Principles of neural ensemble physiology underlying the operation of brain-machine interfaces

Nature Reviews Neuroscience

Volumn 10, Issue 7, 2009, Pages 530-540

  Nicolelis, Miguel A L ^a,b,c   Lebedev, Mikhail A ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Edmond and Lily Safra International Institute of Neuroscience of Natal   (Brazil)

^c EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AUDITORY CORTEX; BRAIN; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; BRAIN MACHINE INTERFACE; CENTRAL NERVOUS SYSTEM; COMPUTER INTERFACE; ELECTRIC ACTIVITY; ELECTRICAL SYNAPSE; ELECTRODE; EXTRACELLULAR SPACE; MACHINE LEARNING; MAMMAL; MONKEY; MOTONEURON; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE CONDUCTION; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RECORDING; REVIEW; TASK PERFORMANCE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; ELECTRIC STIMULATION; ELECTRODES, IMPLANTED; HUMANS; MOTOR ACTIVITY; NEURONAL PLASTICITY; NEURONS; PARALYSIS; PROSTHESES AND IMPLANTS; USER-COMPUTER INTERFACE;

EID: 67649631831     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2653     Document Type: Review

References (192)

1. Carmena, J. M. et al. Learning to control a brain- machine interface for reaching and grasping by primates. PLoS Biol. 1, e42 (2003).
2. Chapin, J. K., Moxon, K. A., Markowitz, R. S. & Nicolelis, M. A. Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nature Neurosci. 2, 664-670 (1999).
3. Donoghue, J. P. Connecting cortex to machines: recent advances in brain interfaces. Nature Neurosci. . (Suppl.), 1085-1088 (2002).
4. Fetz, E. E. Volitional control of neural activity: implications for brain-computer interfaces. J. Physiol. 579, 571-579 (2007).
5. Kennedy, P. R. & Bakay, R. A. Restoration of neural output from a paralyzed patient by a direct brain connection. Neuroreport 9, 1707-1711 (1998).
6. Lebedev, M. A. & Nicolelis, M. A. Brain-machine interfaces: past, present and future. Trends Neurosci. 29, 536-546 (2006).
7. Musallam, S., Corneil, B. D., Greger, B., Scherberger, H. & Andersen, R. A. Cognitive control signals for neural prosthetics. Science 305, 258-262 (2004).
8. Nicolelis, M. A. Actions from thoughts. Nature 409, 403-407 (2001).
9. Nicolelis, M. A. Brain-machine interfaces to restore motor function and probe neural circuits. Nature Rev. Neurosci. 4, 417-422 (2003).
10. Schwartz, A. B., Cui, X. T., Weber, D. J. & Moran, D. W. Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 52, 205-220 (2006).
11. Serruya, M. D., Hatsopoulos, N. G., Paninski, L., Fellows, M. R. & Donoghue, J. P. Instant neural control of a movement signal. Nature 416, 141-142 (2002).
12. Taylor, D. M., Tillery, S. I. & Schwartz, A. B. Direct cortical control of 3D neuroprosthetic devices. Science 296, 1829-1832 (2002).
13. Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361-365 (2000).
14. Chapin, J. K. Neural prosthetic devices for quadriplegia. Curr. Opin. Neurol. 13, 671-675 (2000).
15. Donoghue, J. P., Nurmikko, A., Black, M. & Hochberg, L. R. Assistive technology and robotic control using motor cortex ensemble-based neural interface systems in humans with tetraplegia. J. Physiol. 579, 603-611 (2007).
16. Friehs, G. M., Zerris, V. A., Ojakangas, C. L., Fellows, M. R. & Donoghue, J. P. Brain-machine and brain- computer interfaces. Stroke 35, 2702-2705 (2004).
17. Mussa-Ivaldi, F. A. & Miller, L. E. Brain-machine interfaces: computational demands and clinical needs meet basic neuroscience. Trends Neurosci. 26, 329-334 (2003).
18. Birbaumer, N. Breaking the silence: brain-computer interfaces (BCI) for communication and motor control. Psychophysiology 43, 517-532 (2006).
