Dysfunctions within limbic-motor networks in amyotrophic lateral sclerosis

Neurobiology of Aging

Volumn 34, Issue 11, 2013, Pages 2499-2509

  Passamonti, Luca ^a   Fera, Francesco ^b   Tessitore, Alessandro ^c   Russo, Antonio ^c,d   Cerasa, Antonio ^a   Gioia, Cecilia M ^a   Monsurrò, Maria R ^c   Migliaccio, Raffaella ^c   Tedeschi, Gioacchino ^c   Quattrone, Aldo ^a,b  

^a INSTITUTE OF NEUROLOGICAL SCIENCES   (Italy)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d Istituto di Diagnosi e Cura IDC   (Italy)

Author keywords

Amygdala; Faces; FMRI; Motor neuron disease; Prefrontal cortex

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; AMYOTROPHIC LATERAL SCLEROSIS; ANXIETY; ARTICLE; BRAIN DYSFUNCTION; BRAIN FUNCTION; BRAIN REGION; CLINICAL ARTICLE; COGNITION; CONNECTOME; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE DURATION; DISEASE SEVERITY; EMOTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LIMBIC SYSTEM; MALE; MOTOR CONTROL; MOTOR SYSTEM; NEUROIMAGING; NEUROMODULATION; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIORITY JOURNAL; SUPPLEMENTARY MOTOR AREA;

AMYGDALA; FACES; FMRI; MOTOR NEURON DISEASE; PREFRONTAL CORTEX;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; BRAIN MAPPING; COGNITION DISORDERS; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LIMBIC SYSTEM; LINEAR MODELS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOOD DISORDERS; NEUROPSYCHOLOGICAL TESTS; OXYGEN;

EID: 84881541931     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.05.016     Document Type: Article

References (90)

