Effects of cerebellar lesions on working memory interacting with motor tasks of different complexities

Journal of Neurophysiology

Volumn 110, Issue 10, 2013, Pages 2337-2349

  Ilg, Winfried ^a   Christensen, Andrea ^a   Mueller, Oliver M ^b   Goericke, Sophia L ^b   Giese, Martin A ^a   Timmann, Dagmar ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

Cerebellum; Dual task; Gait; Lesion symptom mapping; Working memory

Indexed keywords

ADULT; ARTICLE; ATAXIA; BRAIN MAPPING; BRAIN REGION; CEREBELLUM INJURY; CEREBELLUM TUMOR; CLINICAL ARTICLE; COGNITION; CONTROLLED STUDY; DENTATE NUCLEUS; DISEASE SEVERITY; FEMALE; GAIT; HEMISPHERE; HUMAN; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; TREADMILL EXERCISE; VOXEL BASED MORPHOMETRY; WALKING; WORKING MEMORY;

CEREBELLUM; DUAL TASK; GAIT; LESION-SYMPTOM MAPPING; WORKING MEMORY;

ADOLESCENT; ADULT; CEREBELLAR ATAXIA; CEREBELLUM; FEMALE; GAIT ATAXIA; HUMANS; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; MOVEMENT; PSYCHOMOTOR PERFORMANCE; YOUNG ADULT;

EID: 84887592689     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00062.2013     Document Type: Article

References (67)