19. Birbaumer, N. & Cohen, L. G. Brain-computer interfaces: communication and restoration of movement in paralysis. J. Physiol. 579, 621-636 (2007).
20. Cohen, E. D. Prosthetic interfaces with the visual system: biological issues. J. Neural Eng. 4, R14-R31 (2007).
21. Dobkin, B. H. Brain-computer interface technology as a tool to augment plasticity and outcomes for neurological rehabilitation. J. Physiol. 579, 637-642 (2007).
22. Kubler, A. & Kotchoubey, B. Brain-computer interfaces in the continuum of consciousness. Curr. Opin. Neurol. 20, 643-649 (2007).
23. Kubler, A. & Neumann, N. Brain-computer interfaces - the key for the conscious brain locked into a paralyzed body. Prog. Brain Res. 150, 513-525 (2005).
24. Leuthardt, E. C., Schalk, G., Moran, D. & Ojemann, J. G. The emerging world of motor neuroprosthetics: a neurosurgical perspective. Neurosurgery 59, 1-14 (2006).
25. Lotte, F., Congedo, M., Lecuyer, A., Lamarche, F. & Arnaldi, B. A review of classification algorithms for EEG-based brain-computer interfaces. J. Neural Eng. 4, R1-R13 (2007).
26. Mason, S. G., Bashashati, A., Fatourechi, M., Navarro, K. F. & Birch, G. E. A comprehensive survey of brain interface technology designs. Ann. Biomed. Eng. 35, 137-169 (2007).
27. Pfurtscheller, G. & Neuper, C. Future prospects of ERD/ERS in the context of brain-computer interface (BCI) developments. Prog. Brain Res. 159, 433-437 (2006).
28. Wolpaw, J. R. Brain-computer interfaces as new brain output pathways. J. Physiol. 579, 613-619 (2007).
29. Birbaumer, N. et al. A spelling device for the paralysed. Nature 398, 297-298 (1999).
30. Karim, A. A. et al. Neural internet: web surfing with brain potentials for the completely paralyzed. Neurorehabil. Neural Repair 20, 508-515 (2006).
31. Kennedy, P. R., Kirby, M. T., Moore, M. M., King, B. & Mallory, A. Computer control using human intracortical local field potentials. IEEE Trans. Neural Syst. Rehabil. Eng. 12, 339-344 (2004).
32. Nijboer, F. et al. A P300-based brain-computer interface for people with amyotrophic lateral sclerosis. Clin. Neurophysiol. 119, 1909-1916 (2008).
33. Nicolelis, M. A., Baccala, L. A., Lin, R. C. & Chapin, J. K. Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268, 1353-1358 (1995).
34. Nicolelis, M. A., Lin, R. C., Woodward, D. J. & Chapin, J. K. Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information. Nature 361, 533-536 (1993).
35. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175 (1971).
36. Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058 (1993).
37. Baker, S. N. et al. Multiple single unit recording in the cortex of monkeys using independently moveable microelectrodes. J. Neurosci. Methods 94, 5-17 (1999).
38. deCharms, R. C., Blake, D. T. & Merzenich, M. M. A multielectrode implant device for the cerebral cortex. J. Neurosci. Methods 93, 27-35 (1999).
39. Eliades, S. J. & Wang, X. Neural substrates of vocalization feedback monitoring in primate auditory cortex. Nature 453, 1102-1106 (2008).
40. Hatsopoulos, N., Joshi, J. & O'Leary, J. G. Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. J. Neurophysiol. 92, 1165-1174 (2004).
41. Jackson, A. & Fetz, E. E. Compact movable microwire array for long-term chronic unit recording in cerebral cortex of primates. J. Neurophysiol. 98, 3109-3118 (2007).
42. Lebedev, M. A. et al. Cortical ensemble adaptation to represent velocity of an artificial actuator controlled by a brain-machine interface. J. Neurosci. 25, 4681-4693 (2005).
43. Nicolelis, M. A. et al. Chronic, multisite, multielectrode recordings in macaque monkeys. Proc. Natl Acad. Sci. USA 100, 11041-11046 (2003).
44. Nicolelis, M. A. et al. Simultaneous encoding of tactile information by three primate cortical areas. Nature Neurosci. 1, 621-630 (1998).