1. Abdallah C.G., Coplan J.D., Jackowski A., Sato J.R., Mao X., Shungu D.C., Mathew S.J. Apilot study of hippocampal volume and N-acetylaspartate (NAA) as response biomarkers in riluzole-treated patients with GAD. Eur. Neuropsychopharmacol 2012, 2013 Apr;23:276-84.
2. Abrahams S., Goldstein L.H., Kew J.J., Brooks D.J., Lloyd C.M., Frith C.D., Leigh P.N. Frontal lobe dysfunction in amyotrophic lateral sclerosis. A PET study. Brain 1996, 119:2105-2120.
3. Abrahams S., Goldstein L.H., Suckling J., Ng V., Simmons A., Chitnis X., Atkins L., Williams S.C., Leigh P.N. Frontotemporal white matter changes in amyotrophic lateral sclerosis. J.Neurol. 2005, 252:321-331.
4. Diagnostic and Statistical Manual of Mental Disorders 1994, American Psychiatric Association, American Psychiatric Association, Washington, DC. fourth ed.
5. Applegate C.D., Kapp B.S., Underwood M.D., McNall C.L. Autonomic and somatomotor effects of amygdala central N. stimulation in awake rabbits. Physiol. Behav. 1983, 31:353-360.
6. Avendano C., Price J.L., Amaral D.G. Evidence for an amygdaloid projection to premotor cortex but not to motor cortex in the monkey. Brain. Res. 1983, 264:111-117.
7. Barbas H. Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci. Biobehav. Rev. 1995, 19:499-510.
8. Benton A.L., Hamsher K.D., Sivan A.B. Multilingual Aphasia Examination 1994, Iowa City, IA: AJA Associates.
9. Benton A.L., Varney N.R., Hamsher K.D. Visuospatial Judgment. A clinical test. Arch Neurol 1978, 35:364-367.
10. Bertolino A., Arciero G., Rubino V., Latorre V., De Candia M., Mazzola V., Blasi G., Caforio G., Hariri A., Kolachana B., Nardini M., Weinberger D.R., Scarabino T. Variation of human amygdala response during threatening stimuli as a function of 5'HTTLPR genotype and personality style. Biol. Psychiatry 2005, 57:1517-1525.
11. Best C.T., Womer J.S., Queen H.F. Hemispheric asymmetries in adults' perception of infant emotional expressions. J.Exp. Psychol. Hum. Percept. Perform. 1994, 20:751-765.
12. Brooks B.R., Miller R.G., Swash M., Munsat T.L. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2000, 1:293-299.
13. Bungener C., Piquard A., Pradat P.F., Salachas F., Meininger V., Lacomblez L. Psychopathology in amyotrophic lateral sclerosis: a preliminary study with 27 ALS patients. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2005, 6:221-225.
14. Canu E., Agosta F., Riva N., Sala S., Prelle A., Caputo D., Perini M., Comi G., Filippi M. The topography of brain microstructural damage in amyotrophic lateral sclerosis assessed using diffusion tensor MR imaging. AJNR Am. J. Neuroradiol. 2011, 32:1307-1314.
15. Carlson S., Martinkauppi S., Rama P., Salli E., Korvenoja A., Aronen H.J. Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. Cereb. Cortex 1998, 8:743-752.
16. Cavallo M., Adenzato M., Macpherson S.E., Karwig G., Enrici I., Abrahams S. Evidence of social understanding impairment in patients with amyotrophic lateral sclerosis. PLoS One 2011, 6:e25948.
17. Cedarbaum J.M., Stambler N., Malta E., Fuller C., Hilt D., Thurmond B., Nakanishi A. The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J.Neurol. Sci. 1999, 169:13-21.
18. Chang J.L., Lomen-Hoerth C., Murphy J., Henry R.G., Kramer J.H., Miller B.L., Gorno-Tempini M.L. Avoxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology 2005, 65:75-80.
19. Davidson R.J. Anterior cerebral asymmetry and the nature of emotion. Brain Cogn. 1992, 20:125-151.
20. Davidson R.J. Affective style, psychopathology, and resilience: brain mechanisms and plasticity. Am. Psychol. 2000, 55:1196-1214.
21. Davis M., Whalen P.J. The amygdala: vigilance and emotion. Mol. Psychiatry 2001, 6:13-34.
22. Delgado M.R., Olsson A., Phelps E.A. Extending animal models of fear conditioning to humans. Biol. Psychol. 2006, 73:39-48.
23. Fera F., Passamonti L., Cerasa A., Gioia M.C., Liguori M., Manna I., Valentino P., Quattrone A. The BDNF val(66)met polymorphism has opposite effects on memory circuits of multiple sclerosis patients and controls. PLoS One 2013, 8:e61063.
