Robust neuroprosthetic control from the stroke perilesional cortex

Journal of Neuroscience

Volumn 35, Issue 22, 2015, Pages 8653-8661

  Gulati, Tanuj ^a,b   Won, Seok Joon ^a,b   Ramanathan, Dhakshin S ^a,b   Wong, Chelsea C ^a,b   Bodepudi, Anitha ^a,b   Swanson, Raymond A ^a,b   Ganguly, Karunesh ^a,b  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain machine interface; Electrophysiology; Plasticity; Stroke

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR ASSESSMENT; BRAIN COMPUTER INTERFACE; BRAIN CORTEX; CEREBROVASCULAR ACCIDENT; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; LEARNING; MALE; MATHEMATICAL MODEL; MOTOR ACTIVITY; MOTOR DYSFUNCTION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROPHYSIOLOGY; NEUROPROSTHESIS; NONHUMAN; PERILESIONAL CORTEX; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIGNAL NOISE RATIO; SPINAL CORD INJURY; STATISTICAL CONCEPTS; TASK PERFORMANCE; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; COMPUTER INTERFACE; LONG EVANS RAT; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN-COMPUTER INTERFACES; MALE; MOTOR CORTEX; MOTOR SKILLS; NEURONS; RATS; RATS, LONG-EVANS; STROKE; USER-COMPUTER INTERFACE;

EID: 84930454231     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5007-14.2015     Document Type: Article

References (63)

