Beta-band amplitude oscillations in the human internal globus pallidus support the encoding of sequence boundaries during initial sensorimotor sequence learning

NeuroImage

Volumn 85, Issue , 2014, Pages 779-793

  Herrojo Ruiz, María ^a   Brücke, Christof ^a   Nikulin, Vadim V ^a,b   Schneider, Gerd Helge ^a   Kühn, Andrea A ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; AMPLITUDE MODULATION; ARTICLE; BASAL GANGLION; BEHAVIOR; BEHAVIORAL SCIENCE; BETA RHYTHM; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; DYSTONIA; FEMALE; FINGER; GLOBUS PALLIDUS; HUMAN; LEARNING; LEARNING AND MEMORY TEST; LOCOMOTION; MALE; MIDDLE AGED; MOTOR DEVELOPMENT; NEUROMODULATION; OSCILLATION; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SEQUENTIAL BEHAVIOR; SKILL TRAINING; TASK PERFORMANCE;

ADULT; AGED; BETA RHYTHM; FEMALE; GLOBUS PALLIDUS; HUMANS; LEARNING; MALE; MIDDLE AGED; PSYCHOMOTOR PERFORMANCE;

EID: 84889687273     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.05.085     Document Type: Article

References (88)

1. Agostino R., Berardelli A., Formica A., Accornero N., Manfredi M. Sequential arm movements in patients with Parkinson's disease Huntington's disease and dystonia. Brain 1992, 115:1481-1495.
2. Aldridge J.W., Berridge K.C. Coding of serial order by neostriatal neurons: a "natural action" approach to movement sequence. J. Neurosci. 1998, 18:2777-2787.
3. Alegre M., Alonso-Frech F., Rodríguez-Oroz M.C., Guridi J., Zamarbide I., Valencia M., Manrique M., Obeso J.A., Artieda J. Movement-related changes in oscillatory activity in the human subthalamic nucleus: ipsilateral vs contralateral movements. Eur. J. Neurosci. 2005, 22:2315-2324.
4. Androulidakis A.G., Brücke C., Kempf F., Kupsch A., Aziz T., Ashkan K., Kuhn A.A., Brown P. Amplitude modulation of oscillatory activity in the subthalamic nucleus during movement. Eur. J. Neurosci. 2008, 27(5):1277-1284.
5. Anzak A., Tan H., Pogosyan A., Foltynie T., Limousin P., Zrinzo L., et al. Subthalamic nucleus activity optimizes maximal effort motor responses in Parkinson's disease. Brain 2012, 135(9):2766-2778.
6. Argyelan M., Carbon M., Ghilardi M.F., Feigin A., Mattis P., Tang C., et al. Dopaminergic suppression of brain deactivation responses during sequence learning. J. Neurosci. 2008, 28:10687-10695.
7. Averbeck B.B., Sohn J.W., Lee D. Activity in prefrontal cortex during dynamic selection of action sequences. Nat. Neurosci. 2006, 9(2):276-282.
8. Barnes T.D., Kubota Y., Hu D., Jin D.Z., Graybiel A.M. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 2005, 437:1158-1161.
9. Becker R., Ritter P., Villringer A. Influence of ongoing alpha rhythm on the visual evoked potential. Neuroimage 2008, 39(2):707-716.
10. Bella S.D., Palmer C. Rate effects on timing key velocity and finger kinematics in piano performance. PLoS One 2011, 6(6):e20518.
11. Benjamini Y., Krieger A.M., Yekuteli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika 2006, 93(3):491-507.
12. Boonstra T.W., Daffertshofer A., Breakspear M., Beek P.J. Multivariate time-frequency analysis of electromagnetic brain activity during bimanual motor learning. Neuroimage 2007, 36(2):370-377.
13. Brashers-Krug T., Shadmehr R., Bizzi E. Consolidation in human motor memory. Nature 1996, 382:252-255.
14. Brown P. Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Curr. Opin. Neurobiol. 2007, 17(6):656-664.
15. Brown R.G., Redondo-Verge L., Chacon J.R., Lucas M.L., Channon S. Dissociation between intentional and incidental sequence learning in Huntington's disease. Brain 2001, 124(Pt 11):2188-2202.
16. Brücke C., Kempf F., Kupsch A., Schneider G.H., Krauss J.K., Aziz T., Yarrow K., Pogosyan A., Brown P., Kühn A.A. Movement-related synchronization of gamma activity is lateralized in patients with dystonia. Eur. J. Neurosci. 2008, 27(9):2322-2329.
17. Brücke C., Huebl J., Schönecker T., Neumann W.J., Yarrow K., et al. Scaling of movement is related to pallidal γ oscillations in patients with dystonia. J. Neurosci. 2012, 32(3):1008-1019.
