Does dysfunction of the mirror neuron system contribute to symptoms in amyotrophic lateral sclerosis?

Clinical Neurophysiology

Volumn 126, Issue 7, 2015, Pages 1288-1294

  Eisen, Andrew ^a   Lemon, Roger ^b   Kiernan, Matthew C ^c   Hornberger, Michael ^d   Turner, Martin R ^e  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF SYDNEY   (Australia)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Amyotrophic lateral sclerosis; Cognition; Empathy; Mirror neurons; Motor cortex

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; ANTERIOR CINGULATE; CELL FUNCTION; CELL MATURATION; CEREBELLUM; EMPATHY; EVOLUTIONARY ADAPTATION; FINGER; FRONTAL VARIANT FRONTOTEMPORAL DEMENTIA; FRONTOTEMPORAL DEMENTIA; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAIT; GESTURE; HAND FUNCTION; HAPLORHINI; HUMAN; IMAGERY; INFERIOR PARIETAL LOBULE; LANGUAGE; MEDIAL PREFRONTAL CORTEX; MIRROR NEURON; MOTONEURON; MOTOR CONTROL; NEOCORTEX; NONHUMAN; OBJECT MANIPULATION; PREFRONTAL CORTEX; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL TRACT; RESPIRATORY FAILURE; REVIEW; RIGIDITY; SOCIAL INTERACTION; SUPPLEMENTARY MOTOR AREA; WALKING; COGNITION; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPEECH;

AMYOTROPHIC LATERAL SCLEROSIS; COGNITION; EMPATHY; GAIT; HUMANS; MIRROR NEURONS; MOTOR ACTIVITY; PYRAMIDAL TRACTS; SPEECH;

EID: 84930538491     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2015.02.003     Document Type: Review

References (95)

1. Acharya S., Shukla S. Mirror neurons: enigma of the metaphysical modular brain. J Nat Sci Biol Med 2012, 3:118-124.
2. Alegre M., Guridi J., Artieda J. The mirror system, theory of mind and Parkinson's disease. J Neurol Sci 2011, 310:194-196.
3. Allali G., van der Meulen M., Beauchet O., Rieger S.W., Vuilleumier P., Assal F. The neural basis of age-related changes in motor imagery of gait: an FMRI study. J Gerontol A Biol Sci Med Sci 2014, 69:1389-1398.
4. Arbib M.A., Liebal K., Pika S. Primate vocalization, gesture, and the evolution of human language. Curr Anthropol 2008, 49:1053-1063. [discussion 63-76].
5. Arias M. Neurology of laughter and humour: pathological laughing and crying. Rev Neurol 2011, 53:415-421.
6. Ash S., Menaged A., Olm C., McMillan C.T., Boller A., Irwin D.J., et al. Narrative discourse deficits in amyotrophic lateral sclerosis. Neurology 2014, 83:520-528.
7. Bae J.S., Menon P., Mioshi E., Kiernan M.C., Vucic S. Cortical hyperexcitability and the split-hand plus phenomenon: pathophysiological insights in ALS. Amyotroph Lateral Scler Frontotemporal Degener 2014, 15:250-256.
8. Berenbaum S.A., Abrams R., Rosenberg S., Taylor M.A. The nature of emotional blunting: a factor-analytic study. Psychiatry Res 1987, 20:57-67.
9. Bonini L., Ferrari P.F. Evolution of mirror systems: a simple mechanism for complex cognitive functions. Ann N Y Acad Sci 2011, 1225:166-175.
10. Braadbaart L., Williams J.H., Waiter G.D. Do mirror neuron areas mediate mu rhythm suppression during imitation and action observation?. Int J Psychophysiol 2013, 89:99-105.
11. Caggiano V., Fogassi L., Rizzolatti G., Casile A., Giese M.A., Thier P. Mirror neurons encode the subjective value of an observed action. Proc Natl Acad Sci U S A 2012, 109:11848-11853.
