Stop-event-related potentials from intracranial electrodes reveal a key role of premotor and motor cortices in stopping ongoing movements

Frontiers in Neuroengineering

Volumn , Issue JUNE, 2012, Pages

  Mattia, M ^a   Spadacenta, S ^b,c   Pavone, L ^b   Quarato, P ^b   Esposito, V ^b   Sparano, A ^b   Sebastiano, F ^b   Di Gennaro, G ^b   Morace, R ^b   Cantore, G ^b   Mirabella, G ^b,c  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b IRCCS NEUROMED   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Countermanding task; Electrocorticography (ECoG); Event related potentials (ERP); Reaching movements; Stop signal task; Volitional inhibition; Voluntary movements

Indexed keywords

ADULT; ARM MOVEMENT; ARTICLE; BRAIN COMPUTER INTERFACE; BRAIN MAPPING; BRODMANN AREA 9; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; COUNTERMANDING TASK; ELECTROCORTICOGRAPHY; ELECTRODE; EVENT RELATED POTENTIAL; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; HUMAN; INHIBITORY CONTROL; INTRACRANIAL ELECTRODE; INTRACTABLE EPILEPSY; MALE; MOTOR CORTEX; MOVEMENT INHIBITION; NERVE CONDUCTION; PREMOTOR CORTEX; PREOPERATIVE EVALUATION; PRIMARY MOTOR CORTEX; REACTION TIME; SCHOOL CHILD; SIGNAL NOISE RATIO; STOP EVENT RELATED POTENTIAL; TASK PERFORMANCE; TEMPORAL LOBE; VOLUNTARY MOVEMENT;

EID: 84875562766     PISSN: 16626443     EISSN: None     Source Type: Journal    
DOI: 10.3389/fneng.2012.00012     Document Type: Article

References (73)

