Low-Frequency Brain Oscillations Track Motor Recovery in Human Stroke

被引:50
作者
Boenstrup, Marlene [1 ,2 ]
Krawinkel, Lutz [2 ]
Schulz, Robert [2 ]
Cheng, Bastian [2 ]
Feldheim, Jan [2 ]
Thomalla, Goetz [2 ]
Cohen, Leonardo G. [1 ]
Gerloff, Christian [2 ]
机构
[1] NINDS, Human Cort Physiol & Stroke Neurorehabil Sect, NIH, Bldg 10,Room 7D38, Bethesda, MD 20892 USA
[2] Univ Med Ctr Hamburg Eppendorf, Dept Neurol, Hamburg, Germany
关键词
BETA OSCILLATIONS; STIMULATION; CORTEX; REHABILITATION; CONNECTIVITY; INTERFACE; MOVEMENT; PREDICTORS; MECHANISMS; DYNAMICS;
D O I
10.1002/ana.25615
中图分类号
R74 [神经病学与精神病学];
学科分类号
摘要
Objective The majority of patients with stroke survive the acute episode and live with enduring disability. Effective therapies to support recovery of motor function after stroke are yet to be developed. Key to this development is the identification of neurophysiologic signals that mark recovery and are suitable and susceptible to interventional therapies. Movement preparatory low-frequency oscillations (LFOs) play a key role in cortical control of movement. Recent animal data point to a mechanistic role of motor cortical LFOs in stroke motor deficits and demonstrate neuromodulation intervention with therapeutic benefit. Their relevance in human stroke pathophysiology is unknown. Methods We studied the relationship between movement-preparatory LFOs during the performance of a visuomotor grip task and motor function in a longitudinal (<5 days, 1 and 3 months) cohort study of 33 patients with motor stroke and in 19 healthy volunteers. Results Acute stroke-lesioned brains fail to generate the LFO signal. Whereas in healthy humans, a transient occurrence of LFOs preceded movement onset at predominantly contralateral frontoparietal motor regions, recordings in patients revealed that movement-preparatory LFOs were substantially diminished to a level of 38% after acute stroke. LFOs progressively increased at 1 and 3 months. This re-emergence closely tracked the recovery of motor function across several movement qualities including grip strength, fine motor skills, and synergies and was frequency band specific. Interpretation Our results provide the first human evidence for a link between movement-preparatory LFOs and functional recovery after stroke, promoting their relevance for movement control. These results suggest that it may be interesting to explore targeted, LFOs-restorative brain stimulation therapy in human stroke patients. ANN NEUROL 2019
引用
收藏
页码:853 / 865
页数:13
相关论文
共 54 条
[1]   Recovery of Over-Ground Walking after Chronic Motor Complete Spinal Cord Injury [J].
Angeli, Claudia A. ;
Boakye, Maxwell ;
Morton, Rebekah A. ;
Vogt, Justin ;
Benton, Kristin ;
Chen, Yangshen ;
Ferreira, Christie K. ;
Harkema, Susan J. .
NEW ENGLAND JOURNAL OF MEDICINE, 2018, 379 (13) :1244-1250
[2]   Brain connectivity and neurological disorders after stroke [J].
Baldassarre, Antonello ;
Ramsey, Lenny E. ;
Siegel, Joshua S. ;
Shulman, Gordon L. ;
Corbetta, Maurizio .
CURRENT OPINION IN NEUROLOGY, 2016, 29 (06) :706-713
[3]   Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices [J].
Bansal, Arjun K. ;
Vargas-Irwin, Carlos E. ;
Truccolo, Wilson ;
Donoghue, John P. .
JOURNAL OF NEUROPHYSIOLOGY, 2011, 105 (04) :1603-1619
[4]   Agreed Definitions and a Shared Vision for New Standards in Stroke Recovery Research: The Stroke Recovery and Rehabilitation Roundtable Taskforce [J].
Bernhardt, Julie ;
Hayward, Kathryn S. ;
Kwakkel, Gert ;
Ward, Nick S. ;
Wolf, Steven L. ;
Borschmann, Karen ;
Krakauer, John W. ;
Boyd, Lara A. ;
Carmichael, S. Thomas ;
Corbett, Dale ;
Cramer, Steven C. .
NEUROREHABILITATION AND NEURAL REPAIR, 2017, 31 (09) :793-799
[5]   Parietofrontal network upregulation after motor stroke [J].
Boenstrup, M. ;
Schulz, R. ;
Schon, G. ;
Cheng, B. ;
Feldheim, J. ;
Thomalla, G. ;
Gerloff, C. .
NEUROIMAGE-CLINICAL, 2018, 18 :720-729
[6]   Evolution of brain activation after stroke in a constant-effort versus constant-output motor task [J].
Boenstrup, Marlene ;
Schulz, Robert ;
Cheng, Bastian ;
Feldheim, Jan ;
Zimerman, Maximo ;
Thomalla, Goetz ;
Hummel, Friedhelm C. ;
Gerloff, Christian .
RESTORATIVE NEUROLOGY AND NEUROSCIENCE, 2015, 33 (06) :845-864
[7]   Contralesional Brain-Computer Interface Control of a Powered Exoskeleton for Motor Recovery in Chronic Stroke Survivors [J].
Bundy, David T. ;
Souders, Lauren ;
Baranyai, Kelly ;
Leonard, Laura ;
Schalk, Gerwin ;
Coker, Robert ;
Moran, Daniel W. ;
Huskey, Thy ;
Leuthardt, Eric C. .
STROKE, 2017, 48 (07) :1908-+
[8]   A brain-spine interface alleviating gait deficits after spinal cord injury in primates [J].
Capogrosso, Marco ;
Milekovic, Tomislav ;
Borton, David ;
Wagner, Fabien ;
Moraud, Eduardo Martin ;
Mignardot, Jean-Baptiste ;
Buse, Nicolas ;
Gandar, Jerome ;
Barraud, Quentin ;
Xing, David ;
Rey, Elodie ;
Duis, Simone ;
Yang Jianzhong ;
Ko, Wai Kin D. ;
Li, Qin ;
Detemple, Peter ;
Denison, Tim ;
Micera, Silvestro ;
Bezard, Erwan ;
Bloch, Jocelyne ;
Courtine, Gregoire .
NATURE, 2016, 539 (7628) :284-+
[9]   Diaschisis: past, present, future [J].
Carrera, Emmanuel ;
Tononi, Giulio .
BRAIN, 2014, 137 :2408-2422
[10]   Neural population dynamics during reaching [J].
Churchland, Mark M. ;
Cunningham, John P. ;
Kaufman, Matthew T. ;
Foster, Justin D. ;
Nuyujukian, Paul ;
Ryu, Stephen I. ;
Shenoy, Krishna V. .
NATURE, 2012, 487 (7405) :51-+