45. Santhanam, G., Ryu, S. I., Yu, B. M., Afshar, A. & Shenoy, K. V. A high-performance brain-computer interface. Nature 442, 195-198 (2006).
46. Hochberg, L. R. et al. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 442, 164-171 (2006).
47. Patil, P. G., Carmena, J. M., Nicolelis, M. A. & Turner, D. A. Ensemble recordings of human subcortical neurons as a source of motor control signals for a brainmachine interface. Neurosurgery 55, 27-35 (2004).
48. Truccolo, W., Friehs, G. M., Donoghue, J. P. & Hochberg, L. R. Primary motor cortex tuning to intended movement kinematics in humans with tetraplegia. J. Neurosci. 28, 1163-1178 (2008).
49. Bizzi, E., Accornero, N., Chapple, W. & Hogan, N. Arm trajectory formation in monkeys. Exp. Brain Res. 46, 139-143 (1982).
50. Bizzi, E., Mussa-Ivaldi, F. A. & Giszter, S. Computations underlying the execution of movement: a biological perspective. Science 253, 287-291 (1991).
51. Cohen, Y. E. & Andersen, R. A. A common reference frame for movement plans in the posterior parietal cortex. Nature Rev. Neurosci. 3, 553-562 (2002).
52. Evarts, E. V. & Fromm, C. Information processing in the sensorimotor cortex during voluntary movement. Prog. Brain Res. 54, 143-155 (1980).
53. Georgopoulos, A. P. Spatial coding of visually guided arm movements in primate motor cortex. Can. J. Physiol. Pharmacol. 66, 518-526 (1988).
54. Georgopoulos, A. P., Schwartz, A. B. & Kettner, R. E. Neuronal population coding of movement direction. Science 233, 1416-1419 (1986).
55. Kakei, S., Hoffman, D. S. & Strick, P. L. Muscle and movement representations in the primary motor cortex. Science 285, 2136-2139 (1999).
56. Lebedev, M. A. & Wise, S. P. Insights into seeing and grasping: distinguishing the neural correlates of perception and action. Behav. Cogn. Neurosci. Rev. 1, 108-129 (2002).
57. Paz, R., Wise, S. P. & Vaadia, E. Viewing and doing: similar cortical mechanisms for perceptual and motor learning. Trends Neurosci. 27, 496-503 (2004).
58. Polit, A. & Bizzi, E. Processes controlling arm movements in monkeys. Science 201, 1235-1237 (1978).
59. Todorov, E. Optimality principles in sensorimotor control. Nature Neurosci. 7, 907-915 (2004).
60. Wise, S. P., di Pellegrino, G. & Boussaoud, D. The premotor cortex and nonstandard sensorimotor mapping. Can. J. Physiol. Pharmacol. 74, 469-482 (1996).
61. Andersen, R. A., Musallam, S. & Pesaran, B. Selecting the signals for a brain-machine interface. Curr. Opin. Neurobiol. 14, 720-726 (2004).
62. Bashashati, A., Fatourechi, M., Ward, R. K. & Birch, G. E. A survey of signal processing algorithms in brain-computer interfaces based on electrical brain signals. J. Neural Eng. 4, R32-57 (2007).
63. Lilly, J. C. in Biological and Biochemical Bases of Behavior (eds Harlow, H. F. & Woolsey, C. N.) 83-100 (Univ. of Wisconsin Press, Madison, Wisconsin, 1958).
64. Lilly, J. C. Distribution of 'motor' functions in the cerebral cortex in the conscious, intact monkey. Science Abstr. 124, 937 (1956).
65. Gerstein, G. L. & Aertsen, A. M. Representation of cooperative firing activity among simultaneously recorded neurons. J. Neurophysiol. 54, 1513-1528 (1985).
66. Gerstein, G. L., Perkel, D. H. & Dayhoff, J. E. Cooperative firing activity in simultaneously recorded populations of neurons: detection and measurement. J. Neurosci. 5, 881-889 (1985).
67. Gerstein, G. L., Perkel, D. H. & Subramanian, K. N. Identification of functionally related neural assemblies. Brain Res. 140, 43-62 (1978).