1. Arduin PJ, Frégnac Y, Shulz DE, Ego-Stengel V (2013) “Master” neurons induced by operant conditioning in rat motor cortex during a brain-machine interface task. J Neurosci 33:8308–8320. CrossRef Medline
2. Biernaskie J, Corbett D (2001) Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. J Neurosci 21:5272–5280. Medline
3. Birbaumer N, Cohen LG (2007) Brain-computer interfaces: communication and restoration of movement in paralysis. J Physiol 579:621-636. CrossRef Medline
4. Birbaumer N, Ramos Murguialday A, Weber C, Montoya P (2009) Neurofeedback and brain-computer interface clinical applications. Int Rev Neurobiol 86:107–117. CrossRef Medline
5. Bliss T, Guzman R, Daadi M, Steinberg GK (2007) Cell transplantation therapy for stroke. Stroke 38:817-826. CrossRef Medline
6. Brinkman J, Kuypers HG (1973) Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. Brain 96:653-674. CrossRef Medline
7. Brown CE, Boyd JD, Murphy TH (2010) Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke. J Cereb Blood Flow Metab 30:783-791. CrossRef Medline
8. Bundy DT, Wronkiewicz M, Sharma M, Moran DW, Corbetta M, Leuthardt EC (2012) Using ipsilateral motor signals in the unaffected cerebral hemisphere as a signal platform for brain-computer interfaces in hemiplegic stroke survivors. J Neural Eng 9:036011. CrossRef Medline
9. Carmena JM, Lebedev MA, Crist RE, O’Doherty JE, Santucci DM, Dimitrov DF, Patil PG, Henriquez CS, Nicolelis MA (2003) Learning to control a brain–machine interface for reaching and grasping by primates. PLoS Biol 1:E42. Medline
10. Carmichael ST, Chesselet MF (2002) Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. J Neurosci 22:6062-6070. Medline
11. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MA (1999) Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nat Neurosci 2:664–670. CrossRef Medline
12. Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305–309. CrossRef Medline
13. Collinger JL, Wodlinger B, Downey JE, Wang W, Tyler-Kabara EC, Weber DJ, McMorland AJ, Velliste M, Boninger ML, Schwartz AB (2013) Highperformance neuroprosthetic control by an individual with tetraplegia. Lancet 381:557–564. CrossRef Medline
14. Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, Abdi A, Baufreton J, Bienvenu TC, Herry C (2014) Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 505:92–96. Medline
15. Cramer SC (2008) Repairing the human brain after stroke: I. Mechanisms of spontaneous recovery. Ann Neurol 63:272–287. CrossRef Medline
16. Daly JJ, Wolpaw JR (2008) Brain-computer interfaces in neurological rehabilitation. Lancet Neurol 7:1032–1043. CrossRef Medline
17. Dancause N (2006) Vicarious function of remote cortex following stroke: recent evidence from human and animal studies. Neuroscientist 12:489-499. CrossRef Medline
18. Fetz EE (1969) Operant conditioning of cortical unit activity. Science 163: 955–958. CrossRef Medline
19. Fetz EE (2007) Volitional control of neural activity: implications for braincomputer interfaces. J Physiol 579:571–579. CrossRef Medline
20. Foroud A, Whishaw IQ (2006) Changes in the kinematic structure and nonkinematic features of movements during skilled reaching after stroke: a Laban Movement Analysis in two case studies. J Neurosci Methods 158: 137–149. CrossRef Medline
21. Ganguly K, Carmena JM (2009) Emergence of a stable cortical map for neuroprosthetic control. Plos Biol 7:e1000153. CrossRef Medline
22. Ganguly K, Secundo L, Ranade G, Orsborn A, Chang EF, Dimitrov DF, Wallis JD, Barbaro NM, Knight RT, Carmena JM (2009) Cortical representation of ipsilateral arm movements in monkey and man. J Neurosci 29: 12948–12956. CrossRef Medline
23. Ganguly K, Dimitrov DF, Wallis JD, Carmena JM (2011) Reversible largescale modification of cortical networks during neuroprosthetic control. Nat Neurosci 14:662-667. CrossRef Medline
24. Ganguly K, Byl NN, Abrams GM (2013) Neurorehabilitation: Motor recovery after stroke as an example. Ann Neurol 74:373–381. CrossRef Medline
25. Guggenmos DJ, Azin M, Barbay S, Mahnken JD, Dunham C, Mohseni P, Nudo RJ (2013) Restoration of function after brain damage using a neural prosthesis. Proc Natl Acad Sci U S A 110:21177–21182. CrossRef Medline
26. Gulati T, Ramanathan DS, Wong CC, Ganguly K (2014) Reactivation of emergent task-related ensembles during slow-wave sleep after neuroprosthetic learning. Nat Neurosci 17:1107–1113. CrossRef Medline
27. Hagemann G, Redecker C, Neumann-Haefelin T, Freund HJ, Witte OW (1998) Increased long-term potentiation in the surround of experimentally induced focal cortical infarction. Ann Neurol 44:255–258. CrossRef Medline
28. Halder S, Agorastos D, Veit R, Hammer EM, Lee S, Varkuti B, Bogdan M, Rosenstiel W, Birbaumer N, Kübler A (2011) Neural mechanisms of brain-computer interface control. Neuroimage 55:1779-1790. CrossRef Medline
29. Hochberg LR, Serruya MD, Friehs GM, Mukand JA, Saleh M, Caplan AH, Branner A, Chen D, Penn RD, Donoghue JP (2006) Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442: 164–171. CrossRef Medline
30. Hochberg LR, Bacher D, Jarosiewicz B, Masse NY, Simeral JD, Vogel J, Haddadin S, Liu J, Cash SS, van der Smagt P, Donoghue JP (2012) Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 485:372–375. CrossRef Medline