1. Al-Yahya E, Dawes H, Smith L, Dennis A, Howells K, Cockburn J. Cognitive motor interference while walking: a systematic review and metaanalysis. Neurosci Biobehav Rev 35: 715-728, 2011.
2. Asanuma C, Thach WR, Jones EG. Anatomical evidence for segregated focal groupings of efferent cells and their terminal ramifications in the cerebellothalamic pathway of the monkey. Brain Res 286: 267-297, 1983.
3. Bates E, Wilson SM, Saygin AP, Dick F, Sereno MI, Knight RT, Dronkers NF. Voxel-based lesion-symptom mapping. Nat Neurosci 6: 448-450, 2003.
4. Bernard JA, Peltier SJ, Benson BL, Wiggins JL, Jaeggi SM, Buschkuehl M, Jonides J, Monk CS, Seidler RD. Dissociable functional networks of the human dentate nucleus. Cereb Cortex. In press.
5. Bloem BR, Valkenburg VV, Slabbekoorn M, van Dijk JG. The multiple tasks test. Strategies in Parkinson's disease. Exp Brain Res 137: 478-486, 2001.
6. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106: 2322-2345, 2011.
7. Cerminara NL, Edge AL, Marple-Horvat DE, Apps R. The lateral cerebellum and visuomotor control. Prog Brain Res 148: 213-226, 2005.
8. Cooper FE, Grube M, Von Kriegstein K, Kumar S, English P, Kelly TP, Chinnery PF, Griffiths TD. Distinct critical cerebellar subregions for components of verbal working memory. Neuropsychologia 50: 189-197, 2012.
9. Cooper SE, Martin JH, Ghez C. Effects of inactivation of the anterior interpositus nucleus on the kinematic and dynamic control of multijoint movement. J Neurophysiol 84: 1988-2000, 2000.
10. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage 33: 127-138, 2006.
11. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage 46: 39-46, 2009.
12. Diedrichsen J, Maderwald S, Kuper M, Thurling M, Rabe K, Gizewski ER, Ladd ME, Timmann D. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage 54: 1786-1794, 2011.
13. Diener HC, Dichgans J. Cerebellar and spinocerebellar gait disorders. In: Clinical Disorders of Balance, Posture and Gait, edited by Bronstein AM, Brandt T, and Woollacott. London: Arnold, 1996, p. 147-155.
14. Dobbs AR, Rule BG. Adult age differences in working memory. Psychol Aging 4: 500-503, 1989.
15. Donchin O, Rabe K, Diedrichsen J, Lally N, Schoch B, Gizewski ER, Timmann D. Cerebellar regions involved in adaptation to force field and visuomotor perturbation. J Neurophysiol 107: 134-147, 2012.
16. Doyon J, Laforce R Jr, Bouchard G, Gaudreau D, Roy J, Poirier M, Bedard PJ, Bedard F, Bouchard JP. Role of the striatum, cerebellum and frontal lobes in the automatization of a repeated visuomotor sequence of movements. Neuropsychologia 36: 625-641, 1998.
17. Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol 89: 634-639, 2003.
18. Evrard HC, Craig AD. Retrograde analysis of the cerebellar projections to the posteroventral part of the ventral lateral thalamic nucleus in the macaque monkey. J Comp Neurol 508: 286-314, 2008.
19. Haggard P, Cockburn J, Cock J, Fordham C, Wade D. Interference between gait and cognitive tasks in a rehabilitating neurological population. J Neurol Neurosurg Psychiatry 69: 479-486, 2000.
20. Hautzel H, Mottaghy FM, Specht K, Muller HW, Krause BJ. Evidence of a modality-dependent role of the cerebellum in working memory? An fMRI study comparing verbal and abstract n-back tasks. Neuroimage 47: 2073-2082, 2009.
21. Holmes G. The cerebellum of man. Brain 62: 1-30, 1939.
22. Ilg W, Giese MA, Gizewski ER, Schoch B, Timmann D. The influence of focal cerebellar lesions on the control and adaptation of gait. Brain 131: 2913-2927, 2008.
23. Ilg W, Golla H, Thier P, Giese MA. Specific influences of cerebellar dysfunctions on gait. Brain 130: 786-798, 2007.
24. Ilg W, Synofzik M, Brötz D, Burkard S, Giese MA, Schöls L. Intensive coordinative training improves motor performance in degenerative cerebellar disease. Neurology 73: 1823-1830, 2009.
25. Ilg W, Timmann D. Gait ataxia-specific cerebellar influences and their rehabilitation. Mov Disord In press.
26. Ito M. Control of mental activities by internal models in the cerebellum. Nat Rev Neurosci 9: 304-313, 2008.
27. Konczak J, Schoch B, Dimitrova A, Gizewski E, Timmann D. Functional recovery of children and adolescents after cerebellar tumour resection. Brain 128: 1428-1441, 2005.
28. Kuper M, Dimitrova A, Thurling M, Maderwald S, Roths J, Elles HG, Gizewski ER, Ladd ME, Diedrichsen J, Timmann D. Evidence for a motor and a non-motor domain in the human dentate nucleus-an fMRI study. Neuroimage 54: 2612-2622, 2011a.
29. Kuper M, Thurling M, Stefanescu R, Maderwald S, Roths J, Elles HG, Ladd ME, Diedrichsen J, Timmann D. Evidence for a motor somatotopy in the cerebellar dentate nucleus-an fMRI study in humans. Hum Brain Mapp 2011b.
30. Lang CE, Bastian AJ. Cerebellar damage impairs automaticity of a recently practiced movement. J Neurophysiol 87: 1336-1347, 2002.
31. Lindenberger U, Marsiske M, Baltes PB. Memorizing while walking: increase in dual-task costs from young adulthood to old age. Psychol Aging 15: 417-436, 2000.
32. Marvel CL, Desmond JE. From storage to manipulation: How the neural correlates of verbal working memory reflect varying demands on inner speech. Brain Lang 120: 42-51, 2012.
33. Marvel CL, Desmond JE. Functional topography of the cerebellum in verbal working memory. Neuropsychol Rev 20: 271-279, 2011.
34. Miyai I, Ito M, Hattori N, Mihara M, Hatakenaka M, Yagura H, Sobue G, Nishizawa M. Cerebellar ataxia rehabilitation trial in degenerative cerebellar diseases. Neurorehabil Neural Repair 26: 515-522, 2012.