24. Friston K.J. Testing for anatomically specified regional effects. Hum. Brain Mapp. 1997, 5:133-136.
25. Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997, 6:218-229.
26. Friston K.J., Holmes A.P., Worsley K.J., Poline J.-P., Frith C.D., Frackowiak R.S.J. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 1994, 2:189-210.
27. Ghashghaei H.T., Barbas H. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 2002, 115:1261-1279.
28. Ghashghaei H.T., Hilgetag C.C., Barbas H. Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 2007, 34:905-923.
29. Gitelman D.R., Penny W.D., Ashburner J., Friston K.J. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 2003, 19:200-207.
30. Goldstein L.H., Newsom-Davis I.C., Bryant V., Brammer M., Leigh P.N., Simmons A. Altered patterns of cortical activation in ALS patients during attention and cognitive response inhibition tasks. J.Neurol. 2011, 258:2186-2198.
31. Groenewegen H.J., Wright C.I., Uylings H.B. The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. J.Psychopharmacol. 1997, 11:99-106.
32. Grossman A.B., Woolley-Levine S., Bradley W.G., Miller R.G. Detecting neurobehavioral changes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2007, 8:56-61.
33. Hamilton M. The assessment of anxiety states by rating. Br. J. Med. Psychol. 1959, 32:50-55.
34. Hariri A.R., Bookheimer S.Y., Mazziotta J.C. Modulating emotional responses: effects of a neocortical network on the limbic system. Neuroreport 2000, 11:43-48.
35. Hariri A.R., Goldberg T.E., Mattay V.S., Kolachana B.S., Callicott J.H., Egan M.F., Weinberger D.R. Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J.Neurosci. 2003, 23:6690-6694.
36. Hariri A.R., Tessitore A., Mattay V.S., Fera F., Weinberger D.R. The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage 2002, 17:317-323.
37. Kato S., Oda M., Hayashi H., Kawata A., Shimizu T. Participation of the limbic system and its associated areas in the dementia of amyotrophic lateral sclerosis. J.Neurol. Sci. 1994, 126:62-69.
38. Kawasaki H., Adolphs R., Oya H., Kovach C., Damasio H., Kaufman O., Howard M. Analysis of single-unit responses to emotional scenes in human ventromedial prefrontal cortex. J.Cogn. Neurosci. 2005, 17:1509-1518.
39. Kober H., Barrett L.F., Joseph J., Bliss-Moreau E., Lindquist K., Wager T.D. Functional grouping and cortical-subcortical interactions in emotion: a meta-analysis of neuroimaging studies. Neuroimage 2008, 42:998-1031.
40. Lang P.J., Davis M. Emotion, motivation, and the brain: reflex foundations in animal and human research. Prog. Brain Res. 2006, 156:3-29.
41. LeDoux J. The emotional brain, fear, and the amygdala. Cell Mol. Neurobiol. 2003, 23:727-738.
42. Leigh P.N., Simmons A., Williams S., Williams V., Turner M., Brooks D. Imaging: MRS/MRI/PET/SPECT: summary. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 2002, 3(suppl 1):S75-S80.
43. Li J., Pan P., Song W., Huang R., Chen K., Shang H. Ameta-analysis of diffusion tensor imaging studies in amyotrophic lateral sclerosis. Neurobiol. Aging 2012, 33:1833-1838.
44. Lomen-Hoerth C., Murphy J., Langmore S., Kramer J.H., Olney R.K., Miller B. Are amyotrophic lateral sclerosis patients cognitively normal?. Neurology 2003, 60:1094-1097.
45. Ludolph A.C., Langen K.J., Regard M., Herzog H., Kemper B., Kuwert T., Bottger I.G., Feinendegen L. Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol. Scand. 1992, 85:81-89.
46. Lulé D., Diekmann V., Anders S., Kassubek J., Kubler A., Ludolph A.C., Birbaumer N. Brain responses to emotional stimuli in patients with amyotrophic lateral sclerosis (ALS). J.Neurol. 2007, 254:519-527.
47. Lulé D., Diekmann V., Muller H.P., Kassubek J., Ludolph A.C., Birbaumer N. Neuroimaging of multimodal sensory stimulation in amyotrophic lateral sclerosis. J.Neurol. Neurosurg. Psychiatry 2010, 81:899-906.
48. Lulé D., Pauli S., Altintas E., Singer U., Merk T., Uttner I., Birbaumer N., Ludolph A.C. Emotional adjustment in amyotrophic lateral sclerosis (ALS). J.Neurol. 2012, 259:334-341.