18. Carbon M., Ma Y., Barnes A., Dhawan V., Chaly T., Ghilardi M.F., et al. Caudate nucleus: influence of dopaminergic input on sequence learning and brain activation in Parkinsonism. Neuroimage 2004, 21:1497-1507.
19. Countermanche R., Fujii N., Graybiel A.M. Synchronous focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J. Neurosci. 2003, 23(37):11741-11752.
20. David O., Kilner J.M., Friston K.J. Mechanisms of evoked and induced responses in MEG/EEG. Neuroimage 2006, 31:1580-1591.
21. Dehaene S., Changeux J.P. A hierarchical neuronal network for planning behavior. PNAS 1997, 94(24):13293-13298.
22. DeLong M.R., Wichmann T. Circuits and circuit disorders of the basal ganglia. Arch. Neurol. 2007, 64:20-24.
23. Delorme A., Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 2004, 134:9-21.
24. Durán B., Sandamirskaya Y., Schöner G. A dynamic field architecture for the generation of hierarchically organized sequences. ICANN 2012, (1):25-32.
25. Finney S.A., Palmer C. Auditory feedback and memory for music performance: sound evidence for an encoding effect. Mem. Cognit. 2003, 31(1):51-64.
26. Fujii N., Graybiel A.M. Representation of action sequence boundaries by macaque prefrontal cortical neurons. Science 2003, 301:1246-1249.
27. Georgiou N., Bradshaw J.L., Iansek R., Phillips J.G., Mattingley J.B., et al. Reduction in external cues and movement sequencing in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 1994, 57(3):368-370.
28. Ghilardi M.F., Carbon M., Silvestri G., Dhawan V., Tagliati M., et al. Impaired sequence learning in carriers of the DYT1 dystonia mutation. Ann. Neurol. 2003, 54:102-109.
29. Goebl W., Bresin R. Measurement and reproduction accuracy of computer-controlled grand pianos. J. Acoust. Soc. Am. 2003, 114:2273-2283.
30. Good P. Permutation Parametric and Bootstrap Tests of Hypotheses 2005, Springer, Berlin. 2nd ed.
31. Grandchamp R., Delorme A. Single-trial normalization for event-related spectral decomposition reduces sensitivity to noisy trials. Front. Psychol. 2011, 2:236.
32. Graybiel A.M. The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 1998, 70(1-2):119-136.
33. Graybiel A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 2008, 31:359-387. (Review).
34. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 2007, 30(7):357-364.
35. Herrmann C.S., Munk M.H., Engel A.K. Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn. Sci. 2004, 8(8):347-355.
36. Herrojo Ruiz M., Jabusch H.C., Altenmüller E. Detecting wrong notes in advance: neuronal correlates of error monitoring in pianists. Cereb. Cortex 2009, 19(11):2625-2639.
37. Hikosaka O., Nakahara H., Rand M.K., Sakai K., Lu X., et al. Parallel neural networks for learning sequential procedures. Trends Neurosci. 1999, 22:464-471.
38. Hikosaka O., Nakamura K., Sakai K., Nakahara H. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 2002, 12(2):217-222.
39. Hohlefeld F.U., Huebl J., Huchzermeyer C., Schneider G.H., Schönecker T., et al. Long-range temporal correlations in the subthalamic nucleus of patients with Parkinson's disease. Eur. J. Neurosci. 2012, 36(6):2812-2821.
40. Janata P., Grafton S.T. Swinging in the brain: shared neural substrates for behaviors related to sequencing and music. Nat. Neurosci. 2003, 6(7):682-687. (Review).
41. Jin X., Costa R.M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 2010, 466:457-462.
42. Joundi R.A., Brittain J.S., Green A.L., Aziz T.Z., Brown P., Jenkinson N. Persistent suppression of subthalamic beta-band activity during rhythmic finger tapping in Parkinson's disease. Clin. Neurophysiol. 2013, 124(3):565-573.
43. Kalcher J., Pfurtscheller G. Discrimination between phase-locked and non-phase-locked event-related EEG activity. Electroencephalogr. Clin. Neurophysiol. 1995, 94(5):381-384.
44. Kao M.H., Doupe A.J., Brainard M.S. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 2005, 433(7026):638-643.
45. Kennerley S.W., Sakai K., Rushworth M.F.S. Organization of action sequences and the role of the pre-SMA. J. Neurophysiol. 2004, 91:978-993.