35. Morton SM, Bastian AJ. Cerebellar control of balance and locomotion. Neuroscientist 10: 247-259, 2004.
36. Morton SM, Bastian AJ. Relative contributions of balance and voluntary legcoordination deficits to cerebellar gait ataxia. J Neurophysiol 89: 1844-1856, 2003.
37. Owen AM, McMillan KM, Laird AR, Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25: 46-59, 2005.
38. Prevosto V, Graf W, Ugolini G. Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. Cereb Cortex 20: 214-228, 2010.
39. Ravizza SM, McCormick CA, Schlerf JE, Justus T, Ivry RB, Fiez JA. Cerebellar damage produces selective deficits in verbal working memory. Brain 129: 306-320, 2006.
40. Rorden C, Karnath HO, Bonilha L. Improving lesion-symptom mapping. J Cogn Neurosci 19: 1081-1088, 2007.
41. Schlerf JE, Verstynen TD, Ivry RB, Spencer RM. Evidence of a novel somatopic map in the human neocerebellum during complex actions. J Neurophysiol 103: 3330-3336, 2011.
42. Schniepp R, Wuehr M, Neuhaeusser M, Kamenova M, Dimitriadis K, Klopstock T, Strupp M, Brandt T, Jahn K. Locomotion speed determines gait variability in cerebellar ataxia and vestibular failure. Mov Disord 27: 125-131, 2012.
43. Schoch B, Dimitrova A, Gizewski ER, Timmann D. Functional localization in the human cerebellum based on voxelwise statistical analysis: a study of 90 patients. Neuroimage 30: 36-51, 2006.
44. Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM. Dual-tasking effects on gait variability: the role of aging, falls, and executive function. Mov Disord 21: 950-957, 2006.
45. Srygley JM, Mirelman A, Herman T, Giladi N, Hausdorff JM. When does walking alter thinking? Age and task associated findings. Brain Res 1253: 92-99, 2009.
46. Stein JF, Glickstein M. Role of the cerebellum in visual guidance of movement. Physiol Rev 72: 967-1017, 1992.
47. Stolze H, Klebe S, Petersen G, Raethjen J, Wenzelburger R, Witt K, Deuschl G. Typical features of cerebellar ataxic gait. J Neurol Neurosurg Psychiatry 73: 310-312, 2002.
48. Stoodley CJ, Schmahmann JD. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 46: 831-844, 2010.
49. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44: 489-501, 2009.
50. Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci 32: 413-434, 2009.
51. Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG. The cerebellar cognitive profile. Brain 134: 3669-3683, 2011.
52. Thach WT, Bastian AJ. Role of the cerebellum in the control and adaptation of gait in health and disease. Prog Brain Res 143: 353-366, 2004.
53. Thach WT, Perry JG, Kane SA, Goodkin HP. Cerebellar nuclei: rapid alternating movement, motor somatotopy, and a mechanism for the control of muscle synergy. Rev Neurol (Paris) 149: 607-628, 1993.
54. Thurling M, Hautzel H, Kuper M, Stefanescu MR, Maderwald S, Ladd ME, Timmann D. Involvement of the cerebellar cortex and nuclei in verbal and visuospatial working memory: a 7T fMRI study. Neuroimage 62: 1537-1550, 2012.
55. Timmann D, Daum I. Cerebellar contributions to cognitive functions: a progress report after two decades of research. Cerebellum 6: 159-162, 2007.
56. Timmann D, Daum I. How consistent are cognitive impairments in patients with cerebellar disorders? Behav Neurol 23: 81-100, 2010.
57. Timmann D, Konczak J, Ilg W, Donchin O, Hermsdorfer J, Gizewski ER, Schoch B. Current advances in lesion-symptom mapping of the human cerebellum. Neuroscience 162: 836-851, 2009.
58. Trouillas P, Takayanagi T, Hallett M, Currier RD, Subramony SH, Wessel K, Bryer A, Diener HC, Massaquoi S, Gomez CM, Coutinho P, Ben Hamida M, Campanella G, Filla A, Schut L, Timann D, Honnorat J, Nighoghossian N, Manyam B. International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. The Ataxia Neuropharmacology Committee of the World Federation of Neurology. J Neurol Sci 145: 205-211, 1997.
59. van de Warrenburg BP, Steijns JA, Munneke M, Kremer BP, Bloem BR. Falls in degenerative cerebellar ataxias. Mov Disord 20: 497-500, 2005.
60. Verrel J, Lovden M, Schellenbach M, Schaefer S, Lindenberger U. Interacting effects of cognitive load and adult age on the regularity of whole-body motion during treadmill walking. Psychol Aging 24: 75-81, 2009.
61. Winter DA. Kinematic and kinetic patterns in human gait: variability and compensating effects. Hum Mov Sci 3: 51-76, 1984.
62. Woollacott M, Shumway-Cook A. Attention and the control of posture and gait: a review of an emerging area of research. Gait Posture 16: 1-14, 2002.
63. Wu T, Liu J, Hallett M, Zheng Z, Chan P. Cerebellum and integration of neural networks in dual-task processing. Neuroimage 65: 466-475, 2013.
64. Yogev G, Giladi N, Peretz C, Springer S, Simon ES, Hausdorff JM. Dual tasking, gait rhythmicity, and Parkinson's disease: which aspects of gait are attention demanding? Eur J Neurosci 22: 1248-1256, 2005.
65. Yogev-Seligmann G, Giladi N, Brozgol M, Hausdorff JM. A training program to improve gait while dual tasking in patients with Parkinson's disease: a pilot study. Arch Phys Med Rehabil 93: 176-181, 2012.
66. Yogev-Seligmann G, Hausdorff JM, Giladi N. The role of executive function and attention in gait. Mov Disord 23: 329-342; quiz 472, 2008.
67. Yogev-Seligmann G, Rotem-Galili Y, Mirelman A, Dickstein R, Giladi N, Hausdorff JM. How does explicit prioritization alter walking during dualtask performance? Effects of age and sex on gait speed and variability. Phys Ther 90: 177-186, 2010.