The pathophysiology of multiple sclerosis: the mechanisms underlying the production of symptoms and the natural history of the disease.

The pathophysiology of multiple sclerosis is reviewed, with emphasis on the axonal conduction properties underlying the production of symptoms, and the course of the disease. The major cause of the negative symptoms during relapses (e.g. paralysis, blindness and numbness) is conduction block, caused largely by demyelination and inflammation, and possibly by defects in synaptic transmission and putative circulating blocking factors. Recovery from symptoms during remissions is due mainly to the restoration of axonal function, either by remyelination, the resolution of inflammation, or the restoration of conduction to axons which persist in the demyelinated state. Conduction in the latter axons shows a number of deficits, particularly with regard to the conduction of trains of impulses and these contribute to weakness and sensory problems. The mechanisms underlying the sensitivity of symptoms to changes in body temperature (Uhthoff's phenomenon) are discussed. The origin of 'positive' symptoms, such as tingling sensations, are described, including the generation of ectopic trains and bursts of impulses, ephaptic interactions between axons and/or neurons, the triggering of additional, spurious impulses by the transmission of normal impulses, the mechanosensitivity of axons underlying movement-induced sensations (e.g. Lhermitte's phenomenon) and pain. The clinical course of the disease is discussed, together with its relationship to the evolution of lesions as revealed by magnetic resonance imaging and spectroscopy. The earliest detectable event in the development of most new lesions is a breakdown of the blood-brain barrier in association with inflammation. Inflammation resolves after approximately one month, at which time there is an improvement in the symptoms. Demyelination occurs during the inflammatory phase of the lesion. An important mechanism determining persistent neurological deficit is axonal degeneration, although persistent conduction block arising from the failure of repair mechanisms probably also contributes.

[1]  S. Waxman,et al.  Sodium channel expression: a dynamic process in neurons and non-neuronal cells. , 1996, Developmental neuroscience.

[2]  D. Mattson,et al.  Nerve conduction block by nitric oxide that is mediated by the axonal environment. , 1998, Journal of neurophysiology.

[3]  H. Kilbinger Modulation of acetylcholine release by nitric oxide. , 1996, Progress in brain research.

[4]  A. Thompson,et al.  Major differences in the dynamics of primary and secondary progressive multiple sclerosis , 1991, Annals of neurology.

[5]  K. Smith,et al.  Saltatory conduction precedes remyelination in axons demyelinated with lysophosphatidyl choline , 1982, Journal of the Neurological Sciences.

[6]  R. Fishman A tribute to Lewis P. Rowland , 1987, Neurology.

[7]  H. Brinkmeier,et al.  On the nature of endogenous antiexcitatory factors in the cerebrospinal fluid of patients with demyelinating neurological disease , 1996, Muscle & nerve.

[8]  Y.-G. Li,et al.  Slow sodium-dependent potential oscillations contribute to ectopic firing in mammalian demyelinated axons. , 1997, Brain : a journal of neurology.

[9]  R. Kaji,et al.  Ouabain reverses conduction disturbances in single demyelinated nerve fibers , 1989, Neurology.

[10]  S G Waxman,et al.  Delayed depolarization and slow sodium currents in cutaneous afferents. , 1994, Journal of neurophysiology.

[11]  J. Merrill,et al.  Cytokines in inflammatory brain lesions: helpful and harmful , 1996, Trends in Neurosciences.

[12]  C. Cleeland,et al.  Symptom instability and thermoregulation in multiple sclerosis , 1972, Neurology.

[13]  M. Koltzenburg,et al.  Circulating adhesion molecules and inflammatory mediators in demyelination , 1995, Neurology.

[14]  C. Schauf,et al.  Neuroelectric blocking factors in human and animal sera evaluated using the isolated frog spinal cord. , 1976, Journal of neurology, neurosurgery, and psychiatry.

[15]  R. Willison,et al.  FLICKER FUSION IN MULTIPLE SCLEROSIS , 1961, Journal of neurology, neurosurgery, and psychiatry.

[16]  M. Rasminsky,et al.  The effects of temperature on conduction in demyelinated single nerve fibers. , 1973, Archives of neurology.

[17]  T A Sears,et al.  The effects of 4‐aminopyridine and tetraethylammonium ions on normal and demyelinated mammalian nerve fibres. , 1981, The Journal of physiology.

[18]  C. Westerberg,et al.  Paroxysmal attacks in multiple sclerosis. , 1975, Brain : a journal of neurology.

