Cortical ensemble adaptation to represent velocity of an artificial actuator controlled by a brain-machine interface

Journal of Neuroscience

Volumn 25, Issue 19, 2005, Pages 4681-4693

  Lebedev, Mikhail A ^a,c   Carmena, Jose M ^a,c   O'Doherty, Joseph E ^b   Zacksenhouse, Miriam ^d   Henriquez, Craig S ^b,c   Principe, Jose C ^e   Nicolelis, Miguel A L ^a,b,c,f  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Duke University   (United States)

^c DUKE UNIVERSITY   (United States)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^e University of Florida   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Body schema; Brain machine interface; Cortical plasticity; Macaque monkey; Motor cortex; Motor learning

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN FUNCTION; CELL POPULATION; CONTROLLED STUDY; HAND MOVEMENT; LIMB MOVEMENT; MOTOR PERFORMANCE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; ROBOTICS; VELOCITY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BEHAVIOR, ANIMAL; BRAIN MAPPING; FEMALE; HAND; LEARNING; MACACA MULATTA; MOTOR CORTEX; MOVEMENT; NEURONS; PREDICTIVE VALUE OF TESTS; PSYCHOMOTOR PERFORMANCE; TIME PERCEPTION; USER-COMPUTER INTERFACE;

EID: 18644376712     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4088-04.2005     Document Type: Article

References (81)