1. Aron, A. R., Behrens, T. E., Smith, S., Frank, M. J., and Poldrack, R.A.(2007). Triangulating a cognitive control network using diffusion- weighted magnetic resonance imaging (MRI) and functional MRI. J. Neurosci. 27, 3743-3752.
2. Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., and Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat. Neurosci. 6, 115-116.
3. Aron, A. R., and Poldrack, R. A. (2006). Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. J. Neurosci. 26, 2424-2433.
4. Band, G. P., van der Molen, M. W., and Logan, G. D. (2003). Horse-race model simulations of the stop-signal procedure. Acta Psychol. (Amst.) 112, 105-142.
5. Bernat, E. M., Malone, S. M., Williams, W. J., Patrick, C. J., and Iacono, W. G. (2007). Decomposing delta, theta, and alpha time-frequency ERP activity from a visual oddball task using PCA. Int. J. Psychophysiol. 64, 62-74.
6. Boucher, L., Palmeri, T. J., Logan, G. D., and Schall, J. D. (2007). Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol. Rev. 114, 376-397.
7. Brass, M., and Haggard, P. (2007). To do or not to do: the neural signature of self-control. J. Neurosci. 27, 9141-9145.
8. Chamberlain, S. R., Blackwell, A. D., Fineberg, N. A., Robbins, T. W., and Sahakian, B. J. (2005). The neuropsychology of obsessive compulsive disorder: the importance of failures in cognitive and behavioral inhibition as candidate endopheno-typic markers. Neurosci. Biobehav. Rev. 29, 399-419.
9. Chamberlain, S. R., and Sahakian, B. J. (2007). The neuropsychiatry of impulsivity. Curr. Opin. Psychiatry 20, 255-261.
10. Chambers, C. D., Bellgrove, M. A., Stokes, M. G., Henderson, T. R., Garavan, H., Robertson, I. H., Morris, A. P., and Mattingley, J.B.(2006). Executive "brake failure" following deactivation of human frontal lobe. J. Cogn. Neurosci. 18, 444-455.
11. Cheney, P. D., and Fetz, E. E. (1980). Functional classes of primate corticomotoneuronal cells and their relation to active force. J. Neurophysiol. 44, 773-791.
12. Churchland, M. M., Cunningham, J. P., Kaufman, M. T., Ryu, S. I.,and Shenoy, K. V. (2010). Cortical preparatory activity: representation of movement or first cog in a dynamical machine? Neuron 68, 387-400.
13. Cimenser, A., Purdon, P. L., Pierce, E. T., Walsh, J. L., Salazar-Gomez, A. F., Harrell, P. G., Tavares-Stoeckel, C., Habeeb, K., and Brown, E. N. (2011). Tracking brain states under general anesthesia by using global coherence analysis. Proc. Natl. Acad. Sci. U.S.A. 108, 8832-8837.
14. Cisek, P., Crammond, D. J., and Kalaska, J. F. (2003). Neural activity in primary motor and dorsal pre-motor cortex in reaching tasks with the contralateral versus ipsilateral arm. J. Neurophysiol. 89, 922-942.
15. Corbetta, M., and Shulman, G. L. (2002). Control of goal-directed and stimulus driven attention in the brain. Nat. Rev. Neurosci. 3, 201-215.
16. Coxon, J. P., Stinear, C. M., and Byblow, W. D. (2006). Intracortical inhibition during volitional inhibition of prepared action. J. Neurophysiol. 95, 3371-3383.
17. Crammond, D. J., and Kalaska, J. F. (2000). Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. J. Neurophysiol. 84, 986-1005.
18. Daly, J. J., and Wolpaw, J. R. (2008). Brain-computer interfaces in neurological rehabilitation. Lancet Neurol. 7, 1032-1043.
19. Dimoska, A., and Johnstone, S. J. (2008). Effects of varying stop-signal probability on ERPs in the stop-signal task: do they reflect variations in inhibitory processing or simply novelty effects? Biol. Psychol. 77, 324-336.
20. Dobkin, B. H. (2007). Brain-computer interface technology as a tool to augment plasticity and outcomes for neurological rehabilitation. J. Physiol. 579, 637-642.
21. Donchin, O., Gribova, A., Steinberg, O., Mitz, A. R., Bergman, H., and Vaadia, E. (2002). Single-unit activity related to bimanual arm movements in the primary and supplementary motor cortices. J. Neurophysiol. 88, 3498-3517.
22. Evarts, E. V. (1968). Relation of pyramidal tract activity to force exerted during voluntary movement. J. Neurophysiol. 31, 14-27.
23. Fetz, E. E. (2007). Volitional control of neural activity: implications for brain-computer interfaces. J. Physiol. 579, 571-579.
24. Floden, D., and Stuss, D. T. (2006). Inhibitory control is slowed in patients with right superior medial frontal damage. J. Cogn. Neurosci. 18, 1843-1849.
