Cortical influences drive amyotrophic lateral sclerosis

Journal of Neurology, Neurosurgery and Psychiatry

Volumn 88, Issue 11, 2017, Pages 917-924

  Eisen, Andrew ^a   Braak, Heiko ^b   Del Tredici, Kelly ^b   Lemon, Roger ^c   Ludolph, Albert C ^b   Kiernan, Matthew C ^d  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF ULM   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Amyotrophic lateral sclerosis; corticomotoneuron; MRI; neuropathology; neurophysiology; proteinopathy; TDP 43

Indexed keywords

TAR DNA BINDING PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; BRAIN CORTEX; BULBAR PARALYSIS; CENTRAL NERVOUS SYSTEM; CORTICOMOTONEURONAL SYSTEM; DIFFUSION TENSOR IMAGING; FASCICULATION; FRONTOTEMPORAL DEMENTIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAIT; HUMAN; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROPHYSIOLOGY; OCULOMOTOR NERVE DISEASE; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY; SPLIT HAND SYNDROME; AXON; DISEASE COURSE; EARLY DIAGNOSIS; NERVE CELL INHIBITION; NERVE ENDING; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; NEUROIMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TDP-43 PROTEINOPATHIES; TRANSCRANIAL MAGNETIC STIMULATION;

AMYOTROPHIC LATERAL SCLEROSIS; AXONS; CEREBRAL CORTEX; DISEASE PROGRESSION; EARLY DIAGNOSIS; FRONTOTEMPORAL DEMENTIA; HUMANS; NEURAL INHIBITION; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEUROIMAGING; PRESYNAPTIC TERMINALS; TDP-43 PROTEINOPATHIES; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 85031668618     PISSN: 00223050     EISSN: 1468330X     Source Type: Journal    
DOI: 10.1136/jnnp-2017-315573     Document Type: Review

References (77)