12. Cartmill E.A., Beilock S., Goldin-Meadow S. A word in the hand: action, gesture and mental representation in humans and non-human primates. Philos Trans R Soc Lond B Biol Sci 2012, 367:129-143.
13. Casile A. Mirror neurons (and beyond) in the macaque brain: An overview of 20years of research. Neurosci Lett 2013, 540:3-14.
14. Casile A., Caggiano V., Ferrari P.F. The mirror neuron system: a fresh view. Neuroscientist 2011, 17:524-538.
15. Cerami C., Dodich A., Canessa N., Crespi C., Iannaccone S., Corbo M., et al. Emotional empathy in amyotrophic lateral sclerosis: a behavioural and voxel-based morphometry study. Amyotroph Lateral Scler Frontotemporal Degener 2014, 15:21-29.
16. Cinelli E., Robertson B., Mutolo D., Grillner S., Pantaleo T., Bongianni F. Neuronal mechanisms of respiratory pattern generation are evolutionary conserved. J Neurosci 2013, 33:9104-9112.
17. Clark H.M., Duffy J.R., Whitwell J.L., Ahlskog J.E., Sorenson E.J., Josephs K.A. Clinical and imaging characterization of progressive spastic dysarthria. Eur J Neurol 2014, 21:368-376.
18. Corballis M.C. Mirror neurons and the evolution of language. Brain Lang 2010, 112:25-35.
19. Corradini A., Antonietti A. Mirror neurons and their function in cognitively understood empathy. Conscious Cogn 2013, 22:1152-1161.
20. Csibra G. Goal attribution to inanimate agents by 6.5-month-old infants. Cognition 2008, 107:705-717.
21. Danion F., Sarlegna F.R. Can the human brain predict the consequences of arm movement corrections when transporting an object? Hints from grip force adjustments. J Neurosci 2007, 27:12839-12843.
22. Decety J. The neuroevolution of empathy. Ann N Y Acad Sci 2011, 1231:35-45.
23. Decety J., Svetlova M. Putting together phylogenetic and ontogenetic perspectives on empathy. Dev Cogn Neurosci 2012, 2:1-24.
24. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., et al. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
25. Del Giudice M., Manera V., Keysers C. Programmed to learn? The ontogeny of mirror neurons. Dev Sci 2009, 12:350-363.
26. Eisen A., Kiernan M., Mitsumoto H., Swash M. Amyotrophic lateral sclerosis: a long preclinical period?. J Neurol Neurosurg Psychiatry 2014, 85:1232-1238.
27. Eisen A., Kuwabara S. The split hand syndrome in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 2012, 83:399-403.
28. Eisen A., Turner M.R., Lemon R. Tools and talk: an evolutionary perspective on the functional deficits associated with amyotrophic lateral sclerosis. Muscle Nerve 2014, 49:469-477.
29. Elamin M., Pender N., Hardiman O., Abrahams S. Social cognition in neurodegenerative disorders: a systematic review. J Neurol Neurosurg Psychiatry 2012, 83:1071-1079.
30. Enticott P.G., Kennedy H.A., Bradshaw J.L., Rinehart N.J., Fitzgerald P.B. Understanding mirror neurons: evidence for enhanced corticospinal excitability during the observation of transitive but not intransitive hand gestures. Neuropsychologia 2010, 48:2675-2680.
31. Ferrari P.F., Tramacere A., Simpson E.A., Iriki A. Mirror neurons through the lens of epigenetics. Trends Cogn Sci 2013, 17:450-457.
32. Filippi M., Agosta F., Scola E., Canu E., Magnani G., Marcone A., et al. Functional network connectivity in the behavioral variant of frontotemporal dementia. Cortex 2013, 49:2389-2401.
33. Fiori F., Sedda A., Ferre E.R., Toraldo A., Querzola M., Pasotti F., et al. Exploring motor and visual imagery in amyotrophic lateral sclerosis. Exp Brain Res 2013, 226:537-547.