1. Alexander GE, Crutcher MD (1990) Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. J Neurophysiol 64:164-178.
2. Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189-220.
3. Ashe J, Georgopoulos AP (1994) Movement parameters and neural activity in motor cortex and area 5. Cereb Cortex 4:590-600.
4. Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP (2005) The parietal representation of hand velocity in a copy task. J Neurophysiol 93:508-518.
5. Baker SN, Spinks R, Jackson A, Lemon RN (2001) Synchronization in monkey motor cortex during a precision grip task. I. Task-dependent modulation in single-unit synchrony. J Neurophysiol 85:869-885.
6. Carmena JM, Lebedev MA, Crist RE, O'Doherty JE, Santucci DM, Dimitrov D, Patil PG, Henriquez CS, Nicolelis MA (2003) Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol 1:193-208.
7. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MAL (1999) Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nat Neurosci 2:664-670.
8. Cheney PD, Fetz EE (1980) Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44:773-791.
9. Cisek P, Kalaska JF (2005) Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45:801-814.
10. Cohen D, Nicolelis MAL (2004) Reduction of single-neuron firing uncertainty by cortical ensembles during motor skill learning. J Neurosci 24:3574-3582.
11. Donchin O, Gribova A, Steinberg O, Bergman H, Vaadia E (1998) Primary motor cortex is involved in bimanual coordination. Nature 395:274-278.
12. Ehrsson HH, Geyer S, Naito E (2003) Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. J Neurophysiol 90:3304-3316.
13. Ehrsson HH, Spense C, Passingham RE (2004) That's my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science 305:875-877.
14. Evarts EV (1966) Pyramidal tract activity associated with a conditioned hand movement in the monkey. J Neurophysiol 29:1011-1027.
15. Floyer-Lea A, Matthews PM (2004) Changing brain networks for visuomotor control with increased movement automaticity. J Neurophysiol 92:2405-2412.
16. Fu QG, Flament D, Coltz JD, Ebner TJ (1995) Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. J Neurophysiol 73:836-854
17. Georgopouios AP (2000) Neural aspects of cognitive motor control. Curr Opin Neurobiol 10:238-241.
18. Georgopouios AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233:1416-1419.
19. Georgopouios AP, Kettner RE, Schwartz AB (1988) Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population. J Neurosci 8:2928-2932.
20. Georgopoulos AP, Ashe J, Smyrnis N, Taira M (1992) The motor cortex and the coding of force. Science 256:1692-1695.
21. Graziano MS (1999) Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. Proc Natl Acad Sci USA 96:10418-10421.
22. Graziano MS, Cooke DF, Taylor CS (2000) Coding the location of the arm by sight. Science 290:1782-1786.
23. Gurfinkel VS, Levick YS, Lebedev MA (1991) Body scheme concept and motor control. Body scheme in the postural automatisms regulation. In: Intellectual processes and their modelling, pp 24-53. Moscow: Nauka.
24. Hatsopoulos NG, Ojakangas CL, Paninski L, Donoghue JP (1998) Information about movement direction obtained from synchronous activity of motor cortical neurons. Proc Natl Acad Sci USA 95:15706-15711.
25. Head H, Holmes G (1911) Sensory disturbances from cerebral lesion. Brain 34:102-254.
26. Iriki A, Tanaka M, Iwamura Y (1996) Coding of modified body schema during tool use by macaque postcentral neurons. NeuroReport 7:2325-2330.
27. Jueptner M, Stephan KM, Frith CD, Brooks DJ, Frackowiak RS, Passingham RE (1997) Anatomy of motor learning. I. Frontal cortex and attention to action. J Neurophysiol 77:1313-1324.
28. Johnson MT, Ebner TJ (2000) Processing of multiple kinematic signals in the cerebellum and motor cortices. Brain Res Brain Res Rev 33:155-168.
29. Johnson MT, Mason CR, Ebner TJ (2001) Central processes for the multiparametric control of arm movements in primates. Curr Opin Neurobiol 11:684-688.
30. Kakei S, Hoffman DS, Strick PL (1999) Muscle and movement representations in the primary motor cortex. Science 285:2136-2139.
31. Kakei S, Hoffman DS, Strick PL (2001) Direction of action is represented in the ventral premotor cortex. Nat Neurosci 4:1020-1025.
32. Kralik JD, Dimitrov DF, Krupa DJ, Katz DB, Cohen D, Nicolelis MAL (2001) Techniques for long-term multisite neuronal ensemble recordings in behaving animals. Methods 25:121-150.
33. Lebedev MA, Wise SP (2000) Oscillations in the premotor cortex: single-unit activity from awake, behaving monkeys. Exp Brain Res 130:195-215.
34. Lebedev MA, Wise SP (2001) Tuning for the orientation of spatial attention in dorsal premotor cortex. Eur J Neurosci 13:1002-1008.
35. Lebedev MA, Wise SP (2002) Insights into seeing and grasping: distinguishing the neural correlates of perception and action. Behav Cogn Neurosci Rev 1:108-129.
36. Lebedev MA, Denton JM, Nelson RJ (1994) Vibration-entrained and premovement activity in monkey primary somatosensory cortex. J Neurophysiol 72:1654-1673.
37. Lebedev MA, Douglass DK, Moody SL, Wise SP (2001) Prefrontal cortex neurons reflecting reports of a visual illusion. J Neurophysiol 85:1395-1411.
38. Lebedev MA, Carmena JM, Nicolelis MAL (2003) Directional tuning of frontal and parietal neurons during operation of brain-machine interface. Soc Neurosci Abstr 29:279.22.
39. Lebedev MA, Messinger A, Kralik JD, Wise SP (2004) Representation of attended versus remembered locations in prefrontal cortex. PLoS Biol 2:1919-1935.
40. Lee D, Port NL, Kruse W, Georgopoulos AP (1998) Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex. J Neurosci 18:1161-1170.
41. Leonardo M, Fieldman J, Sadato N, Campbell G, Ibanez V, Cohen L, Deiber M, Jezzard P, Pons T, Turner R, Le Bihan D, Hallett M (1995) A functional magnetic resonance imaging study of cortical regions associated with motor task execution and motor ideation in humans. Hum Brain Mapp 3:83-92.