1. Al-Chalabi A, Jones A, Troakes C, et al. The genetics and neuropathology of amyotrophic lateral sclerosis. Acta Neuropathol 2012;124:339-52.
2. Mackenzie IR, Neumann M, Bigio EH, et al. Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: consensus recommendations. Acta Neuropathol 2009; 117: 15-18
3. Buratti E, Romano M, Baralle FE. TDP-43 high throughput screening analyses in neurodegeneration: Advantages and pitfalls. Mol Cell Neurosci 2013;56:465-74.
4. Fallini C, Bassell GJ, Rossoll W. The ALS disease protein TDP-43 is actively transported in motor neuron axons and regulates axon outgrowth. Hum Mol Genet, 2012; 21: 3703-18
5. Braak H, Del Tredici K. Neuroanatomy and pathology of Sporadic Parkinsons disease. Adv Anat Embryol Cell Biol 2009;201:1-119.
6. Charcot J. Sclerose laterale amytrophique. Oeuvres Compltes. Bureaux du Proges Medical 1874;2:249-66
7. Kiernan JA, Hudson AJ. Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. Brain 1991;114 (Pt 2):843-53.
8. Eisen A, Calne D. Amyotrophic lateral sclerosis, Parkinsons disease and Alzheimersdisease: phylogenetic disorders of the human neocortex sharing many characteristics. Can J Neurol Sci 1992; 19: 117-23
9. Eisen A, Weber M. The motor cortex and amyotrophic lateral sclerosis. Muscle Nerve 2001;24:564-73.
10. Braak H, Brettschneider J, Ludolph AC, et al. Amyotrophic lateral sclerosis-A model of corticofugal axonal spread. Nat Rev Neurol 2013;9:708-14
11. Kiernan MC, Vucic S, Cheah BC, et al. Amyotrophic lateral sclerosis. Lancet 2011;377:942-55.
12. Welniarz Q, Dusart I, Roze E. The corticospinal tract: Evolution, development, and human disorders. Dev Neurobiol 2016
13. Isa T, Kinoshita M, Nishimura Y. Role of Direct vs. Indirect Pathways from the Motor Cortex to Spinal Motoneurons in the Control of Hand Dexterity. Front Neurol 2013;4:191.
14. Lemon RN. Descending pathways in motor control. Annu Rev Neurosci 2008;31:195-218
15. Lemon RN. What drives corticospinal output? F1000 Biol Rep 2010;2:51.
16. Muir RB, Lemon RN. Corticospinal neurons with a special role in precision grip. Brain Res 1983;261:312-6
17. Eisen A, Turner MR, Lemon R. Tools and talk: An evolutionary perspective on the functional deficits associated with amyotrophic lateral sclerosis. Muscle Nerve 2014;49:469-77.
18. Kuypers H. Anatomy of the descending pathways. In: Brookhart J, Mountcastle VB, eds. Handbook of Physiology-The Nervous System II American Physiological Society. Bethesda, MD, 1981: 597-666
19. Kuypers HG. Corticobular connexions to the pons and lower brain-stem in man: An anatomical study. Brain 1958;81:364-88.
20. Iwatsubo T, Kuzuhara S, Kanemitsu A, et al. Corticofugal projections to the motornuclei of the brainstem and spinal cord in humans. Neurology 1990;40:309-12
21. Rathelot JA, Strick PL. Subdivisions of primary motor cortex based on corticomotoneuronal cells. Proc Natl Acad Sci U S A 2009;106:918-23.
22. de Noordhout AM, Rapisarda G, Bogacz D, et al. Corticomotoneuronal synaptic connections in normal man: An electrophysiological study. Brain 1999;122 7:1327-40.
23. Barthélemy D, Grey MJ, Nielsen JB, et al. Involvement of the corticospinal tract in the control of human gait. Prog Brain Res 2011;192:181-97.
24. Fornia L, Ferpozzi V, Montagna M, et al. Functional Characterization of the Left Ventrolateral Premotor Cortex in Humans: A Direct Electrophysiological Approach. Cereb Cortex 2016.
25. Eisen A, Kuwabara S. The split hand syndrome in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2012;83:399-403.
26. Simon NG, Lee M, Bae JS, et al. Dissociated lower limb muscle involvement in amyotrophic lateral sclerosis. J Neurol 2015;262:1424-32.
27. Eisen A. Amyotrophic lateral sclerosis: A 40-year personal perspective. J Clin Neurosci 2009;16:505-12.
28. Petersen NC, Taylor JL, Murray NP, et al. Differential effects of low-intensity motor cortical stimulation on the inspiratory activity in scalene muscles during voluntary and involuntary breathing. Respir Physiol Neurobiol 2011;175:265-71.
29. Espadaler J, Rogić M, Deletis V, et al. Representation of cricothyroid muscles at the primary motor cortex (M1) in healthy subjects, mapped by navigated transcranial magnetic stimulation (nTMS). Clin Neurophysiol 2012;123:2205-11.
30. Simonyan K. The laryngeal motor cortex: its organization and connectivity. Curr Opin Neurobiol 2014;28:15-21.
31. Andersen PM. Mutation in C9orf72 changes the boundaries of ALS and FTD. Lancet Neurol 2012;11:205-7.
32. Phukan J, Pender NP, Hardiman O. Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurol 2007;6:994-1003.
33. Burrell JR, Halliday GM, Kril JJ, et al. The frontotemporal dementia-motor neuron disease continuum. Lancet 2016;388:919-31.
34. Eisen A, Lemon R, Kiernan MC, et al. Does dysfunction of the mirror neuron system contribute to symptoms in amyotrophic lateral sclerosis? Clin Neurophysiol 2015;126:1288-94.
35. Jelsone-Swain L, Persad C, Burkard D, et al. Action processing and mirror neuron function in patients with amyotrophic lateral sclerosis: An fMRI study. PLoS One 2015;10:e0119862.
36. Eisen A, Vucic S. Fasciculation potentials: A diagnostic biomarker of early ALS? J Neurol Neurosurg Psychiatry 2013;84:948.
37. de Carvalho M, Swash M. Physiology of the fasciculation potentials in amyotrophic lateral sclerosis: which motor units fasciculate? J Physiol Sci 2016.
38. Gorges M, Möller HP, Lulé D, et al. Eye Movement Deficits Are Consistent with a Staging Model of pTDP-43 Pathology in Amyotrophic Lateral Sclerosis. PLoS One 2015;10:e0142546.
39. Schall JD. Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. J Neurophysiol 1991;66:530-58.