[19]  J. G. Phadke,et al.  Atypical and clinically silent multiple sclerosis: a report of 12 cases discovered unexpectedly at necropsy. , 1983, Journal of neurology, neurosurgery, and psychiatry.

[20]  M. Rasminsky Ephaptic transmission between single nerve fibres in the spinal nerve roots of dystrophic mice. , 1980 .

[21]  Y. Courtois,et al.  Control of nitric oxide production by endogenous TNF-alpha in mouse retinal pigmented epithelial and Muller glial cells. , 1997, Biochemical and biophysical research communications.

[22]  J. Howe,et al.  Lhermitte's sign in multiple sclerosis: a clinical survey and review of the literature. , 1982, Journal of neurology, neurosurgery, and psychiatry.

[23]  C. Katsetos,et al.  Inducible Nitric Oxide Synthase and Nitrotyrosine Are Found in Monocytes/Macrophages and/or Astrocytes in Acute, but Not in Chronic, Multiple Sclerosis , 1998, Clinical Diagnostic Laboratory Immunology.

[24]  S. Aparicio,et al.  Anti-synaptic antibody in allergic encephalomyelitis I. Neurophysiological studies, in guinea pigs, on the exposed cerebral cortex and peripheral nerves, following immunological challenges with myelin and synaptosomes , 1975, Brain Research.

[25]  S. Waxman Clinicopathological correlations in multiple sclerosis and related diseases. , 1981, Advances in neurology.

[26]  T. Olsen,et al.  Early Time Course of N‐Acetylaspartate, Creatine and Phosphocreatine, and Compounds Containing Choline in the Brain After Acute Stroke: A Proton Magnetic Resonance Spectroscopy Study , 1992, Stroke.

[27]  A. Blight,et al.  The effects of 4-aminopyridine on neurological deficits in chronic cases of traumatic spinal cord injury in dogs: a phase I clinical trial. , 1991, Journal of neurotrauma.

[28]  A. Sumner,et al.  Effect of digitalis on central demyelinative conduction block in vivo , 1989, Annals of neurology.

[29]  W. Sheremata,et al.  Persistent neurological deficit precipitated by hot bath test in multiple sclerosis. , 1983, JAMA.

[30]  R. Liblau,et al.  Schwann cell transplantation and myelin repair of the CNS , 1997, Multiple sclerosis.

[31]  S. Waxman,et al.  Mechanisms of paresthesiae, dysesthesiae, and hyperesthesiae: role of Na+ channel heterogeneity. , 1996, European neurology.

[32]  K. Hagbarth,et al.  Ectopic sensory discharges and paresthesiae in patients with disorders of peripheral nerves, dorsal roots and dorsal columns , 1984, Pain.

[33]  Kenneth J. Smith Conduction properties of central demyelinated and remyelinated axons, and their relation to symptom production in demyelinating disorders , 1994, Eye.

[34]  F. A. Davis,et al.  Effect of intravenous sodium bicarbonate, disodium edetate (Na2EDTA), and hyperventilation on visual and oculomotor signs in multiple sclerosis , 1970, Journal of neurology, neurosurgery, and psychiatry.

[35]  P. Rudge,et al.  Abnormalities of the auditory evoked potentials in patients with multiple sclerosis. , 1977, Brain : a journal of neurology.

[36]  V. Provitera,et al.  Profile of cerebrospinal fluid and serum cytokines in patients with relapsing-remitting multiple sclerosis: a correlation with clinical activity. , 1998, Immunopharmacology and immunotoxicology.

[37]  S. Waxman,et al.  Transplanted Olfactory Ensheathing Cells Remyelinate and Enhance Axonal Conduction in the Demyelinated Dorsal Columns of the Rat Spinal Cord , 1998, The Journal of Neuroscience.

[38]  J. England,et al.  Immunocytochemical investigations of sodium channels along nodal and internodal portions of demyelinated axons , 1996, Microscopy research and technique.

[39]  J. Chalk,et al.  Conduction abnormalities are restricted to the central nervous system in experimental autoimmune encephalomyelitis induced by inoculation with proteolipid protein but not with myelin basic protein. , 1994, Brain : a journal of neurology.

[40]  W. Mcdonald,et al.  Spontaneous and mechanically evoked activity due to central demyelinating lesion , 1980, Nature.

[41]  G. Celesia,et al.  Visual electroencephalographic computer analysis (VECA) , 1977, Neurology.

[42]  F. Eusebi,et al.  Interferon inhibits synaptic potentiation in rat hippocampus , 1991, Brain Research.