68. Kruger, J. & Bach, M. Simultaneous recording with 30 microelectrodes in monkey visual cortex. Exp. Brain Res. 41, 191-194 (1981).
69. McNaughton, B. L., Barnes, C. A. & O'Keefe, J. The contributions of position, direction, and velocity to single unit activity in the hippocampus of freelymoving rats. Exp. Brain Res. 52, 41-49 (1983).
70. Shin, H. C. & Chapin, J. K. Mapping the effects of motor cortex stimulation on single neurons in the dorsal column nuclei in the rat: direct responses and afferent modulation. Brain Res. Bull. 22, 245-252 (1989).
71. Barlow, H. B. Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1, 371-394 (1972).
72. Hubel, D. H. & Wiesel, T. N. Early exploration of the visual cortex. Neuron 20, 401-412 (1998).
73. Averbeck, B. B. & Lee, D. Coding and transmission of information by neural ensembles. Trends Neurosci. 27, 225-230 (2004).
74. Covey, E. Neural population coding and auditory temporal pattern analysis. Physiol. Behav. 69, 211-220 (2000).
75. Doetsch, G. S. Patterns in the brain. Neuronal population coding in the somatosensory system. Physiol. Behav. 69, 187-201 (2000).
76. Sakurai, Y. Population coding by cell assemblies - what it really is in the brain. Neurosci. Res. 26, 1-16 (1996).
77. Young, T. On the theory of light and colours. Philos. Trans. R. Soc. Lond. B Biol. Sci. 92, 12-48 (1802).
78. Hebb, D. O. The Organization of Behavior: A Neuropsychological Theory (Wiley, New York, 1949).
79. Barlow, H. B. in The Cognitive Neurosciences (ed. Gazzaniga, M.) 415-435 (MIT Press, Cambridge, 1995).
80. Barlow, H. B. Pattern recognition and the responses of sensory neurons. Ann. NY Acad. Sci. 156, 872-881 (1969).
81. Cajal, R. Histology of the Nervous System of Man and Vertebrates (Oxford Univ. Press, New York, 1899).
82. Hubel, D. H. Eye, Brain and Vision (W. H. Freeman and Company, New York, 1988).
83. Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106-154 (1962).
84. Breakspear, M. & Stam, C. J. Dynamics of a neural system with a multiscale architecture. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 1051-1074 (2005).
85. Serences, J. T. & Yantis, S. Selective visual attention and perceptual coherence. Trends Cogn. Sci. 10, 38-45 (2006).
86. Simon, S. A., de Araujo, I. E., Gutierrez, R. & Nicolelis, M. A. The neural mechanisms of gustation: a distributed processing code. Nature Rev. Neurosci. 7, 890-901 (2006).
87. Bichot, N. P., Thompson, K. G., Chenchal Rao, S. & Schall, J. D. Reliability of macaque frontal eye field neurons signaling saccade targets during visual search. J. Neurosci. 21, 713-725 (2001).
88. Brecht, M., Schneider, M., Sakmann, B. & Margrie, T. W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704-710 (2004).
89. Houweling, A. R. & Brecht, M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451, 65-68 (2008).
90. Shadlen, M. N. & Newsome, W. T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916-1936 (2001).
91. Fetz, E. E. Operant conditioning of cortical unit activity. Science 163, 955-958 (1969).
92. Fetz, E. E. & Finocchio, D. V. Correlations between activity of motor cortex cells and arm muscles during operantly conditioned response patterns. Exp. Brain Res. 23, 217-240 (1975).
93. Fetz, E. E. & Finocchio, D. V. Operant conditioning of specific patterns of neural and muscular activity. Science 174, 431-435 (1971).
94. Moritz, C. T., Perlmutter, S. I. & Fetz, E. E. Direct control of paralysed muscles by cortical neurons. Nature 456, 639-642 (2008).
95. Eliades, S. J. & Wang, X. Chronic multi-electrode neural recording in free-roaming monkeys. J. Neurosci. Methods 172, 201-214 (2008).
96. Guillory, K. S. & Normann, R. A. A 100-channel system for real time detection and storage of extracellular spike waveforms. J. Neurosci. Methods 91, 21-29 (1999).