34. Gatti R., Tettamanti A., Gough P.M., Riboldi E., Marinoni L., Buccino G. Action observation versus motor imagery in learning a complex motor task: a short review of literature and a kinematics study. Neurosci Lett 2013, 540:37-42.
35. Gentilucci M., Benuzzi F., Gangitano M., Grimaldi S. Grasp with hand and mouth: a kinematic study on healthy subjects. J Neurophysiol 2001, 86:1685-1699.
36. Gentilucci M., Dalla Volta R. Spoken language and arm gestures are controlled by the same motor control system. Q J Exp Psychol (Hove) 2008, 61:944-957.
37. Gentilucci M., Dalla Volta R., Gianelli C. When the hands speak. J Physiol Paris 2008, 102:21-30.
38. Girardi A., Macpherson S.E., Abrahams S. Deficits in emotional and social cognition in amyotrophic lateral sclerosis. Neuropsychology 2011, 25:53-65.
39. Hamilton A.F. Reflecting on the mirror neuron system in autism: a systematic review of current theories. Dev Cogn Neurosci 2013, 3:91-105.
40. Hardiman O., van den Berg L.H., Kiernan M.C. Clinical diagnosis and management of amyotrophic lateral sclerosis. Nat Rev Neurol 2011, 7:639-649.
41. Hickok G. The myth of mirror neurons: the real neuroscience of communication and cognition 2014, W.W. Norton.
42. Hickok G., Rogalsky C., Chen R., Herskovits E.H., Townsley S., Hillis A.E. Partially overlapping sensorimotor networks underlie speech praxis and verbal short-term memory: evidence from apraxia of speech following acute stroke. Front Hum Neurosci 2014, 8:649.
43. Higginbotham D.R., Isaak M.I., Domingue J.N. The exaptation of manual dexterity for articulate speech: an electromyogram investigation. Exp Brain Res 2008, 186:603-609.
44. Hornberger M., Yew B., Gilardoni S., Mioshi E., Gleichgerrcht E., Manes F., et al. Ventromedial-frontopolar prefrontal cortex atrophy correlates with insight loss in frontotemporal dementia and Alzheimer's disease. Hum Brain Mapp 2014, 35:616-626.
45. Johansson R.S., Westling G. Programmed and triggered actions to rapid load changes during precision grip. Exp Brain Res 1988, 71:72-86.
46. Kable J.W., Kan I.P., Wilson A., Thompson-Schill S.L., Chatterjee A. Conceptual representations of action in the lateral temporal cortex. J Cogn Neurosci 2005, 17:1855-1870.
47. Kiernan M.C., Vucic S., Cheah B.C., Turner M.R., Eisen A., Hardiman O., et al. Amyotrophic lateral sclerosis. Lancet 2011, 377:942-955.
48. Kilner J.M., Friston K.J., Frith C.D. Predictive coding: an account of the mirror neuron system. Cogn Process 2007, 8:159-166.
49. Kim J.H., Lee B.H. Action observation training for functional activities after stroke: a pilot randomized controlled trial. NeuroRehabilitation 2013, 33:565-574.
50. Kraskov A., Philipp R., Waldert S., Vigneswaran G., Quallo M.M., Lemon R.N. Corticospinal mirror neurons. Philos Trans R Soc Lond B Biol Sci 2014, 369:20130174.
51. Lamm C., Decety J., Singer T. Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 2011, 54:2492-2502.
52. Lemon R.N. What drives corticospinal output?. F1000 Biol Rep 2010, 2:51.
53. Lemon R.N., Mantel G.W., Muir R.B. Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. J Physiol 1986, 381:497-527.
54. Levy R., Dubois B. Apathy and the functional anatomy of the prefrontal cortex-basal ganglia circuits. Cereb Cortex 2006, 16:916-928.
55. Lillo P., Mioshi E., Zoing M.C., Kiernan M.C., Hodges J.R. How common are behavioural changes in amyotrophic lateral sclerosis?. Amyotroph Lateral Scler 2011, 12:45-51.