[43]  J. Cerf,et al.  Multiple Sclerosis: Serum Factor Producing Reversible Alterations in Bioelectric Responses , 1966, Science.

[44]  David Regan,et al.  Differential diagnosis of multiple sclerosis by visual evoked potential recording. , 1974, Brain : a journal of neurology.

[45]  S. Chandler,et al.  Matrix metalloproteinases, tumor necrosis factor and multiple sclerosis: an overview , 1997, Journal of Neuroimmunology.

[46]  S. Waxman,et al.  Transplantation of glial cells enhances action potential conduction of amyelinated spinal cord axons in the myelin-deficient rat. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[47]  A J Thompson,et al.  A comparison of the pathology of primary and secondary progressive multiple sclerosis. , 1994, Brain : a journal of neurology.

[48]  P. Shrager,et al.  Survival, development, and electrical activity of central nervous system myelinated axons exposed to tumor necrosis factor in vitro , 1995, Journal of neuroscience research.

[49]  H. Goren,et al.  The hot bath test in the diagnosis of multiple sclerosis. , 1981, JAMA.

[50]  L. G. Miller,et al.  Interleukin‐1 Modulates GABAergic and Glutamatergic Function in Brain a , 1994, Annals of the New York Academy of Sciences.

[51]  S. Waxman,et al.  Restoration of Normal Conduction Properties in Demyelinated Spinal Cord Axons in the Adult Rat by Transplantation of Exogenous Schwann Cells , 1996, The Journal of Neuroscience.

[52]  M. Pender The pathophysiology of myelin basic protein-induced acute experimental allergic encephalomyelitis in the Lewis rat , 1988, Journal of the Neurological Sciences.

[53]  T. Deerinck,et al.  Clusters of axonal Na+ channels adjacent to remyelinating Schwann cells , 1996, Journal of neurocytology.

[54]  M. Pender Recovery from acute experimental allergic encephalomyelitis in the Lewis rat. Early restoration of nerve conduction and repair by Schwann cells and oligodendrocytes. , 1989, Brain : a journal of neurology.

[55]  F. A. Davis,et al.  Altered thermal sensitivity in injured and demyelinated nerve , 1971, Journal of neurology, neurosurgery, and psychiatry.

[56]  H Bostock,et al.  Ectopic activity in demyelinated spinal root axons of the rat. , 1992, The Journal of physiology.

[57]  G. Siggins,et al.  Interleukin 1β inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus , 1993, Brain Research.

[58]  S. Waxman,et al.  Distribution of sodium channels in chronically demyelinated spinal cord axons: immuno-ultrastructural localization and electrophysiological observations , 1991, Brain Research.

[59]  T. Sears,et al.  The pathophysiology of demyelination and its implications for the symptomatic treatment of multiple sclerosis , 1978, Neurology.

[60]  K. Smith,et al.  Effects of 4-aminopyridine on demyelinated axons, synapses and muscle tension. , 2000, Brain : a journal of neurology.

[61]  A. L. Leiman,et al.  Myelination inhibiting and neuroelectric blocking factors in experimental allergic encephalomyelitis. , 1975, Science.

[62]  A. Hirano,et al.  Asymptomatic Demyelinated Plaque , 1974 .

[63]  M. Bornstein,et al.  Functional Studies of Cultured Brain Tissues as Related to "Demyelinative Disorders" , 1965, Science.

[64]  Hyung-Cheul Shin,et al.  Interleukin 2 suppresses afferent sensory transmission in the primary somatosensory cortex , 1995, Neuroreport.

[65]  Elisabeth F. Targ,et al.  4-aminopyridine leads to restoration of conduction in demyelinated rat sciatic nerve , 1985, Brain Research.

[66]  S. Waxman,et al.  Chapter 29 Enhancement of action potential conduction following demyelination: experimental approaches to restoration of function in multiple sclerosis and spinal cord injury , 1994 .

[67]  C. Schauf,et al.  Physiologic basis for neuroelectric blocking activity in multiple sclerosis , 1981, Neurology.

[68]  W. Mcdonald,et al.  The restoration of conduction by central remyelination. , 1981, Brain : a journal of neurology.

[69]  Davis Fa,et al.  Circulating toxic factors in multiple sclerosis: a perspective. , 1981 .

[70]  L. Jacobs,et al.  The lesion causing continuous facial myokymia in multiple sclerosis. , 1994, Archives of neurology.