42. Li CS, Padoa-Schioppa C, Bizzi E (2001) Neuronal correlates of motor performance and motor learning in the primary motor cortex of monkeys adapting to an external force field. Neuron 30:593-607.
43. Maravita A, Spence C, Driver J (2003) Multisensory integration and the body schema: close to hand and within reach. Curr Biol 13:R531-R539.
44. Maruishi M, Tanaka Y, Muranaka H, Tsuji T, Ozawa Y, Imaizumi S, Miyatani M, Kawahara J (2004) Brain activation during manipulation of the myoelectric prosthetic hand: a functional magnetic resonance imaging study. NeuroImage 21:1604-1611.
45. Moran DW, Schwartz AB (1999) Motor cortical representation of speed and direction during reaching. J Neurophysiol 82:2676-2692.
46. Murthy VN, Fetz EE (1992) Coherent 25-to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci USA 89:5670-5674.
47. Murthy VN, Fetz EE (1996a) Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior. J Neurophysiol 76:3949-3967.
48. Murthy VN, Fetz EE (1996b) Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol 76:3968-3982.
49. Musallam S, Corneil BD, Greger B, Scherberger H, Andersen RA (2004) Cognitive control signals for neural prosthetics. Science 305:258-262.
50. Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE (1999) Illusory arm movements activate cortical motor areas: a positron emission tomography study. J Neurosci 19:6134-6144.
51. Nicolelis MA, Baccala LA, Lin RC, Chapin JK (1995) Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268:1353-1358.
52. Nicolelis MAL (2001) Actions from thoughts. Nature 409:403-407.
53. Nicolelis MAL (2003) Brain-machine interfaces to restore motor function and probe neural circuits. Nat Rev Neurosci 4:417-422.
54. Nicolelis MAL, Ribeiro S (2002) Multielectrode recordings: the next steps. Curr Opin Neurobiol 12:602-606.
55. Nicolelis MAL, Ghazanfar AA, Faggin BM, Votaw S, Oliveira LM (1997) Reconstructing the engram: simultaneous, multisite, many single neuron recordings. Neuron 18:529-537.
56. Nicolelis MAL, Dimitrov D, Carmena JM, Crist R, Lehew G, Kralik JD, Wise SP (2003) Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci USA 100:11041-11046.
57. Ochiai T, Mushiake H, Tanji J (2002) Effects of image motion in the dorsal premotor cortex during planning of an arm movement. J Neurophysiol 88:2167-2171.
58. Padoa-Schioppa C, Li CS, Bizzi E (2004) Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. J Neurophysiol 91:449-473.
59. Paninski L, Fellows MR, Hatsopoulos NG, Donoghue JP (2004) Spatiotemporal tuning of motor cortical neurons for hand position and velocity. J Neurophysiol 91:515-532.
60. Patil PG, Carmena JM, Nicolelis MA, Turner DA (2004) Ensemble recordings of human subcortical neurons as a source of motor control signals for a brain-machine interface. Neurosurgery 55:27-35.
61. Paz R, Vaadia E (2004) Learning-induced improvement in encoding and decoding of specific movement directions by neurons in the primary motor cortex. PLoS Biol 2:264-274.
62. Paz R, Boraud T, Natan C, Bergman H, Vaadia E (2003) Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nat Neurosci 6:882-890.
63. Paz R, Wise SP, Vaadia E (2004) Viewing and doing: similar cortical mechanisms for perceptual and motor learning. Trends Neurosci 27:496-503.
64. Porro CA, Francescato MP, Cettolo V, Diamond ME, Baraldi P, Zuiani C, Bazzocchi M, di Prampero PE (1996) Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J Neurosci 16:7688-7698.
65. Riehle A, Grun S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278:1950-1953.
66. Riehle A, Grammont F, Diesmann M, Grun S (2000) Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation. J Physiol (Paris) 94:569-582.
67. Roux FE, Lotterie JA, Cassol E, Lazorthes Y, Sol JC, Berry I (2003) Cortical areas involved in virtual movement of phantom limbs: comparison with normal subjects. Neurosurgery 53:1342-1352.
68. Schwartz AB, Moran DW, Reina GA (2004) Differential representation of perception and action in the frontal cortex. Science 303:380-383.
69. Scott SH (2004) Optimal feedback control and the neural basis of volitional motor control. Nat Rev Neurosci 5:532-546.
70. Sergio LE, Kalaska JF (1998) Changes in the temporal pattern of primary motor cortex activity in a directional isometric force versus limb movement task. J Neurophysiol 80:1577-1583.
71. Serruya MD, Hatsopoulos NG, Paninski L, Fellows MR, Donoghue JP (2002) Instant neural control of a movement signal. Nature 416:141-142.
72. Shadlen MN, Newsome WT (1998) The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci 18:3870-3896.
73. Shen L, Alexander GE (1997a) Neural correlates of a spatial sensory-to-motor transformation in primary motor cortex. J Neurophysiol 77:1171-1194.
74. Shen L, Alexander GE (1997b) Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. J Neurophysiol 77:1195-1212.
75. Taylor DM, Tillery SI, Schwartz AB (2002) Direct cortical control of 3D neuroprosthetic devices. Science 296:1829-1832.
76. Todorov E (2000) Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci 3:391-398.
77. Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226-1235.
78. Wessberg J, Nicolelis MAL (2004) Optimizing a linear algorithm for real-time robotic control using chronic cortical ensemble recordings in monkeys. J Cogn Neurosci 16:1022-1035.
79. Wessberg J, Stambaugh CR, Kralik JD, Beck PD, Laubach M, Chapin JK, Kim J, Biggs SJ, Srinivasan MA, Nicolelis MA (2000) Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408:361-365.
80. Wise SP, Boussaoud D, Johnson PB, Caminiti R (1997) Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci 20:25-42.
81. Wise SP, Moody SL, Blomstrom KJ, Mitz AR (1998) Changes in motor cortical activity during visuomotor adaptation. Exp Brain Res 121:285-299.