56. Lillo P., Savage S., Mioshi E., Kiernan M.C., Hodges J.R. Amyotrophic lateral sclerosis and frontotemporal dementia: a behavioural and cognitive continuum. Amyotroph Lateral Scler 2012, 13:102-109.
57. Lough S., Kipps C.M., Treise C., Watson P., Blair J.R., Hodges J.R. Social reasoning, emotion and empathy in frontotemporal dementia. Neuropsychologia 2006, 44:950-958.
58. Lule D., Diekmann V., Kassubek J., Kurt A., Birbaumer N., Ludolph A.C., et al. Cortical plasticity in amyotrophic lateral sclerosis: motor imagery and function. Neurorehabil Neural Repair 2007, 21:518-526.
59. Maclarnon A., Hewitt G. Increased breathing control: another factor in the evolution of human language. Evol Anthropol 2004, 13:181-197.
60. Maier M.A., Bennett K.M., Hepp-Reymond M.C., Lemon R.N. Contribution of the monkey corticomotoneuronal system to the control of force in precision grip. J Neurophysiol 1993, 69:772-785.
61. Marshall J. Mirror neurons. Proc Natl Acad Sci U S A 2014, 111:6531.
62. Mefferd A.S., Pattee G.L., Green J.R. Speaking rate effects on articulatory pattern consistency in talkers with mild ALS. Clin Linguist Phon 2014, 28:799-811.
63. Mehta U.M., Thirthalli J., Basavaraju R., Gangadhar B.N., Pascual-Leone A. Reduced mirror neuron activity in schizophrenia and its association with theory of mind deficits: evidence from a transcranial magnetic stimulation study. Schizophr Bull 2014, 40:1083-1094.
64. Menon P., Bae J.S., Mioshi E., Kiernan M.C., Vucic S. Split-hand plus sign in ALS: differential involvement of the flexor pollicis longus and intrinsic hand muscles. Amyotroph Lateral Scler Frontotemporal Degener 2013, 14:315-318.
65. Mukamel R., Ekstrom A.D., Kaplan J., Iacoboni M., Fried I. Single-neuron responses in humans during execution and observation of actions. Curr Biol 2010, 20:750-756.
66. Piguet O., Hornberger M., Mioshi E., Hodges J.R. Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management. Lancet Neurol 2011, 10:162-172.
67. Pinto S., Carvalho M. Breathing new life into treatment advances for respiratory failure in amyotrophic lateral sclerosis patients. Neurodegener Dis Manag 2014, 4:83-102.
68. Plata Bello J., Modrono C., Marcano F., Gonzalez-Mora J.L. The mirror neuron system and motor dexterity: what happens?. Neuroscience 2014, 275:285-295.
69. Rascovsky K., Hodges J.R., Knopman D., Mendez M.F., Kramer J.H., Neuhaus J., et al. Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 2011, 134:2456-2477.
70. Renfrew C. Neuroscience, evolution and the sapient paradox: the factuality of value and of the sacred. Philos Trans R Soc Lond B Biol Sci 2008, 363:2041-2047.
71. Renton A.E., Majounie E., Waite A., Simon-Sanchez J., Rollinson S., Gibbs J.R., et al. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
72. Rizzolatti G., Fabbri-Destro M., Cattaneo L. Mirror neurons and their clinical relevance. Nat Clin Pract Neurol 2009, 5:24-34.
73. Rizzolatti G., Sinigaglia C. Mirrors in the Brain: How our minds share actions, emotions and experience 2008, Oxford University Press, Oxford, UK.
74. Rosen H.J., Gorno-Tempini M.L., Goldman W.P., Perry R.J., Schuff N., Weiner M., et al. Patterns of brain atrophy in frontotemporal dementia and semantic dementia. Neurology 2002, 58:198-208.