[71]  I. Moseley,et al.  Asymptomatic spinal cord lesions in clinically isolated optic nerve, brain stem, and spinal cord syndromes suggestive of demyelination , 1998, Journal of neurology, neurosurgery, and psychiatry.

[72]  Peter Shrager,et al.  Axonal coding of action potentials in demyelinated nerve fibers , 1993, Brain Research.

[73]  J. Kastrup,et al.  Chronic pain treatment with intravenous lidocaine. , 1986, Neurological research.

[74]  D. Hanley,et al.  Induction of nitric oxide synthase in demyelinating regions of multiple sclerosis brains , 1994, Annals of neurology.

[75]  Kenneth J. Smith,et al.  The use of potassium channel blocking agents in the therapy of demyelinating diseases , 1994, Annals of neurology.

[76]  W. I. McDonald,et al.  Spontaneous and evoked electrical discharges from a central demyelinating lesion , 1982, Journal of the Neurological Sciences.

[77]  S G Waxman,et al.  Noninactivating, tetrodotoxin-sensitive Na+ conductance in rat optic nerve axons. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Y. Ando,et al.  Changes in nitrite and nitrate (NO2 −/NO3 −) levels in cerebrospinal fluid of patients with multiple sclerosis , 1997, Journal of the Neurological Sciences.

[79]  Shuxian Hu,et al.  Differential regulation by cytokines of human astrocyte nitric oxide production , 1995, Glia.

[80]  P. Shrager,et al.  Optical measurement of conduction in single demyelinated axons , 1990, The Journal of general physiology.

[81]  J. Schwarz,et al.  Phenytoin and Carbamazepine: Potential‐ and Frequency‐Dependent Block of Na Currents in Mammalian Myelinated Nerve Fibers , 1989, Epilepsia.

[82]  Y. Mimura,et al.  Mechanisms of hyperpolarization induced by two cytokines, hTNFα and hIL-1α in neurons of the mollusc,Onchidium , 1994, Brain Research.

[83]  H. Wiśniewski,et al.  RELATION BETWEEN MYELINATION AND FUNCTION IN MS AND EAE.: 56 , 1976 .

[84]  M. Kuno,et al.  Electrophysiological properties of spinal motoneurones of normal and dystrophic mice. , 1975, The Journal of physiology.

[85]  T. Sears,et al.  Continuous conduction in demyelinated mammalian nerve fibres , 1976, Nature.

[86]  W. Mcdonald,et al.  Morphological characteristics of central demyelination and remyelination: A single‐fiber study , 1977, Annals of neurology.

[87]  C. Schauf,et al.  The occurrence, specificity, and role of neuroelectric blocking factors in multiple sclerosis , 1978, Neurology.

[88]  H. Link,et al.  Review: cytokines and the pathogenesis of multiple sclerosis , 1996, Journal of neuroscience research.

[89]  T A Sears,et al.  Internodal conduction in undissected demyelinated nerve fibres , 1972, The Journal of physiology.

[90]  H. Köller,et al.  Cerebrospinal fluid from multiple sclerosis patients inactivates neuronal Na+ current. , 1996, Brain : a journal of neurology.

[91]  D. Mattson,et al.  Interferon-beta-1-b (IFN-B) decreases induced nitric oxide (NO) production by a human astrocytoma cell line , 1998, Journal of Neuroimmunology.

[92]  M H Brill,et al.  Conduction through demyelinated plaques in multiple sclerosis: computer simulations of facilitation by short internodes. , 1978, Journal of neurology, neurosurgery, and psychiatry.

[93]  William Albert Hugh Rushton,et al.  Initiation of the Propagated Disturbance , 1937 .

[94]  S. Levinson,et al.  Clustering of Na+ channels and node of Ranvier formation in remyelinating axons , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[95]  R Wagner,et al.  Tumour necrosis factor-α induces ectopic activity in nociceptive primary afferent fibres , 1997, Neuroscience.

[96]  A. Compston,et al.  Monoclonal antibody treatment exposes three mechanisms underlying the clinical course of multiple sclerosis , 1999, Annals of neurology.

[97]  Davis Fa,et al.  Approaches to the development of pharmacological interventions in multiple sclerosis. , 1981 .

[98]  C. Schauf,et al.  Complement‐dependent serum , 1978, Neurology.

[99]  T. Sears,et al.  The pathophysiology of acute experimental allergic encephalomyelitis in the rabbit. , 1984, Brain : a journal of neurology.

[100]  C. Brosnan,et al.  Cytokine localization in multiple sclerosis lesions , 1995, Neurology.