25. Freeman, W. J., Holmes, M. D., Burke, B. C., and Vanhatalo, S. (2003). Spatial spectra of scalp EEG and EMG from awake humans. Clin. Neurophysiol. 114, 1053-1068.
26. Haggard, P. (2008). Human volition: towards a neuroscience of will. Nat. Rev. Neurosci. 9, 934-946.
27. Hanes, D. P., Patterson, W. F., and Schall, J. D. (1998). Role of frontal eye fields in countermanding sac-cades: visual, movement, and fixation activity. J. Neurophysiol. 79, 817-834.
28. Heinze, H. J., Münte, T. F., and Mangun, G. R. (1994). Cognitive Electrophysiology. Boston, MA: Birkhäuser.
29. Hjorth, B. (1975). An on-line transformation of EEG scalp potentials into orthogonal source derivations. Electroencephalogr. Clin. Neurophysiol. 39, 526-530.
30. Hyvärinen, A. (1999). Fast and robust fixed-point algorithms for independent component analysis. IEEE Trans. Neural Netw. 10, 626-634.
31. Hyvärinen, A., and Oja, E. (1997). A Fast Fixed-Point Algorithm for Independent Component Analysis. Neural Comput. 9, 1483-1492.
32. Jung, T. P., Makeig, S., McKeown, M. J., Bell, A. J., Lee, T. W., and Sejnowski, T. J. (2001). Imaging brain dynamics using independent component analysis. Proc. IEEE Inst. Electr. Electron. Eng. 89, 1107-1122.
33. Kawashima, R., Matsumura, M., Sadato, N., Naito, E., Waki, A., Nakamura, S., Matsunami, K., Fukuda, H., and Yonekura, Y. (1998). Regional cerebral blood flow changes in human brain related to ipsilateral and contralateral complex hand movements - a PET study. Eur. J. Neurosci. 10, 2254-2260.
34. Kok, A., Ramautar, J. R., De Ruiter, M. B., Band, G. P., and Ridderinkhof, K. R. (2004). ERP components associated with successful and unsuccessful stopping in a stop-signal task. Psychophysiology 41, 9-20.
35. Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C.S., Rainey, L., Kochunov, P. V., Nickerson, D., Mikiten, S. A., and Fox, P. T. (2000). Automated Talairach Atlas labels for functional brain mapping. Hum. Brain Mapp. 10, 120-131.
36. Leuthardt, E. C., Schalk, G., Wolpaw, J. R., Ojemann, J. G., and Moran, D. W. (2004). A brain-computer interface using electrocorticographic signals in humans. J. Neural Eng. 1, 63-71.
37. Levitt, H. (1971). Transformed up-down method in psychoacustics. J. Acoust. Soc. Am. 49, 467-477.
38. Li, C. S., Yan, P., Sinha, R., and Lee, T. W. (2008). Subcortical processes of motor response inhibition during a stop signal task. Neuroimage 41, 1352-1363.
39. Liotti, M., Pliszka, S. R., Perez, R. 3rd, Luus, B., Glahn, D., and Semrud-Clikeman, M. (2007). Electrophysiological correlates of response inhibition in children and adolescents with ADHD: influence of gender, age, and previous treatment history. Psychophysiology 44, 936-948.
40. Logan, G. D. (1994). "On the ability to inhibit thought and action: a users' guide to the stop signal paradigm," in Inhibitory Processes in Attention, Memory and Language, eds D. Dagenbach and T. H. Carr (San Diego, CA: Academic Press), 189-239.
41. Logan, G. D., and Cowan, W. B. (1984). On the ability to inhibit thought and action: a theory of an act of control. Psychol. Rev. 91, 295-327.
42. Mars, R. B., Coles, M. G., Hulstijn, W., and Toni, I. (2008). Delay-related cerebral activity and motor preparation. Cortex 44, 507-520.
43. Millán, J. D. R., Rupp, R., Müller-Putz, G. R., Murray-Smith, R., Giugliemma, C., Tangermann, M., Vidaurre, C., Cincotti, F., Kübler, A., Leeb, R., Neuper, C., Müller, K.-R., and Mattia, D. (2010). Combining brain-computer interfaces and assistive technologies: state-of-the-art and challenges. Front. Neurosci. 4:161. doi: 10.3389/fnins. 2010.00161
44. Miller, K. J., Makeig, S., Hebb, A. O., Rao, R. P., denNijs, M., and Ojemann, J. G. (2007). Cortical electrode localization from X-rays and simple mapping for electrocorticographic research: the "Location on Cortex" (LOC) package for MATLAB. J. Neurosci. Methods 162, 303-308.
45. Mink, J. W. (1996). The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381-425.
46. Mirabella, G. (2007). Endogenous inhibition and the neural basis of "free won't." J. Neurosci. 27, 13919-13920.
47. Mirabella, G., Iaconelli, S., Romanelli, P., Modugno, N., Lena, F., Manfredi, M., and Cantore, G. (2012). Deep brain stimulation of subthalamic nuclei affects arm response inhibition in Parkinson's patients. Cereb. Cortex 22, 1124-1132.