97. Mountcastle, V. B., Reitboeck, H. J., Poggio, G. F. & Steinmetz, M. A. Adaptation of the Reitboeck method of multiple microelectrode recording to the neocortex of the waking monkey. J. Neurosci. Methods 36, 77-84 (1991).
98. Musallam, S., Bak, M. J., Troyk, P. R. & Andersen, R. A. A floating metal microelectrode array for chronic implantation. J. Neurosci. Methods 160, 122-127 (2007).
99. Nicolelis, M. A., Ghazanfar, A. A., Faggin, B. M., Votaw, S. & Oliveira, L. M. Reconstructing the engram: simultaneous, multisite, many single neuron recordings. Neuron 18, 529-537 (1997).
100. Grinvald, A. Imaging input and output dynamics of neocortical networks in vivo: exciting times ahead. Proc. Natl Acad. Sci. USA 102, 14125-14126 (2005).
101. Grinvald, A., Frostig, R. D., Siegel, R. M. & Bartfeld, E. High-resolution optical imaging of functional brain architecture in the awake monkey. Proc. Natl Acad. Sci. USA 88, 11559-11563 (1991).
102. Lendvai, B., Stern, E. A., Chen, B. & Svoboda, K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876-881 (2000).
103. Logothetis, N. K., Guggenberger, H., Peled, S. & Pauls, J. Functional imaging of the monkey brain. Nature Neurosci. 2, 555-562 (1999).
104. Nikolenko, V., Poskanzer, K. E. & Yuste, R. Two-photon photostimulation and imaging of neural circuits. Nature Methods 4, 943-950 (2007).
105. Ohki, K., Chung, S., Ch'ng, Y. H., Kara, P. & Reid, R. C. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433, 597-603 (2005).
106. Ohki, K. et al. Highly ordered arrangement of single neurons in orientation pinwheels. Nature 442, 925-928 (2006).
107. Rainer, G., Augath, M., Trinath, T. & Logothetis, N. K. Nonmonotonic noise tuning of BOLD fMRI signal to natural images in the visual cortex of the anesthetized monkey. Curr. Biol. 11, 846-854 (2001).
108. Siegel, R. M., Duann, J. R., Jung, T. P. & Sejnowski, T. Spatiotemporal dynamics of the functional architecture for gain fields in inferior parietal lobule of behaving monkey. Cereb. Cortex 17, 378-390 (2007).
109. Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D. W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161-165 (1997).
110. Ts'o, D. Y., Frostig, R. D., Lieke, E. E. & Grinvald, A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417-420 (1990).
111. Yuste, R. Fluorescence microscopy today. Nature Methods 2, 902-904 (2005).
112. Schmidt, E. M. Single neuron recording from motor cortex as a possible source of signals for control of external devices. Ann. Biomed. Eng. 8, 339-349 (1980).
113. Isaacs, R. E., Weber, D. J. & Schwartz, A. B. Work toward real-time control of a cortical neural prothesis. IEEE Trans. Rehabil. Eng. 8, 196-198 (2000).
114. Wolpaw, J. R. & McFarland, D. J. Control of a twodimensional movement signal by a noninvasive braincomputer interface in humans. Proc. Natl Acad. Sci. USA 101, 17849-17854 (2004).
115. Fitzsimmons, N. A., Drake, W., Hanson, T. L., Lebedev, M. A. & Nicolelis, M. A. Primate reaching cued by multichannel spatiotemporal cortical microstimulation. J. Neurosci. 27, 5593-5602 (2007).
116. Lebedev, M. A., O'Doherty, J. E. & Nicolelis, M. A. Decoding of temporal intervals from cortical ensemble activity. J. Neurophysiol. 99, 166-186 (2008).
117. Santucci, D. M., Kralik, J. D., Lebedev, M. A. & Nicolelis, M. A. Frontal and parietal cortical ensembles predict single-trial muscle activity during reaching movements in primates. Eur. J. Neurosci. 22, 1529-1540 (2005).
118. Wessberg, J. & Nicolelis, M. A. Optimizing a linear algorithm for real-time robotic control using chronic cortical ensemble recordings in monkeys. J. Cogn. Neurosci. 16, 1022-1035 (2004).