49. Mohammadi B., Kollewe K., Samii A., Krampfl K., Dengler R., Munte T.F. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp. Neurol. 2009, 217:147-153.
50. Morecraft R.J., Stilwell-Morecraft K.S., Cipolloni P.B., Ge J., McNeal D.W., Pandya D.N. Cytoarchitecture and cortical connections of the anterior cingulate and adjacent somatomotor fields in the rhesus monkey. Brain Res. Bull. 2012, 87:457-497.
51. Mori H., Yagishita A., Takeda T., Mizutani T. Symmetric temporal abnormalities on MR imaging in amyotrophic lateral sclerosis with dementia. AJNR Am. J. Neuroradiol. 2007, 28:1511-1516.
52. Mumford J.A., Nichols T.E. Power calculation for group fMRI studies accounting for arbitrary design and temporal autocorrelation. Neuroimage 2008, 39:261-268.
53. Murphy J., Henry R., Lomen-Hoerth C. Establishing subtypes of the continuum of frontal lobe impairment in amyotrophic lateral sclerosis. Arch. Neurol. 2007, 64:330-334.
54. Murphy J.M., Henry R.G., Langmore S., Kramer J.H., Miller B.L., Lomen-Hoerth C. Continuum of frontal lobe impairment in amyotrophic lateral sclerosis. Arch. Neurol. 2007, 64:530-534.
55. Nachev P., Kennard C., Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat. Rev. Neurosci. 2008, 9:856-869.
56. Nelson H.E. Amodified card sorting test sensitive to frontal lobe defects. Cortex 1976, 12:313-324.
57. Olney N.T., Goodkind M.S., Lomen-Hoerth C., Whalen P.K., Williamson C.A., Holley D.E., Verstaen A., Brown L.M., Miller B.L., Kornak J., Levenson R.W., Rosen H.J. Behavior, physiology and experience of pathological laughing and crying in amyotrophic lateral sclerosis. Brain 2011, 134:3458-3469.
58. Olsson Ozanne A.G., Strang S., Persson L.I. Quality of life, anxiety and depression in ALS patients and their next of kin. J.Clin. Nurs. 2011, 20:283-291.
59. Palmieri A., Naccarato M., Abrahams S., Bonato M., D'Ascenzo C., Balestreri S., Cima V., Querin G., Dal Borgo R., Barachino L., Volpato C., Semenza C., Pegoraro E., Angelini C., Soraru G. Right hemisphere dysfunction and emotional processing in ALS: an fMRI study. J.Neurol 2010, 257:1970-1978.
60. Papps B., Abrahams S., Wicks P., Leigh P.N., Goldstein L.H. Changes in memory for emotional material in amyotrophic lateral sclerosis (ALS). Neuropsychologia 2005, 43:1107-1114.
61. Passamonti, L., Cerasa, A., Liguori, M., Gioia, M.C., Valentino, P., Nisticò, R., Quattrone, A., Fera, F. Neurobiological mechanisms underlying emotional processing in relapsing-remitting multiple sclerosis. Brain. 2009 Dec;132(Pt 12):3380-91. doi: 10.1093/brain/awp095.
62. Passingham R.E., Bengtsson S.L., Lau H.C. Medial frontal cortex: from self-generated action to reflection on one's own performance. Trends Cogn. Sci. 2010, 14:16-21.
63. Phan K.L., Wager T., Taylor S.F., Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002, 16:331-348.
64. Pichon S., de Gelder B., Grezes J. Emotional modulation of visual and motor areas by dynamic body expressions of anger. Soc. Neurosci. 2008, 3:199-212.
65. Pinkhardt E.H., van Elst L.T., Ludolph A.C., Kassubek J. Amygdala size in amyotrophic lateral sclerosis without dementia: an invivo study using MRI volumetry. BMC Neurol. 2006, 6:48.
66. Pouga L., Berthoz S., de Gelder B., Grezes J. Individual differences in socioaffective skills influence the neural bases of fear processing: the case of alexithymia. Hum. Brain Mapp. 2010, 31:1469-1481.
67. Raaphorst J., de Visser M., van Tol M.J., Linssen W.H., van der Kooi A.J., de Haan R.J., van den Berg L.H., Schmand B. Cognitive dysfunction in lower motor neuron disease: executive and memory deficits in progressive muscular atrophy. J.Neurol. Neurosurg. Psychiatry 2011, 82:170-175.
68. Rabkin J.G., Albert S.M., Del Bene M.L., O'Sullivan I., Tider T., Rowland L.P., Mitsumoto H. Prevalence of depressive disorders and change over time in late-stage ALS. Neurology 2005, 65:62-67.
69. Rey A. Memorisation d'une serie de 15 mots en 5 repetitions 1958, Paris: Presses Universitaries des France.