46. Kinoshita H., Furuya S., Aoki T., Altenmüller E. Loudness control in pianists as exemplified in keystroke force measurements on different touches. J. Acoust. Soc. Am. 2007, 121:2959-2969.
47. Knowlton B.J., Mangels J.A., Squire L.R. A neostriatal habit learning system in humans. Science 1996, 273(5280):1399-1402.
48. Koechlin E., Jubault T. Broca's area and the hierarchical organization of human behavior. Neuron 2006, 50(6):963-974.
49. Kühn A.A., Williams D., Kupsch A., Limousin P., Hariz M., et al. Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain 2004, 127:735-746.
50. Kühn A.A., Doyle L., Pogosyan A., Yarrow K., Kupsch A., Schneider G.H., Hariz M.I., Trottenberg T., Brown P. Modulation of beta oscillations in the subthalamic area during motor imagery in Parkinson's disease. Brain 2006, 129:695-706.
51. Kullback S., Leibler R.A. On information and sufficiency. Ann. Math. Stat. 1951, 22:79-86.
52. Lehéricy S., Benali H., Van de Moortele P.F., Pélégrini-Issac M., Waechter T., et al. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. PNAS 2005, 102(35):12566-12571.
53. Linkenkaer-Hansen K., Nikouline V.V., Palva J.M., Ilmoniemi R.J. Long-range temporal correlations and scaling behavior in human brain oscillations. J. Neurosci. 2001, 21:1370-1377.
54. Linkenkaer-Hansen K., Nikulin V.V., Palva J.M., Kaila K., Ilmoniemi R.J. Stimulus-induced change in long-range temporal correlations and scaling behaviour of sensorimotor oscillations. Eur. J. Neurosci. 2004, 19(1):203-211.
55. Litvak V., Eusebio A., Jha A., Oostenveld R., Barnes G., Foltynie T., Limousin P., Zrinzo L., Hariz M.I., Friston K., Brown P. Movement-related changes in local and long-range synchronization in Parkinson's disease revealed by simultaneous magnetoencephalography and intracranial recordings. J. Neurosci. 2012, 32(31):10541-10553.
56. Liu X., Wang S., Yianni J., Nandi D., Bain P.G., Gregory R., Stein J.F., Aziz T.Z. The sensory and motor representation of synchronized oscillations in the globus pallidus in patients with primary dystonia. Brain 2008, 131(Pt 6):1562-1573.
57. Mallat S. A Wavelet Tour of Signal Processing 1999, Academic Press, San Diego.
58. Mazaheri A., Nieuwenhuis I.L., van Dijk H., Jensen O. Prestimulus alpha and mu activity predicts failure to inhibit motor responses. Hum. Brain Mapp. 2009, 30(6):1791-1800.
59. Minetti A.E., Ardigò L.P., McKee T. Keystroke dynamics and timing: accuracy, precision and difference between hands in pianist's performance. J. Biomech. 2007, 40(16):3738-3743.
60. Mushiake H., Strick P.L. Pallidal neuron activity during sequential arm movements. J. Neurophysiol. 1995, 74:2754-2758.
61. Ölveczky B.P., Otchy T.M., Goldberg J.H., Aronov D., Fee M.S. Changes in the neural control of a complex motor sequence during learning. J. Neurophysiol. 2011, 106:386-397.
62. Omlor W., Patino L., Mendez-Balbuena I., Schulte-Mönting J., Kristeva R. Corticospinal beta-range coherence is highly dependent on the pre-stationary motor state. J. Neurosci. 2011, 31(22):8037-8045.
63. Oswal A., Litvak V., Sauleau P., Brown P. Beta reactivity prospective facilitation of executive processing and its dependence on dopaminergic therapy in Parkinson's disease. J. Neurosci. 2012, 32(29):9909-9916.
64. Palva J.M., Zhigalov A., Hirvonen J., Korhonen O., Linkenkaer-Hansen K., Palva S. Neuronal long-range temporal correlations and avalanche dynamics are correlated with behavioral scaling laws. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(9):3585-3590.
65. Pammi V.S., Miyapuram K.P., Ahmed Samejima K., Bapim R.S., et al. Changing the structure of complex visuo-motor sequences selectively activates the fronto-parietal network. Neuroimage 2012, 59:1180-1189.
66. Peng C.K., Havlin S., Stanley H.E., Goldberger A.L. Quantification of scaling exponents and crossover phenomena in nonstationary heartbeat time series. Chaos 1995, 5(1):82-87.