119. Zacksenhouse, M. et al. Cortical modulations increase in early sessions with brain-machine interface. PLoS ONE 2, e619 (2007).
120. Costa, R. M. et al. Rapid alterations in corticostriatal ensemble coordination during acute dopaminedependent motor dysfunction. Neuron 52, 359-369 (2006).
121. Dzirasa, K. et al. Dopaminergic control of sleep-wake states. J. Neurosci. 26, 10577-10589 (2006).
122. Lin, S. C., Gervasoni, D. & Nicolelis, M. A. Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles. J. Neurophysiol. 96, 3209-3219 (2006).
123. Haykin, S. Adaptive Filter Theory (PrenticeHall, Upper Saddle River, New Jersey, 2002).
124. Fetz, E. E. Are movement parameters recognizably coded in activity of single neurons? Behav. Brain Sci. 15, 679-690 (1992).
125. Carmena, J. M., Lebedev, M. A., Henriquez, C. S. & Nicolelis, M. A. Stable ensemble performance with single-neuron variability during reaching movements in primates. J. Neurosci. 25, 10712-10716 (2005).
126. Ghazanfar, A. A., Krupa, D. J. & Nicolelis, M. A. Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons. Exp. Brain Res. 141, 88-100 (2001).
127. Ghazanfar, A. A. & Nicolelis, M. A. Spatiotemporal properties of layer V neurons of the rat primary somatosensory cortex. Cereb. Cortex 9, 348-361 (1999).
128. Ghazanfar, A. A., Stambaugh, C. R. & Nicolelis, M. A. Encoding of tactile stimulus location by somatosensory thalamocortical ensembles. J. Neurosci. 20, 3761-3775 (2000).
129. de Araujo, I. E. et al. Food reward in the absence of taste receptor signaling. Neuron 57, 930-941 (2008).
130. Soares, E. S. et al. Behavioral and neural responses to gustatory stimuli delivered non-contingently through intra-oral cannulas. Physiol. Behav. 92, 629-642 (2007).
131. Glaser, E. M. & Ruchkin, D. S. Principles of Neurobiological Signal Analysis (Academic Press, New York, 1976).
132. Quian Quiroga, R. & Panzeri, S. Extracting information from neuronal populations: information theory and decoding approaches. Nature Rev. Neurosci. 10, 173-185 (2009).
133. Faisal, A. A., Selen, L. P. & Wolpert, D. M. Noise in the nervous system. Nature Rev. Neurosci. 9, 292-303 (2008).
134. Fontanini, A. & Katz, D. B. Behavioral states, network states, and sensory response variability. J. Neurophysiol. 100, 1160-1168 (2008).
135. Getting, P. A. Emerging principles governing the operation of neural networks. Annu. Rev. Neurosci. 12, 185-204 (1989).
136. Nicolelis, M. A. Computing with thalamocortical ensembles during different behavioural states. J. Physiol. 566, 37-47 (2005).
137. van Beers, R. J., Baraduc, P. & Wolpert, D. M. Role of uncertainty in sensorimotor control. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 1137-1145 (2002).
138. Abeles, M. Neural Circuits of the Cerebral Cortex (Cambridge Univ. Press, Cambridge, 1991).
139. Chestek, C. A. et al. Single-neuron stability during repeated reaching in macaque premotor cortex. J. Neurosci. 27, 10742-10750 (2007).
140. Brooks, V. B., Adrien, J. & Dykes, R. W. Task-related discharge of neurons in motor cortex and effects of denatate cooling. Brain Res. 40, 85-88 (1972).
141. Niki, H. & Watanabe, M. Prefrontal unit activity and delayed response: relation to cue location versus direction of response. Brain Res. 105, 79-88 (1976).
142. Sanchez, J. C. et al. Ascertaining the importance of neurons to develop better brain-machine interfaces. IEEE Trans. Biomed. Eng. 51, 943-953 (2004).