70. Ringholz G.M., Appel S.H., Bradshaw M., Cooke N.A., Mosnik D.M., Schulz P.E. Prevalence and patterns of cognitive impairment in sporadic ALS. Neurology 2005, 65:586-590.
71. Rippon G.A., Scarmeas N., Gordon P.H., Murphy P.L., Albert S.M., Mitsumoto H., Marder K., Rowland L.P., Stern Y. An observational study of cognitive impairment in amyotrophic lateral sclerosis. Arch. Neurol. 2006, 63:345-352.
72. Roesch M.R., Singh T., Brown P.L., Mullins S.E., Schoenbaum G. Ventral striatal neurons encode the value of the chosen action in rats deciding between differently delayed or sized rewards. J.Neurosci. 2009, 29:13365-13376.
73. Schmolck H., Mosnik D., Schulz P. Rating the approachability of faces in ALS. Neurology 2007, 69:2232-2235.
74. Shibasaki H., Hallett M. What is the Bereitschaftspotential?. Clin. Neurophysiol. 2006, 117:2341-2356.
75. Shiflett M.W., Balleine B.W. At the limbic-motor interface: disconnection of basolateral amygdala from nucleus accumbens core and shell reveals dissociable components of incentive motivation. Eur. J. Neurosci. 2010, 32:1735-1743.
76. Solari A., Motta A., Mendozzi L., Aridon P., Bergamaschi R., Ghezzi A., Mancardi G.L., Milanese C., Montanari E., Pucci E. Italian version of the Chicago multiscale depression inventory: translation, adaptation and testing in people with multiple sclerosis. Neurol. Sci. 2004, 24:375-383.
77. Sumner P., Nachev P., Morris P., Peters A.M., Jackson S.R., Kennard C., Husain M. Human medial frontal cortex mediates unconscious inhibition of voluntary action. Neuron 2007, 54:697-711.
78. Takeda T., Uchihara T., Chikugo T., Hiraga T., Kitaguchi M., Kojima H. Preferential involvement of the basolateral limbic circuit in an amyotrophic lateral sclerosis patient. Eur. J. Neurol. 2007, 14:e5-e6.
79. Takeda T., Uchihara T., Mochizuki Y., Mizutani T., Iwata M. Memory deficits in amyotrophic lateral sclerosis patients with dementia and degeneration of the perforant pathway: a clinicopathological study. J.Neurol. Sci. 2007, 260:225-230.
80. Tedeschi G., Trojsi F., Tessitore A., Corbo D., Sagnelli A., Paccone A., D'Ambrosio A., Piccirillo G., Cirillo M., Cirillo S., Monsurro M.R., Esposito F. Interaction between aging and neurodegeneration in amyotrophic lateral sclerosis. Neurobiol. Aging 2012, 33:886-898.
81. Tsujimoto M., Senda J., Ishihara T., Niimi Y., Kawai Y., Atsuta N., Watanabe H., Tanaka F., Naganawa S., Sobue G. Behavioral changes in early ALS correlate with voxel-based morphometry and diffusion tensor imaging. J.Neurol. Sci. 2011, 307:34-40.
82. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
83. Vignola A., Guzzo A., Calvo A., Moglia C., Pessia A., Cavallo E., Cammarosano S., Giacone S., Ghiglione P., Chio A. Anxiety undermines quality of life in ALS patients and caregivers. Eur. J. Neurol. 2008, 15:1231-1236.
84. Voon V., Brezing C., Gallea C., Ameli R., Roelofs K., LaFrance W.C., Hallett M. Emotional stimuli and motor conversion disorder. Brain 2010, 133:1526-1536.
85. Voon V., Brezing C., Gallea C., Hallett M. Aberrant supplementary motor complex and limbic activity during motor preparation in motor conversion disorder. Mov. Disord. 2011, 26:2396-2403.
86. Wicks P., Abrahams S., Masi D., Hejda-Forde S., Leigh P.N., Goldstein L.H. Prevalence of depression in a 12-month consecutive sample of patients with ALS. Eur. J. Neurol. 2007, 14:993-1001.
87. Witgert M., Salamone A.R., Strutt A.M., Jawaid A., Massman P.J., Bradshaw M., Mosnik D., Appel S.H., Schulz P.E. Frontal-lobe mediated behavioral dysfunction in amyotrophic lateral sclerosis. Eur. J. Neurol. 2010, 17:103-110.
88. Worsley K.J., Marrett S., Neelin P., Vandal A.C., Friston K.J., Evans A.C. Aunified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 1996, 4:58-73.
89. Xue G., Aron A.R., Poldrack R.A. Common neural substrates for inhibition of spoken and manual responses. Cereb. Cortex 2008, 18:1923-1932.
90. Zimmerman E.K., Eslinger P.J., Simmons Z., Barrett A.M. Emotional perception deficits in amyotrophic lateral sclerosis. Cogn. Behav. Neurol. 2007, 20:79-82.