOI] [PubMed] [Google Scholar]
- Facchetti D., Mai R., Colombo A., Capra R., Marciano N., Gasparotti R., Poloni M. Limited clinical significance of traditional and quantitative EEG in multiple sclerosis. Acta Neurol Belg. 1994;94(4):245–250. [PubMed] [Google Scholar]
- Fein G., Raz J., Brown F. F., Merrin E. L. Common reference coherence data are confounded by power and phase effects. Electroencephalogr Clin Neurophysiol. 1988 Jun;69(6):581–584. doi: 10.1016/0013-4694(88)90171-x. [DOI] [PubMed] [Google Scholar]
- Feng Y. K. Clinico-electroencephalographic studies of multiple sclerosis. Clin Exp Neurol. 1981;17:47–57. [PubMed] [Google Scholar]
- Filley C. M., Heaton R. K., Nelson L. M., Burks J. S., Franklin G. M. A comparison of dementia in Alzheimer's disease and multiple sclerosis. Arch Neurol. 1989 Feb;46(2):157–161. doi: 10.1001/archneur.1989.00520380061013. [DOI] [PubMed] [Google Scholar]
- Foong J., Rozewicz L., Chong W. K., Thompson A. J., Miller D. H., Ron M. A. A comparison of neuropsychological deficits in primary and secondary progressive multiple sclerosis. J Neurol. 2000 Feb;247(2):97–101. doi: 10.1007/pl00007804. [DOI] [PubMed] [Google Scholar]
- Foong J., Rozewicz L., Quaghebeur G., Davie C. A., Kartsounis L. D., Thompson A. J., Miller D. H., Ron M. A. Executive function in multiple sclerosis. The role of frontal lobe pathology. Brain. 1997 Jan;120(Pt 1):15–26. doi: 10.1093/brain/120.1.15. [DOI] [PubMed] [Google Scholar]
- Franklin G. M., Nelson L. M., Filley C. M., Heaton R. K. Cognitive loss in multiple sclerosis. Case reports and review of the literature. Arch Neurol. 1989 Feb;46(2):162–167. doi: 10.1001/archneur.1989.00520380066014. [DOI] [PubMed] [Google Scholar]
- Gotman J., Levtova V. Amygdala-hippocampus relationships in temporal lobe seizures: a phase-coherence study. Epilepsy Res. 1996 Sep;25(1):51–57. doi: 10.1016/0920-1211(96)00021-6. [DOI] [PubMed] [Google Scholar]
- Green J. B., Russell D. J. Electroencephalographic asymmetry with midline cyst and deficient corpus callosum. Case report. Neurology. 1966 Jun;16(6):541–545. doi: 10.1212/wnl.16.6.541. [DOI] [PubMed] [Google Scholar]
- Heaton R. K., Nelson L. M., Thompson D. S., Burks J. S., Franklin G. M. Neuropsychological findings in relapsing-remitting and chronic-progressive multiple sclerosis. J Consult Clin Psychol. 1985 Feb;53(1):103–110. doi: 10.1037//0022-006x.53.1.103. [DOI] [PubMed] [Google Scholar]
- Hjorth B. An on-line transformation of EEG scalp potentials into orthogonal source derivations. Electroencephalogr Clin Neurophysiol. 1975 Nov;39(5):526–530. doi: 10.1016/0013-4694(75)90056-5. [DOI] [PubMed] [Google Scholar]
- Koeda T., Knyazeva M., Njiokiktjien C., Jonkman E. J., De Sonneville L., Vildavsky V. The EEG in acallosal children. Coherence values in the resting state: left hemisphere compensatory mechanism? Electroencephalogr Clin Neurophysiol. 1995 Dec;95(6):397–407. doi: 10.1016/0013-4694(95)00171-9. [DOI] [PubMed] [Google Scholar]
- Kurtzke J. F. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983 Nov;33(11):1444–1452. doi: 10.1212/wnl.33.11.1444. [DOI] [PubMed] [Google Scholar]