31. Hummel FC, Cohen LG (2006) Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke? Lancet Neurol 5:708-712. CrossRef Medline
32. Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T (2009) Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12:1586-1593. CrossRef Medline
33. Jarosiewicz B, Chase SM, Fraser GW, Velliste M, Kass RE, Schwartz AB (2008) Functional network reorganization during learning in a braincomputer interface paradigm. Proc Natl Acad Sci U S A 105:19486-19491. CrossRef Medline
34. Koralek AC, Long JD, Costa RM, Carmena JM (2010) Corticostriatal dynamics during learning and performance of a neuroprosthetic task. Conf Proc IEEE Eng Med Biol Soc 2010:2682–2685. Medline
35. Koralek AC, Jin X, Long JD 2nd, Costa RM, Carmena JM (2012) Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature 483:331–335. CrossRef Medline
36. Laaksonen K, Helle L, Parkkonen L, Kirveskari E, Mäkelä JP, Mustanoja S, Tatlisumak T, Kaste M, Forss N (2013) Alterations in spontaneous brain oscillations during stroke recovery. PLoS One 8:e61146. CrossRef Medline
37. Langhorne P, Bernhardt J, Kwakkel G (2011) Stroke rehabilitation. Lancet 377:1693–1702. CrossRef Medline
38. Lopes-dos-Santos V, Ribeiro S, Tort AB (2013) Detecting cell assemblies in large neuronal populations. J Neurosci Methods 220:149-166. CrossRef Medline
39. Mitchell JF, Sundberg KA, Reynolds JH (2009) Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63:879-888. CrossRef Medline
40. Mitra P, Bokil H (2008) Observed brain dynamics. New York: OUP.
41. Moritz CT, Perlmutter SI, Fetz EE (2008) Direct control of paralysed muscles by cortical neurons. Nature 456:639–642. CrossRef Medline
42. Murphy TH, Corbett D (2009) Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci 10:861-872. CrossRef Medline
43. Musallam S, Corneil BD, Greger B, Scherberger H, Andersen RA (2004) Cognitive control signals for neural prosthetics. Science 305:258-262. CrossRef Medline
44. Norrving B, Kissela B (2013) The global burden of stroke and need for a continuum of care. Neurology 80:S5–12. CrossRef Medline
45. Nudo RJ, Milliken GW (1996) Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophysiol 75:2144-2149. Medline
46. Nudo RJ, Wise BM, SiFuentes F, Milliken GW (1996) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272:1791–1794. CrossRef Medline
47. Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12:919-926. CrossRef Medline
48. Ramanathan D, Conner JM, Tuszynski MH (2006) A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proc Natl Acad Sci U S A 103:11370-11375. CrossRef Medline
49. Ramos-Murguialday A, Broetz D, Rea M, Läer L, Yilmaz O, Brasil FL, Liberati G, Curado MR, Garcia-Cossio E, Vyziotis A, Cho W, Agostini M, Soares E, Soekadar S, Caria A, Cohen LG, Birbaumer N (2013) Brain–machine interface in chronic stroke rehabilitation: a controlled study. Ann Neurol 74:100-108. CrossRef Medline
50. Rutishauser U, Ross IB, Mamelak AN, Schuman EM (2010) Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464:903–907. CrossRef Medline
51. Santhanam G, Ryu SI, Yu BM, Afshar A, Shenoy KV (2006) A highperformance brain-computer interface. Nature 442:195–198. CrossRef Medline
52. Schiene K, Bruehl C, Zilles K, Qü M, Hagemann G, Kraemer M, Witte OW (1996) Neuronal hyperexcitability and reduction of GABAA-receptor expression in the surround of cerebral photothrombosis. J Cereb Blood Flow Metab 16:906-914. Medline
53. Serruya MD, Hatsopoulos NG, Paninski L, Fellows MR, Donoghue JP (2002) Instant neural control of a movement signal. Nature 416:141–142. CrossRef Medline
54. Stinear CM, Barber PA, Petoe M, Anwar S, Byblow WD (2012) The PREP algorithm predicts potential for upper limb recovery after stroke. Brain 135:2527–2535. CrossRef Medline
55. Strehl U, Leins U, Goth G, Klinger C, Hinterberger T, Birbaumer N (2006) Self-regulation of slow cortical potentials: a new treatment for children with attention-deficit/hyperactivity disorder. Pediatrics 118:e1530-1540. CrossRef Medline
56. Suner S, Fellows MR, Vargas-Irwin C, Nakata GK, Donoghue JP (2005) Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex. IEEE Trans Neural Syst Rehabil Eng 13:524-541. CrossRef Medline
57. Taylor DM, Tillery SI, Schwartz AB (2002) Direct cortical control of 3D neuroprosthetic devices. Science 296:1829-1832. CrossRef Medline
58. Van Huffelen AC, Poortvliet DC, Van der Wulp CJ (1984) Quantitative electroencephalography in cerebral ischemia: detection of abnormalities in “normal” EEGs. Prog Brain Res 62:3–28. CrossRef Medline
59. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB (2008) Cortical control of a prosthetic arm for self-feeding. Nature 453:1098-1101. CrossRef Medline
60. Vinck M, Womelsdorf T, Buffalo EA, Desimone R, Fries P (2013) Attentional modulation of cell-class-specific gamma-band synchronization in awake monkey area v4. Neuron 80:1077–1089. CrossRef Medline
61. Ward NS (2004) Functional reorganization of the cerebral motor system after stroke. Curr Opin Neurol 17:725–730. CrossRef Medline
62. Wong CC, Ramanathan DS, Gulati T, Won SJ, Ganguly K (2015) An automated behavioral box to assess forelimb function in rats. J Neurosci Methods 246:30-37. CrossRef Medline
63. Zeitler M, Fries P, Gielen S (2006) Assessing neuronal coherence with single-unit, multi-unit, and local field potentials. Neural Comput 18: 2256–2281. CrossRef Medline