67. Penhune V.B., Doyon J. Cerebellum and M1 interaction during early learning of timed motor sequences. Neuroimage 2005, 26:801-812.
68. Pfurtscheller G., Stancak A., Edlinger E. On the existence of different types of central beta rhythms below 30Hz. Electroencephalogr. Clin. Neurophysiol. 1997, 102:316-325.
69. Pfurtscheller G., Graimann B., Huggins J.E., Levine S.P., Schuh L.A. Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin. Neurophysiol. 2003, 114(7):1226-1236.
70. Pfurtscheller G., Neuper C., Brunner C., da Silva F.L. Beta rebound after different types of motor imagery in man. Neurosci. Lett. 2005, 378:156-159.
71. Poil S.S., Hardstone R., Mansvelder H.D., Linkenkaer-Hansen K. Critical-state dynamics of avalanches and oscillations jointly emerge from balanced excitation/inhibition in neuronal networks. J. Neurosci. 2012, 32(29):9817-9823.
72. Ray N.J., Brittain J.S., Holland P., Joundi R.A., Stein J.F., Aziz T.Z., Jenkinson N. The role of the subthalamic nucleus in response inhibition: evidence from local field potential recordings in the human subthalamic nucleus. Neuroimage 2012, 60(1):271-278.
73. Reinacher M., Becker R., Villringer A., Ritter P. Oscillatory brain states interact with late cognitive components of the somatosensory evoked potential. J. Neurosci. Methods 2009, 183(1):49-56.
74. Rosin R., Topka H., Dichgans J. Gait initiation in Parkinson's disease. Mov. Disord. 1997, 12(5):682-690.
75. Sakai K., Kitaguchi K., Hikosaka O. Chunking during human visuomotor sequence learning. Exp. Brain Res. 2003, 152:229-242.
76. Schönecker T., Kupsch A., Kühn A.A., Schneider G.H., Hoffmann K.T. Automated optimization of subcortical cerebral MR imaging-atlas coregistration for improved postoperative electrode localization in deep brain stimulation. Am. J. Neuroradiol. 2009, 30(10):1914-1921.
77. Shadmehr R., Brashers Krug T. Functional stages in the formation of human long-term motor memory. J. Neurosci. 1997, 17:409-419.
78. Siberstein P., Kuhn A.A., Kupsch A., Trottenberg T., Krauss J.K., et al. Patterning of globus pallidus local field potentials differs between Parkinson's disease and dystonia. Brain 2003, 126:2597-2608.
79. Stringer S.M., Rolls E.T., Taylor P. Learning movement sequences with a delayed reward signal in a hierarchical model of motor function. Neural Netw. 2007, 20(2):172-181.
80. Tallon-Baudry C., Bertrand O., Delpuech C., Pernier J. Stimulus specificity of phase-locked and non-phase-locked 40-Hz visual responses in human. J. Neurosci. 1996, 16(13):4240-4249.
81. Tremblay P.L., Bedard M.A., Langlois D., Blanchet P.J., Lemay M., Parent M. Movement chunking during sequence learning is a dopamine-dependant process: a study conducted in Parkinson's disease. Exp. Brain Res. 2010, 205(3):375-385.
82. van Dijk H., Schoffelen J.M., Oostenveld R., Jensen O. Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J. Neurosci. 2008, 28(8):1816-1823.
83. van Wijk B.C., Daffertshofer A., Roach N., Praamstra P. A role of beta oscillatory synchrony in biasing response competition?. Cereb. Cortex 2009, 19:1294-1302.
84. Warabi T., Fukushima K., Olley P.M., Chiba S., Yanagisawa N. Difficulty in terminating the preceding movement/posture explains the impaired initiation of new movements in Parkinson's disease. Neurosci. Lett. 2011, 496(2):84-89.
85. Williams D., Kuhn A.A., Kupsch A., Tijssen M., van Bruggen G., et al. Behavioural cues are associated with modulations of synchronous oscillations in the human subthalamic nucleus. Brain 2003, 126:1975-1985.
86. Willingham D.B., Koroshetz W.J. Evidence for neurally dissociable motor skill systems in Huntington's disease patients. Psychobiology 1993, 21:173-182.
87. Wymbs N.F., Bassett D.S., Mucha P.J., Porter M.A., Grafton S.T. Differential recruitment of the sensorimotor putamen and frontoparietal cortex during motor chunking in humans. Neuron 2012, 74(5):936-946.
88. Zatorre R.J., Chen J.L., Penhune V.B. When the brain plays music: auditory-motor interactions in music perception and production. Nat. Rev. Neurosci. 2007, 8(7):547-558. (Review).