[101]  B E Kendall,et al.  Serial gadolinium enhanced magnetic resonance imaging in multiple sclerosis. , 1988, Brain : a journal of neurology.

[102]  A. L. Leiman,et al.  Neuroelectric blocking factors in multiple sclerosis and normal human sera. , 1976, Archives of neurology.

[103]  R J Sclabassi,et al.  Somatosensory response to stimulus trains in patients with multiple sclerosis. , 1974, Electroencephalography and clinical neurophysiology.

[104]  Kenneth J. Smith,et al.  Internodal potassium currents can generate ectopic impulses in mammalian myelinated axons , 1993, Brain Research.

[105]  C. Bever The current status of studies of aminopyridines in patients with multiple sclerosis , 1994, Annals of neurology.

[106]  T. Sears,et al.  Overcoming conduction failure in demyelinated nerve fibres by prolonging action potentials , 1978, Nature.

[107]  D. Li,et al.  Serial magnetic resonance scanning in multiple sclerosis: A second prospective study in relapsing patients , 1989, Annals of neurology.

[108]  C. Schroeder,et al.  Preliminary studies of cytokine-induced functional effects on the visual pathways in the rabbit , 1989, Journal of Neuroimmunology.

[109]  F. A. Davis Neurological deficits following the hot bath test in multiple sclerosis. , 1985, JAMA.

[110]  R. Miller,et al.  Raised serum nitrate and nitrite levels in patients with multiple sclerosis , 1997, Journal of the Neurological Sciences.

[111]  G J Barker,et al.  Serial proton magnetic resonance spectroscopy in acute multiple sclerosis lesions. , 1994, Brain : a journal of neurology.

[112]  G J Barker,et al.  Sensitivity of contrast enhanced MRI in multiple sclerosis. Effects of gadolinium dose, magnetization transfer contrast and delayed imaging. , 1997, Brain : a journal of neurology.

[113]  C. D. DE GROOT,et al.  Immunocytochemical Characterization of the Expression of Inducible and Constitutive Isoforms of Nitric Oxide Synthase in Demyelinating Multiple Sclerosis Lesions , 1997, Journal of neuropathology and experimental neurology.

[114]  C. Brosnan,et al.  Selective inhibition of human glial inducible nitric oxide synthase by interferon‐β: Implications for multiple sclerosis , 1998, Annals of neurology.

[115]  S. Waxman,et al.  Downregulation of Tetrodotoxin-Resistant Sodium Currents and Upregulation of a Rapidly Repriming Tetrodotoxin-Sensitive Sodium Current in Small Spinal Sensory Neurons after Nerve Injury , 1997, The Journal of Neuroscience.

[116]  T. Sears,et al.  Effect of Demyelination on Conduction in the Central Nervous System , 1969, Nature.

[117]  P. Kara,et al.  Dynamic modulation of cerebral cortex synaptic function by nitric oxide. , 1998, Progress in brain research.

[118]  J. Selhorst,et al.  Uhthoff and his symptom. , 1995, Journal of neuro-ophthalmology : the official journal of the North American Neuro-Ophthalmology Society.

[119]  E. Cho,et al.  Multiple sclerosis: Remyelination of nascent lesions: Remyelination of nascent lesions , 1993 .

[120]  J. M. Ritchie,et al.  Molecular dissection of the myelinated axon , 1993, Annals of neurology.

[121]  R. Edlich,et al.  A fatal case of sun exposure in a multiple sclerosis patient. , 1989, The Journal of emergency medicine.

[122]  M. Lazdunski,et al.  Increase of sodium channels in demyelinated lesions of multiple sclerosis , 1991, Brain Research.

[123]  A. Thompson,et al.  Persistent functional deficit in multiple sclerosis and autosomal dominant cerebellar ataxia is associated with axon loss. , 1995, Brain : a journal of neurology.

[124]  M. Rasminsky Ectopic generation of impulses and cross‐talk in spinal nerve roots of “dystrophic” mice , 1978, Annals of neurology.

[125]  F. Abboud,et al.  Nitric Oxide as an Autocrine Regulator of Sodium Currents in Baroreceptor Neurons , 1998, Neuron.

[126]  D. Goodkin Interferon β therapy for multiple sclerosis , 1998, The Lancet.

[127]  P. Gloor,et al.  FACIAL MYOKYMIA IN MULTIPLE SCLEROSIS , 1961 .

[128]  C. Schauf,et al.  Movement phosphenes in optic neuritis , 1976, Neurology.