- Locatelli T., Cursi M., Liberati D., Franceschi M., Comi G. EEG coherence in Alzheimer's disease. Electroencephalogr Clin Neurophysiol. 1998 Mar;106(3):229–237. doi: 10.1016/s0013-4694(97)00129-6. [DOI] [PubMed] [Google Scholar]
- Lublin F. D., Reingold S. C. Defining the clinical course of multiple sclerosis: results of an international survey. National Multiple Sclerosis Society (USA) Advisory Committee on Clinical Trials of New Agents in Multiple Sclerosis. Neurology. 1996 Apr;46(4):907–911. doi: 10.1212/wnl.46.4.907. [DOI] [PubMed] [Google Scholar]
- Merrin E. L., Floyd T. C. Negative symptoms and EEG alpha in schizophrenia: a replication. Schizophr Res. 1996 May;19(2-3):151–161. doi: 10.1016/0920-9964(96)88522-7. [DOI] [PubMed] [Google Scholar]
- Miki Y., Grossman R. I., Udupa J. K., Wei L., Kolson D. L., Mannon L. J., Grossman M. Isolated U-fiber involvement in MS: preliminary observations. Neurology. 1998 May;50(5):1301–1306. doi: 10.1212/wnl.50.5.1301. [DOI] [PubMed] [Google Scholar]
- Miller D. H., Barkhof F., Berry I., Kappos L., Scotti G., Thompson A. J. Magnetic resonance imaging in monitoring the treatment of multiple sclerosis: concerted action guidelines. J Neurol Neurosurg Psychiatry. 1991 Aug;54(8):683–688. doi: 10.1136/jnnp.54.8.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Montplaisir J., Nielsen T., Côté J., Boivin D., Rouleau I., Lapierre G. Interhemispheric EEG coherence before and after partial callosotomy. Clin Electroencephalogr. 1990 Jan;21(1):42–47. doi: 10.1177/155005949002100114. [DOI] [PubMed] [Google Scholar]
- Nagase Y., Terasaki O., Okubo Y., Matsuura M., Toru M. Lower interhemispheric coherence in a case of agenesis of the corpus callosum. Clin Electroencephalogr. 1994 Jan;25(1):36–39. doi: 10.1177/155005949402500110. [DOI] [PubMed] [Google Scholar]
- Newton T. F., Leuchter A. F., Miller E. N., Weiner H. Quantitative EEG in patients with AIDS and asymptomatic HIV infection. Clin Electroencephalogr. 1994 Jan;25(1):18–25. doi: 10.1177/155005949402500107. [DOI] [PubMed] [Google Scholar]
- Nielsen T., Montplaisir J., Lassonde M. Decreased interhemispheric EEG coherence during sleep in agenesis of the corpus callosum. Eur Neurol. 1993;33(2):173–176. doi: 10.1159/000116928. [DOI] [PubMed] [Google Scholar]
- Ormerod I. E., Miller D. H., McDonald W. I., du Boulay E. P., Rudge P., Kendall B. E., Moseley I. F., Johnson G., Tofts P. S., Halliday A. M. The role of NMR imaging in the assessment of multiple sclerosis and isolated neurological lesions. A quantitative study. Brain. 1987 Dec;110(Pt 6):1579–1616. doi: 10.1093/brain/110.6.1579. [DOI] [PubMed] [Google Scholar]
- Pascual-Marqui R. D., Gonzalez-Andino S. L., Valdes-Sosa P. A., Biscay-Lirio R. Current source density estimation and interpolation based on the spherical harmonic Fourier expansion. Int J Neurosci. 1988 Dec;43(3-4):237–249. doi: 10.3109/00207458808986175. [DOI] [PubMed] [Google Scholar]
- Pascual-Marqui R. D. The spherical spline Laplacian does not produce artifactually high coherences: comments on two articles by Biggins et al. Electroencephalogr Clin Neurophysiol. 1993 Jul;87(1):62–66. doi: 10.1016/0013-4694(93)90176-v. [DOI] [PubMed] [Google Scholar]