48. Mirabella, G., Pani, P., and Ferraina, S. (2008). Context influences on the preparation and execution of reaching movements. Cogn. Neuropsychol. 25, 996-1010.
49. Mirabella, G., Pani, P., and Ferraina, S. (2009). The presence of visual gap affects the duration of stopping process. Exp. Brain Res. 192, 199-209.
50. Mirabella, G., Pani, P., and Ferraina, S. (2011). Neural correlates of cognitive control of reaching movements in the dorsal premotor cortex of rhesus monkeys. J. Neurophysiol. 106, 1454-1466.
51. Mirabella, G., Pani, P., Paré, M., and Ferraina, S. (2006). Inhibitory control of reaching movements in humans. Exp. Brain Res. 174, 240-255.
52. Moritz, C. T., Perlmutter, S. I., and Fetz, E. E. (2008). Direct control of paralysed muscles by cortical neurons. Nature 456, 639-642.
53. Mostofsky, S. H., and Simmonds, D. J. (2008). Response inhibition and response selection: two sides of the same coin. J. Cogn. Neurosci. 20, 751-761.
54. Nachev, P., Wydell, H., O'Neill, K., Husain, M., and Kennard, C. (2007). The role of the pre-supplementary motor area in the control of action. Neuroimage 36(Suppl. 2), T155-T163.
55. Nambu, A., Tokuno, H., and Takada, M. (2002). Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci. Res. 43, 111-117.
56. Nicolelis, M. A. (2003). Brain-machine interfaces to restore motor function and probe neural circuits. Nat. Rev. Neurosci. 4, 417-422.
57. Osman, A., Kornblum, S., and Meyer, D. E. (1990). Does motor programming necessitate response execution? J. Exp. Psychol. Hum. Percept. Perform. 16, 183-198.
58. Ramautar, J. R., Kok, A., and Ridderinkhof, K. R. (2006). Effects of stop-signal modality on the N2/P3 complex elicited in the stop-signal paradigm. Biol. Psychol. 72, 96-109.
59. Schalk, G. (2010). Can electro-corticography (ECoG) support robust and powerful brain-computer interfaces? Front. Neuroeng. 3:9. doi: 10.3389/fneng. 2010.00009
60. Schalk, G., Miller, K. J., Anderson, N. R., Wilson, J. A., Smyth, M. D., Ojemann, J. G., Moran, D. W., Wolpaw, J. R., and Leuthardt, E. C. (2008). Two-dimensional movement control using electrocortico-graphic signals in humans. J. Neural Eng. 5, 75-84.
61. Schmajuk, N. A., Larrauri, J. A., Hagenbuch, N., Levin, E. D., Feldon, J., and Yee, B. K. (2006). Startle and prepulse inhibition as a function of background noise: a computational and experimental analysis. Behav. Brain Res. 170, 182-196.
62. Schwartz, A. B. (2004). Cortical neural prosthetics. Annu. Rev. Neurosci. 27, 487-507.
63. Srinivasan, R., Nunez, P. L., and Silberstein, R. B. (1998). Spatial filtering and neocortical dynamics: estimates of EEG coherence. IEEE Trans. Biomed. Eng. 45, 814-826.
64. Stinear, C. M., Coxon, J. P., and Byblow, W. D. (2009). Primary motor cortex and movement prevention: where Stop meets Go. Neurosci. Biobehav. Rev. 33, 662-673.
65. Swann, N., Tandon, N., Canolty, R., Ellmore, T. M., McEvoy, L. K., Dreyer, S., DiSano, M., and Aron, A. R. (2009). Intracranial EEG reveals a time- and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J. Neurosci. 29, 12675-12685.
66. Tallon-Baudry, C., and Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3, 151-162.
67. Tanji, J., and Evarts, E. V. (1976). Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J. Neurophysiol. 39, 1062-1068.
68. van den Wildenberg, W. P., van Boxtel, G. J., van der Molen, M. W., Bosch, D. A., Speelman, J. D., and Brunia, C. H. (2006). Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson's disease. J. Cogn. Neurosci. 18, 626-636.
69. Wang, W., Collinger, J. L., Perez, M. A., Tyler-Kabara, E. C., Cohen, L. G., Birbaumer, N., Brose, S. W., Schwartz, A. B., Boninger, M. L., and Weber, D. J. (2010). Neural interface technology for rehabilitation: exploiting and promoting neuroplasticity. Phys. Med. Rehabil. Clin. N. Am. 21, 157-178.
70. Weinrich, M., and Wise, S. P. (1982). The premotor cortex of the monkey. J. Neurosci. 2, 1329-1345.
71. Wetherill, G. B., and Levitt, H. (1965). Sequential estimation of points on a psychometric function. Br. J. Math. Stat. Psychol. 18, 1-10.
72. Wolpert, D. M., and Miall, R. C. (1996). Forward models for physiological motor control. Neural Netw. 9, 1265-1279.
73. Zandbelt, B. B., and Vink, M. (2010). On the role of the striatum in response inhibition. PLoS ONE 5:e13848. doi: 10.1371/journal. pone.0013848