[129]  K. Burchiel Abnormal impulse generation in focally demyelinated trigeminal roots , 1980 .

[130]  M. Small,et al.  The cervical somatosensory evoked potential (SEP) in the diagnosis of multiple sclerosis , 1978, Journal of the Neurological Sciences.

[131]  William H. Calvin,et al.  Impulses reflected from dorsal root ganglia and from focal nerve injuries , 1976, Brain Research.

[132]  A. Ghezzi,et al.  Epilepsy in multiple sclerosis. , 1990, European neurology.

[133]  O Herreras,et al.  The effect of depressing glial function in rat brain in situ on ion homeostasis, synaptic transmission, and neuron survival , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[134]  J. Bolaños,et al.  Evidence for increased nitric oxide production in multiple sclerosis. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[135]  D. Burke Microneurography, impulse conduction, and paresthesias , 1993, Muscle & nerve.

[136]  T A Sears,et al.  The effects of experimental demyelination on conduction in the central nervous system. , 1970, Brain : a journal of neurology.

[137]  J. M. Ritchie,et al.  Evidence for the presence of potassium channels in the paranodal region of acutely demyelinated mammalian single nerve fibres. , 1981, The Journal of physiology.

[138]  D. Paty,et al.  CORRELATION BETWEEN NMR SCAN AND BRAIN SLICE DATA IN MULTIPLE SCLEROSIS , 1984, The Lancet.

[139]  J. Kurtzke Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[140]  Moses Rodriguez,et al.  Absence of neurological deficits following extensive demyelination in a class I-deficient murine model of multiple sclerosis , 1998, Nature Medicine.

[141]  C. Hölscher Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity , 1997, Trends in Neurosciences.

[142]  R. Schmidt,et al.  Peroxynitrite formation within the central nervous system in active multiple sclerosis , 1998, Journal of Neuroimmunology.

[143]  M. Pender The pathophysiology of acute experimental allergic encephalomyelitis induced by whole spinal cord in the Lewis rat , 1988, Journal of the Neurological Sciences.

[144]  K. Smith,et al.  A mechanism for ectopic firing in central demyelinated axons. , 1995, Brain : a journal of neurology.

[145]  D. Paty,et al.  Magnetic resonance in multiple sclerosis. , 1997, Current opinion in neurology and neurosurgery.

[146]  Mark J. Brown,et al.  Multifocal demyelinating neuropathy with persistent conduction block , 1982, Neurology.

[147]  H. Shibasaki,et al.  Racial modification of clinical picture of multiple sclerosis Comparison between British and Japanese patients , 1981, Journal of the Neurological Sciences.

[148]  F. Barkhof,et al.  Accumulation of hypointense lesions ("black holes") on T1 spin-echo MRI correlates with disease progression in multiple sclerosis , 1996, Neurology.

[149]  M. Lazdunski,et al.  TRAAK Is a Mammalian Neuronal Mechano-gated K+Channel* , 1999, The Journal of Biological Chemistry.

[150]  Kenneth J. Smith,et al.  Conduction in Segmentally Demyelinated Mammalian Central Axons , 1997, The Journal of Neuroscience.

[151]  A. Compston,et al.  Beta-interferon and multiple sclerosis , 1997, Trends in Neurosciences.

[152]  J. Chalk,et al.  Restoration of conduction in the spinal roots correlates with clinical recovery from experimental autoimmune encephalomyelitis , 1995, Muscle & nerve.

[153]  J. Olesen,et al.  In vivo determination of T1 and T2 in the brain of patients with severe but stable multiple sclerosis , 1988, Magnetic resonance in medicine.

[154]  J. Taubenberger,et al.  Correlation between magnetic resonance imaging findings and lesion development in chronic, active multiple sclerosis , 1993, Annals of neurology.

[155]  B E Kendall,et al.  Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenetic and clinical implications. , 1990, Brain : a journal of neurology.

[156]  A. Compston,et al.  Transient increase in symptoms associated with cytokine release in patients with multiple sclerosis. , 1996, Brain : a journal of neurology.

[157]  A. Hodgkin,et al.  The action of calcium on the electrical properties of squid axons , 1957, The Journal of physiology.

[158]  S. Waxman,et al.  Evoked potentials in suspected multiple sclerosis: Diagnostic value and prediction of clinical course , 1988, Journal of the Neurological Sciences.

[159]  P. Shrager,et al.  Resolving three types of chloride channels in demyelinated Xenopus axons , 1994, Journal of neuroscience research.