143. Ghazanfar, A. A. & Schroeder, C. E. Is neocortex essentially multisensory? Trends Cogn. Sci. 10, 278-285 (2006).
144. Graziano, M. S. & Gross, C. G. Spatial maps for the control of movement. Curr. Opin. Neurobiol. 8, 195-201 (1998).
145. Avillac, M., Deneve, S., Olivier, E., Pouget, A. & Duhamel, J. R. Reference frames for representing visual and tactile locations in parietal cortex. Nature Neurosci. 8, 941-949 (2005).
146. Benedek, G., Eordegh, G., Chadaide, Z. & Nagy, A. Distributed population coding of multisensory spatial information in the associative cortex. Eur. J. Neurosci. 20, 525-529 (2004).
147. Bridgeman, B. Multiplexing in single cells of the alert monkeys visual cortex during brightness discrimination. Neuropsychologia 20, 33-42 (1982).
148. Driver, J. & Noesselt, T. Multisensory interplay reveals crossmodal influences on 'sensory-specific' brain regions, neural responses, and judgments. Neuron 57, 11-23 (2008).
149. Friedrich, R. W., Habermann, C. J. & Laurent, G. Multiplexing using synchrony in the zebrafish olfactory bulb. Nature Neurosci. 7, 862-871 (2004).
150. Lebedev, M. A., Messinger, A., Kralik, J. D. & Wise, S. P. Representation of attended versus remembered locations in prefrontal cortex. PLoS Biol. 2, e365 (2004).
151. Stanford, T. R. & Stein, B. E. Superadditivity in multisensory integration: putting the computation in context. Neuroreport 18, 787-792 (2007).
152. Stein, B. E. & Stanford, T. R. Multisensory integration: current issues from the perspective of the single neuron. Nature Rev. Neurosci. 9, 255-266 (2008).
153. Fitzsimmons, N. A., Lebedev, M. A., Peikon, I. D. & Nicolelis, M. A. Decoding of monkey bipedal walking from cortical neuronal ensembles. Front. Integr. Neurosci. 3, 3 (2009).
154. Alexander, R. M. Bipedal animals, and their differences from humans. J. Anat. 204, 321-330 (2004).
155. Dietz, V. Do human bipeds use quadrupedal coordination? Trends Neurosci. 25, 462-467 (2002).
156. Prilutsky, B. I., Sirota, M. G., Gregor, R. J. & Beloozerova, I. N. Quantification of motor cortex activity and full-body biomechanics during unconstrained locomotion. J. Neurophysiol. 94, 2959-2969 (2005).
157. Narayanan, N. S., Kimchi, E. Y. & Laubach, M. Redundancy and synergy of neuronal ensembles in motor cortex. J. Neurosci. 25, 4207-4216 (2005).
158. Shadlen, M. N. & Newsome, W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18, 3870-3896 (1998).
159. Schwartz, A. B., Taylor, D. M. & Tillery, S. I. Extraction algorithms for cortical control of arm prosthetics. Curr. Opin. Neurobiol. 11, 701-707 (2001).
160. Velliste, M., Perel, S., Spalding, M. C., Whitford, A. S. & Schwartz, A. B. Cortical control of a prosthetic arm for self-feeding. Nature 453, 1098-1101 (2008).
161. Cohen, D. & Nicolelis, M. A. Reduction of single-neuron firing uncertainty by cortical ensembles during motor skill learning. J. Neurosci. 24, 3574-3582 (2004).
162. Lashley, K. S. An examination of the "continuity theory" as applied to discrimination learning. J. Gen. Psychol. 26, 241-265 (1942).
163. Lashley, K. S. The mechanism of vision: XV. Preliminary studies of the rat's capacity for detail vision. J. Gen. Psychol. 18, 123-193 (1938).
164. Leonardo, A. Degenerate coding in neural systems. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 995-1010 (2005).
165. Reeke, G. N. Jr & Edelman, G. M. Selective networks and recognition automata. Ann. NY Acad. Sci. 426, 181-201 (1984).
166. Tononi, G., Sporns, O. & Edelman, G. M. Measures of degeneracy and redundancy in biological networks. Proc. Natl Acad. Sci. USA 96, 3257-3262 (1999).