75. Sato K., Morimoto N., Deguchi K., Ikeda Y., Matsuura T., Abe K. Seven amyotrophic lateral sclerosis patients diagnosed only after development of respiratory failure. J Clin Neurosci 2014, 21:1341-1343.
76. Saxe R. Uniquely human social cognition. Curr Opin Neurobiol 2006, 16:235-239.
77. Schieber M.H. Dissociating motor cortex from the motor. J Physiol 2011, 589:5613-5624.
78. Serrien D.J., Kaluzny P., Wicki U., Wiesendanger M. Grip force adjustments induced by predictable load perturbations during a manipulative task. Exp Brain Res 1999, 124:100-106.
79. Shamay-Tsoory S.G., Tomer R., Goldsher D., Berger B.D., Aharon-Peretz J. Impairment in cognitive and affective empathy in patients with brain lesions: anatomical and cognitive correlates. J Clin Exp Neuropsychol 2004, 26:1113-1127.
80. Shibuya K., Misawa S., Nasu S., Sekiguchi Y., Mitsuma S., Beppu M., et al. Split hand syndrome in amyotrophic lateral sclerosis: different excitability changes in the thenar and hypothenar motor axons. J Neurol Neurosurg Psychiatry 2013, 84:969-972.
81. Singer T. The neuronal basis and ontogeny of empathy and mind reading: review of literature and implications for future research. Neurosci Biobehav Rev 2006, 30:855-863.
82. Snowden J.S., Harris J., Richardson A., Rollinson S., Thompson J.C., Neary D., et al. Frontotemporal dementia with amyotrophic lateral sclerosis: a clinical comparison of patients with and without repeat expansions in C9orf72. Amyotroph Lateral Scler Frontotemporal Degener 2013, 14:172-176.
83. Stanton B.R., Williams V.C., Leigh P.N., Williams S.C., Blain C.R., Giampietro V.P., et al. Cortical activation during motor imagery is reduced in amyotrophic lateral sclerosis. Brain Res 2007, 1172:145-151.
84. Strong M.J. The syndromes of frontotemporal dysfunction in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 2008, 9:323-338.
85. Stuss D.T., Alexander M.P. Executive functions and the frontal lobes: a conceptual view. Psychol Res 2000, 63:289-298.
86. Thomsen G.M., Gowing G., Latter J., Chen M., Vit J.P., Staggenborg K., et al. Delayed disease onset and extended survival in the SOD1G93A rat model of amyotrophic lateral sclerosis after suppression of mutant SOD1 in the motor cortex. J Neurosci 2014, 34:15587-15600.
87. Trimble M. Why humans like to cry - tragedy evolution, and the brain 2012, Oxford University Press, Oxford.
88. Uddin L.Q., Iacoboni M., Lange C., Keenan J.P. The self and social cognition: the role of cortical midline structures and mirror neurons. Trends Cogn Sci 2007, 11:153-157.
89. Venkadesan M., Valero-Cuevas F.J. Neural control of motion-to-force transitions with the fingertip. J Neurosci 2008, 28:1366-1373.
90. Vigneswaran G., Philipp R., Lemon R.N., Kraskov A. M1 corticospinal mirror neurons and their role in movement suppression during action observation. Curr Biol 2013, 23:236-243.
91. Virji-Babul N., Rose A., Moiseeva N., Makan N. Neural correlates of action understanding in infants: influence of motor experience. Brain Behav 2012, 2:237-242.
92. Vucic S., Kiernan M.C. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain 2006, 129:2436-2446.
93. Wang C., Wai Y., Kuo B., Yeh Y.Y., Wang J. Cortical control of gait in healthy humans: an fMRI study. J Neural Transm 2008, 115:1149-1158.
94. Weber M., Eisen A., Stewart H., Hirota N. The split hand in ALS has a cortical basis. J Neurol Sci 2000, 180:66-70.
95. Zaki J., Ochsner K.N. The neuroscience of empathy: progress, pitfalls and promise. Nat Neurosci 2012, 15:675-680.