- Perrin F., Pernier J., Bertrand O., Echallier J. F. Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol. 1989 Feb;72(2):184–187. doi: 10.1016/0013-4694(89)90180-6. [DOI] [PubMed] [Google Scholar]
- Peyser J. M., Rao S. M., LaRocca N. G., Kaplan E. Guidelines for neuropsychological research in multiple sclerosis. Arch Neurol. 1990 Jan;47(1):94–97. doi: 10.1001/archneur.1990.00530010120030. [DOI] [PubMed] [Google Scholar]
- Quattrini A., Paggi A., Ortenzi A., Di Bella P., Cianci F., Forastieri L. CT and EEG investigations in 100 patients with multiple sclerosis (MS). Ital J Neurol Sci. 1981 Jan;2(1):25–34. doi: 10.1007/BF02351684. [DOI] [PubMed] [Google Scholar]
- Rao S. M., Leo G. J., Haughton V. M., St Aubin-Faubert P., Bernardin L. Correlation of magnetic resonance imaging with neuropsychological testing in multiple sclerosis. Neurology. 1989 Feb;39(2 Pt 1):161–166. doi: 10.1212/wnl.39.2.161. [DOI] [PubMed] [Google Scholar]
- Rao S. M. Neuropsychology of multiple sclerosis: a critical review. J Clin Exp Neuropsychol. 1986 Oct;8(5):503–542. doi: 10.1080/01688638608405173. [DOI] [PubMed] [Google Scholar]
- Rovaris M., Filippi M., Falautano M., Minicucci L., Rocca M. A., Martinelli V., Comi G. Relation between MR abnormalities and patterns of cognitive impairment in multiple sclerosis. Neurology. 1998 Jun;50(6):1601–1608. doi: 10.1212/wnl.50.6.1601. [DOI] [PubMed] [Google Scholar]
- Sklar B., Hanley J., Simmons W. W. An EEG experiment aimed toward identifying dyslexic children. Nature. 1972 Dec 15;240(5381):414–416. doi: 10.1038/240414a0. [DOI] [PubMed] [Google Scholar]
- Sloan E. P., Fenton G. W., Kennedy N. S., MacLennan J. M. Neurophysiology and SPECT cerebral blood flow patterns in dementia. Electroencephalogr Clin Neurophysiol. 1994 Sep;91(3):163–170. doi: 10.1016/0013-4694(94)90066-3. [DOI] [PubMed] [Google Scholar]
- Standardizzazione e taratura italiana di test neuropsicologici. Gruppo Italiano per lo Studio Neuropsicologico dell'Invecchiamento. Ital J Neurol Sci. 1987 Dec;Suppl 8:1–120. [PubMed] [Google Scholar]
- Swirsky-Sacchetti T., Mitchell D. R., Seward J., Gonzales C., Lublin F., Knobler R., Field H. L. Neuropsychological and structural brain lesions in multiple sclerosis: a regional analysis. Neurology. 1992 Jul;42(7):1291–1295. doi: 10.1212/wnl.42.7.1291. [DOI] [PubMed] [Google Scholar]
- Szentágothai J. The Ferrier Lecture, 1977. The neuron network of the cerebral cortex: a functional interpretation. Proc R Soc Lond B Biol Sci. 1978 May 16;201(1144):219–248. doi: 10.1098/rspb.1978.0043. [DOI] [PubMed] [Google Scholar]
- Thatcher R. W., Krause P. J., Hrybyk M. Cortico-cortical associations and EEG coherence: a two-compartmental model. Electroencephalogr Clin Neurophysiol. 1986 Aug;64(2):123–143. doi: 10.1016/0013-4694(86)90107-0. [DOI] [PubMed] [Google Scholar]
- Wada Y., Nanbu Y., Koshino Y., Shimada Y., Hashimoto T. Inter- and intrahemispheric EEG coherence during light drowsiness. Clin Electroencephalogr. 1996 Apr;27(2):84–88. doi: 10.1177/155005949602700207. [DOI] [PubMed] [Google Scholar]