[160]  T. Guthrie Visual and motor changes in patients with multiple sclerosis; a result of induced changes in environmental temperature. , 1951, A.M.A. archives of neurology and psychiatry.

[161]  K. Burchiel Ectopic impulse generation in demyelinated axons: Effects of PaCO2, pH, and disodium edetate , 1981, Annals of neurology.

[162]  William H. Calvin,et al.  Can neuralgias arise from minor demyelination? Spontaneous firing, mechanosensitivity, and afterdischarge from conducting axons , 1982, Experimental Neurology.

[163]  C. Schauf,et al.  Plasmapheresis decreases neuroelectric blocking activity in multiple sclerosis , 1982, Neurology.

[164]  W. Mcdonald,et al.  Delayed visual evoked response in optic neuritis. , 1972, Lancet.

[165]  Hans Lassmann,et al.  Inflammatory central nervous system demyelination: Correlation of magnetic resonance imaging findings with lesion pathology , 1997, Annals of neurology.

[166]  J. C. Gardner,et al.  Multiple sclerosis lesions of the auditory pons are not silent. , 1994, Brain : a journal of neurology.

[167]  F. Barkhof,et al.  Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis , 1998, Neurology.

[168]  S. A. Wilson,et al.  Disorders of motility and muscle tone with special reference to the corpus striatum , 1925 .

[169]  T. Finger,et al.  Changed distribution of sodium channels along demyelinated axons. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[170]  W. Matthews,et al.  Paroxysmal symptoms in multiple sclerosis , 1975, Journal of the Neurological Sciences.

[171]  S G Waxman,et al.  Physiological effects of 4‐aminopyridine on demyelinated mammalian motor and sensory fibers , 1987, Annals of neurology.

[172]  S. K. Malhotra,et al.  Reactive astrocytes: cellular and molecular cues to biological function , 1997, Trends in Neurosciences.

[173]  C. Brosnan,et al.  Pathophysiologic effect of interleukin-1b in the rabbit retina. , 1990, The American journal of pathology.

[174]  C. Schauf,et al.  Impulse conduction in multiple sclerosis: a theoretical basis for modification by temperature and pharmacological agents , 1974, Journal of neurology, neurosurgery, and psychiatry.

[175]  M. Rasminsky Hyperexcitability of pathologically myelinated axons and positive symptoms in multiple sclerosis. , 1981, Advances in neurology.

[176]  P. Thompson,et al.  Propriospinal myoclonus in multiple sclerosis. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[177]  A. Thompson,et al.  Spinal cord atrophy and disability in multiple sclerosis. A new reproducible and sensitive MRI method with potential to monitor disease progression. , 1996, Brain : a journal of neurology.

[178]  B E Kendall,et al.  The role of NMR imaging in the assessment of multiple sclerosis and isolated neurological lesions. A quantitative study. , 1987, Brain : a journal of neurology.

[179]  Remyelination in multiple sclerosis , 1979, Annals of neurology.

[180]  C. Schauf,et al.  Disruption of the perineurium in amphibian peripheral nerve , 1980, Neurology.

[181]  William H. Calvin,et al.  A neurophysiological theory for the pain mechanism of tic douloureux , 1977, Pain.

[182]  W. Mcdonald,et al.  The longstanding MS lesion. A quantitative MRI and electron microscopic study. , 1991, Brain : a journal of neurology.

[183]  H. Bostock,et al.  Effects of 4-aminopyridine on normal and demyelinated mammalian nerve fibres , 1980, Nature.

[184]  R. Franklin,et al.  Requirements for schwann cell migration within cns environments: A viewpoint , 1993, International Journal of Developmental Neuroscience.

[185]  R. Kaji,et al.  Physiological consequences of antiserum-mediated experimental demyelination in CNS. , 1988, Brain : a journal of neurology.

[186]  D. I. Stephanova,et al.  Action potentials and ionic currents through paranodally demyelinated human motor nerve fibres: computer simulations , 1997, Biological Cybernetics.

[187]  J. Oger,et al.  Multiple sclerosis , 1988, Neurology.

[188]  J. Ulrich,et al.  The optic nerve in multiple sclerosis: A morphological study with retrospective clinico-pathological correlations , 1983 .

[189]  C. Bever,et al.  The effects of 4‐aminopyridine in multiple sclerosis patients , 1994, Neurology.

[190]  P. O. Osterman,et al.  Paroxysmal itching in multiple sclerosis , 1976, The British journal of dermatology.

[191]  N. Namerow Circadian temperature rhythm and vision in multiple sclerosis , 1968, Neurology.