167. Merzenich, M. M. et al. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8, 33-55 (1983).
168. Merzenich, M. M. et al. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10, 639-665 (1983).
169. Krupa, D. J., Wiest, M. C., Shuler, M. G., Laubach, M. & Nicolelis, M. A. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 304, 1989-1992 (2004).
170. Chen, L. L. & Wise, S. P. Evolution of directional preferences in the supplementary eye field during acquisition of conditional oculomotor associations. J. Neurosci. 16, 3067-3081 (1996).
171. Laubach, M., Wessberg, J. & Nicolelis, M. A. Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405, 567-571 (2000).
172. Li, C. S., Padoa-Schioppa, C. & Bizzi, E. 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 (2001).
173. Mitz, A. R., Godschalk, M. & Wise, S. P. Learningdependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations. J. Neurosci. 11, 1855-1872 (1991).
174. Padoa-Schioppa, C., Li, C. S. & Bizzi, E. Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. J. Neurophysiol. 91, 449-473 (2004).
175. Padoa-Schioppa, C., Li, C. S. & Bizzi, E. Neuronal correlates of kinematics-to-dynamics transformation in the supplementary motor area. Neuron 36, 751-765 (2002).
176. Paz, R., Boraud, T., Natan, C., Bergman, H. & Vaadia, E. Preparatory activity in motor cortex reflects learning of local visuomotor skills. Nature Neurosci. 6, 882-890 (2003).
177. Paz, R. & Vaadia, E. Learning-induced improvement in encoding and decoding of specific movement directions by neurons in the primary motor cortex. PLoS Biol. 2, e45 (2004).
178. Rokni, U., Richardson, A. G., Bizzi, E. & Seung, H. S. Motor learning with unstable neural representations. Neuron 54, 653-666 (2007).
179. Wise, S. P., Moody, S. L., Blomstrom, K. J. & Mitz, A. R. Changes in motor cortical activity during visuomotor adaptation. Exp. Brain Res. 121, 285-299 (1998).
180. de Lange, F. P., Roelofs, K. & Toni, I. Motor imagery: a window into the mechanisms and alterations of the motor system. Cortex 44, 494-506 (2008).
181. Decety, J. The neurophysiological basis of motor imagery. Behav. Brain Res. 77, 45-52 (1996).
182. Jeannerod, M. & Frak, V. Mental imaging of motor activity in humans. Curr. Opin. Neurobiol. 9, 735-739 (1999).
183. Neuper, C., Muller-Putz, G. R., Scherer, R. & Pfurtscheller, G. Motor imagery and EEG-based control of spelling devices and neuroprostheses. Prog. Brain Res. 159, 393-409 (2006).
184. Jackson, A., Mavoori, J. & Fetz, E. E. Long-term motor cortex plasticity induced by an electronic neural implant. Nature 444, 56-60 (2006).
185. Bach-y-Rita, P. & S., W. K. Sensory substitution and the human-machine interface. Trends Cogn. Sci. 7, 541-546 (2003).
186. Segond, H., Weiss, D. & Sampaio, E. Human spatial navigation via a visuo-tactile sensory substitution system. Perception 34, 1231-1249 (2005).
187. Eliades, S. J. & Wang, X. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb. Cortex 15, 1510-1523 (2005).
188. Lin, S. C. & Nicolelis, M. A. Neuronal ensemble bursting in the basal forebrain encodes salience irrespective of valence. Neuron 59, 138-149 (2008).
189. Pantoja, J. et al. Neuronal activity in the primary somatosensory thalamocortical loop is modulated by reward contingency during tactile discrimination. J. Neurosci. 27, 10608-10620 (2007).
190. Pereira, A. et al. Processing of tactile information by the hippocampus. Proc. Natl Acad. Sci. USA 104, 18286-18291 (2007).
191. Stapleton, J. R., Lavine, M. L., Nicolelis, M. A. & Simon, S. A. Ensembles of gustatory cortical neurons anticipate and discriminate between tastants in a single lick. Front. Neurosci. 1, 161-174 (2007).
192. Kim, H. K. et al. Continuous shared control stabilizes reach and grasping with brain-machine interfaces. IEEE Trans. Biomed. Eng. 53, 1164-1173 (2005).