40. Brettschneider J, Del Tredici K, Toledo JB, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 2013;74:20-38.
41. Vucic S, Ziemann U, Eisen A, et al. Transcranial magnetic stimulation and amyotrophic lateral sclerosis: pathophysiological insights. J Neurol Neurosurg Psychiatry 2013;84:1161-70.
42. Meyer BU, Röricht S, Gräfin von Einsiedel H, et al. Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. Brain 1995;118(Pt 2):429-40.
43. Menon P, Kiernan MC, Vucic S. Cortical hyperexcitability precedes lower motor neuron dysfunction in ALS. Clin Neurophysiol 2015;126:803-9.
44. Vucic S, Nicholson GA, Kiernan MC. Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain 2008;131:1540-50.
45. Vucic S, Lin CS, Cheah BC, et al. Riluzole exerts central and peripheral modulating effects in amyotrophic lateral sclerosis. Brain 2013;136:1361-70.
46. Vucic S, Nicholson GA, Kiernan MC. Cortical excitability in hereditary motor neuronopathy with pyramidal signs: comparison with ALS. J Neurol Neurosurg Psychiatry 2010;81:97-100.
47. Wittstock M, Wolters A, Benecke R. Transcallosal inhibition in amyotrophic lateral sclerosis. Clin Neurophysiol 2007;118:301-7.
48. Burrell JR, Kiernan MC, Vucic S, et al. Motor neuron dysfunction in frontotemporal dementia. Brain 2011;134:2582-94.
49. Eisen A, Kim S, Pant B, et al. ALS): A phylogenetic disease of the corticomotoneuron? Muscle Nerve 1992;15:219-24.
50. van Es MA, Van Vught PW, Blauw HM, et al. ITPR2 as a susceptibility gene in sporadic amyotrophic lateral sclerosis: A genome-wide association study. Lancet Neurol 2007;6:869-77.
51. Kwak S, Kawahara Y. Deficient RNA editing of GluR2 and neuronal death in amyotropic lateral sclerosis. J Mol Med 2005;83:110-20.
52. Braak H, Ludolph AC, Neumann M, et al. Pathological TDP-43 changes in Betz cells differ from those in bulbar and spinal á-motoneurons in sporadic amyotrophic lateral sclerosis. Acta Neuropathol 2017;133:79-90.
53. Böttner-Ennever JA. The extraocular motor nuclei: organization and functional neuroanatomy. Prog Brain Res 2006;151:95-125.
54. Firmin L, Field P, Maier MA, et al. Axon diameters and conduction velocities in the macaque pyramidal tract. J Neurophysiol 2014;112:1229-40.
55. Vigneswaran G, Kraskov A, Lemon RN. Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J Neurosci 2011;31:14235-42.
56. Soares D, Goldrick I, Lemon RN, et al. Expression of Kv3.1b potassium channel is widespread in macaque motor cortex pyramidal cells: A histological comparison between rat and macaque. J Comp Neurol. In Press. 2017;525:2164-74.
57. Smethurst P, Newcombe J, Troakes C, et al. In vitro prion-like behaviour of TDP-43 in ALS. Neurobiol Dis 2016;96:236-47.
58. Guo L, Shorter J. Biology and Pathobiology of TDP-43 and Emergent Therapeutic Strategies. Cold Spring Harb Perspect Med 2016:a024554.
59. Feiler MS, Strobel B, Freischmidt A, et al. TDP-43 is intercellularly transmitted across axon terminals. J Cell Biol 2015;211:897-911.
60. Stopschinski BE, Diamond MI. The prion model for progression and diversity of neurodegenerative diseases. Lancet Neurol 2017;16:323-32.
61. Bäumer D, Butterworth R, Menke RA, et al. Progressive hemiparesis (Mills syndrome) with aphasia in amyotrophic lateral sclerosis. Neurology 2014;82:457-8.
62. Tomasch J. The numerical capacity of the human cortico-pontocerebellar system. Brain Res 1969;13:476-84.
63. Menke RA, Agosta F, Grosskreutz J, et al. Neuroimaging endpoints in Amyotrophic Lateral Sclerosis. Neurotherapeutics 2017;14:11-23.
64. Schulthess I, Gorges M, Möller HP, et al. Functional connectivity changes resemble patterns of pTDP-43 pathology in amyotrophic lateral sclerosis. Sci Rep 2016;6:38391.
65. Turner MR, Agosta F, Bede P, et al. Neuroimaging in amyotrophic lateral sclerosis. Biomark Med 2012;6:319-37.
66. Agosta F, Valsasina P, Riva N, et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One 2012;7:e42816.
67. Chio A, Pagani M, Agosta F, et al. Neuroimaging in amyotrophic lateral sclerosis: insights into structural and functional changes. Lancet Neurol 2014;13:1228-40.
68. Kassubek J, Möller HP, Del Tredici K, et al. Diffusion tensor imaging analysis of sequential spreading of disease in amyotrophic lateral sclerosis confirms patterns of TDP-43 pathology. Brain 2014;137:1733-40.
69. V erstraete E, Veldink JH, van den Berg LH, et al. Structural brain network imaging shows expanding disconnection of the motor system in amyotrophic lateral sclerosis. Hum Brain Mapp 2014;35:1351-61.
70. Schmidt R, Verstraete E, de Reus MA, et al. Correlation between structural and functional connectivity impairment in amyotrophic lateral sclerosis. Hum Brain Mapp 2014;35:4386-95.
71. Turner MR, Bowser R, Bruijn L, et al. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 2013;14:19-32.
72. Philips T, Rothstein JD. Rodent models of Amyotrophic Lateral Sclerosis. Curr Protoc Pharmacol 2015;695:1-21.
73. Owen JP, Li YO, Ziv E, et al. The structural connectome of the human brain in agenesis of the corpus callosum. Neuroimage 2013;70:340-55.
74. Cookson MR. Evolution of neurodegeneration. Curr Biol 2012;22:R753-R761.
75. Uchida A, Sasaguri H, Kimura N, et al. Non-human primate model of amyotrophic lateral sclerosis with cytoplasmic mislocalization of TDP-43. Brain 2012;135:833-46.
76. Eisen A, Kiernan M, Mitsumoto H, et al. Amyotrophic lateral sclerosis: A long preclinical period? J Neurol Neurosurg Psychiatry 2014;85:1232-8.
77. Biane JS, Scanziani M, Tuszynski MH, et al. Motor cortex maturation is associated with reductions in recurrent connectivity among functional subpopulations and increases in intrinsic excitability. J Neurosci 2015;35:4719-28.