[192]  Kenneth J. Smith,et al.  Conduction properties of central nerve fibers remyelinated by Schwann cells , 1992, Brain Research.

[193]  N. Geschwind,et al.  Major morbidity related to hyperthermia in multiple sclerosis , 1983, Annals of neurology.

[194]  S. Waxman Sodium channel blockade by antibodies: A new mechanism of neurological disease? , 1995, Annals of neurology.

[195]  T. Sears,et al.  Conduction failure in demyelination: is it inevitable? , 1981, Advances in neurology.

[196]  V. Lennon,et al.  Depression of complex bioelectric discharges in cerebral tissue cultures by thermolabile complement-dependent serum factors , 1975, Experimental Neurology.

[197]  K. Smith,et al.  Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. , 1997, Brain : a journal of neurology.

[198]  Karl J. Friston,et al.  Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction , 1993, Annals of neurology.

[199]  A. Paintal,et al.  The influence of diameter of medullated nerve fibres of cats on the rising and falling phases of the spike and its recovery , 1966, The Journal of physiology.

[200]  W. Blakemore,et al.  Dependence of axolemmal differentiation on contact with glial cells in chronically demyelinated lesions of cat spinal cord , 1985, Brain Research.

[201]  W. Mcdonald,et al.  Visual Evoked Response in Diagnosis of Multiple Sclerosis , 1973, British medical journal.

[202]  Z. Koles,et al.  A computer simulation of conduction in demyelinated nerve fibres , 1972, The Journal of physiology.

[203]  S. Aparicio,et al.  Anti-synaptic antibody in allergic encephalomyelitis II. The synapse-blocking effects in tissue culture of demyelinating sera from experimental allergic encephalomyelitis , 1975, Brain Research.

[204]  E. Uemura,et al.  Microglial release of nitric oxide by the synergistic action of β-amyloid and IFN-γ , 1995, Brain Research.

[205]  P. Grafe,et al.  Activity‐dependent excitability changes in normal and demyelinated rat spinal root axons. , 1985, The Journal of physiology.

[206]  R. Willison,et al.  The electromyogram in facial myokymia and hemifacial spasm. , 1973, Journal of the neurological sciences.

[207]  C. Woolf,et al.  Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor α , 1997, British journal of pharmacology.

[208]  A. Sumner,et al.  Effect of digitals on clinical symptoms and conduction variables in patients with multiple sclerosis , 1990, Annals of neurology.

[209]  J. M. Ritchie,et al.  Action potential conduction and sodium channel content in the optic nerve of the myelin-deficient rat , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[210]  T A Sears,et al.  The internodal axon membrane: electrical excitability and continuous conduction in segmental demyelination. , 1978, The Journal of physiology.

[211]  M. Schachner,et al.  Disruption and reorganization of sodium channels in experimental allergic neuritis , 1998, Muscle & nerve.

[212]  B E Kendall,et al.  The pathophysiology of acute optic neuritis. An association of gadolinium leakage with clinical and electrophysiological deficits. , 1991, Brain : a journal of neurology.

[213]  W. Young,et al.  Extracellular potassium activity and axonal conduction in spinal cord of the myelin-deficient mutant rat , 1989, Experimental Neurology.

[214]  W. Pryse-Phillips,et al.  Sudden Death in Multiple Sclerosis Associated with Sun Exposure: a Report of Two Cases , 1995, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[215]  F. Barkhof,et al.  Cortical lesions in multiple sclerosis. , 1999, Brain : a journal of neurology.

[216]  W. Mcdonald,et al.  Central remyelination restores secure conduction , 1979, Nature.

[217]  M. Mcdermott,et al.  Quantitative assessment of sustained‐release 4‐aminopyridine for symptomatic treatment of multiple sclerosis , 1997, Neurology.

[218]  Stephen G. Waxman,et al.  Demyelination in spinal cord injury , 1989, Journal of the Neurological Sciences.

[219]  Kenneth J. Smith,et al.  REVIEW ■ : Axonal Hyperexcitability: Mechanisms and Role in Symptom Production in Demyelinating Diseases , 1997 .

[220]  C. Rubinstein,et al.  Single channel characterization of multiple types of potassium channels in demyelinated Xenopus axons , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[221]  O. Bagasra,et al.  Activation of the inducible form of nitric oxide synthase in the brains of patients with multiple sclerosis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[222]  S. Waxman,et al.  Radial glia give rise to perinodal processes , 1991, Brain Research.