Neural correlates of cognitive control of reaching movements in the dorsal premotor cortex of rhesus monkeys

Journal of Neurophysiology

Volumn 106, Issue 3, 2011, Pages 1454-1466

  Mirabella, G ^a,b   Pani, P ^a   Ferraina, S ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Countermanding task; Single units; Stop task; Voluntary control

Indexed keywords

ANIMAL EXPERIMENT; ARM MOVEMENT; ARTICLE; BEHAVIORAL SCIENCE; COGNITION; MALE; NERVE CELL; NERVOUS SYSTEM FUNCTION; NONHUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; RHESUS MONKEY; TASK PERFORMANCE; VOLUNTARY MOVEMENT;

ANIMALS; COGNITION; MACACA MULATTA; MALE; MOTOR CORTEX; MOVEMENT; NEURONS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE;

EID: 80052580395     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00995.2010     Document Type: Article

References (82)

1. Aizawa H, Tanji J. Corticocortical and thalamocortical responses of neurons in the monkey primary motor cortex and their relation to a trained motor task. J Neurophysiol 71: 550-60, 1994.
2. Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA. Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27: 3743-3752, 2007.
3. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW. Stopsignal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6: 115-116, 2003.
4. Aron AR, Poldrack RA. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26: 2424-2433, 2006.
5. Band GP, van der Molen MW, Logan GD. Horse-race model simulations of the stop-signal procedure. Acta Psychol (Amst) 112: 105-142, 2003.
6. Bergeron A, Guitton D. In multiple-step gaze shifts: omnipause (OPNs) and collicular fixation neurons encode gaze position error; OPNs gate saccades. J Neurophysiol 88: 1726-1742, 2002.
7. Boucher L, Palmeri TJ, Logan GD, Schall JD. Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol Rev 114: 376-397, 2007.
8. Boussaoud D, Barth TM, Wise SP. Effects of gaze on apparent visual responses of frontal cortex neurons. Exp Brain Res 93: 423-434, 1993.
9. Boussaoud D, Jouffrais C, Bremmer F. Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey. J Neurophysiol 80: 1132-1150, 1998.
10. Büttner-Ennever JA, Cohen B, Pause M, Fries W. Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man. J Comp Neurol 267: 307-321, 1988.
11. Carey DP. Eye-hand coordination: eye to hand or hand to eye? Curr Biol 10: R416-R419, 2000.
12. Chambers CD, Bellgrove MA, Stokes MG, Henderson TR, Garavan H, Robertson IH, Morris AP, Mattingley JB. Executive "brake failure" following deactivation of human frontal lobe. J Cogn Neurosci 18: 444-455, 2006.
13. Chen X, Scangos KW, Stuphorn V. Supplementary motor area exerts proactive and reactive control of arm movements. J Neurosci 30: 14657-75, 2010.
14. Cheney PD, Fetz EE. Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol 44: 773-791, 1980.
15. Cheney PD, Fetz EE, Palmer SS. Patterns of facilitation and suppression of antagonist forelimb muscles from motor cortex sites in the awake monkey. J Neurophysiol 53: 805-820, 1985.
16. Churchland MM, Shenoy KV. Delay of movement caused by disruption of cortical preparatory activity. J Neurophysiol 97: 348-359, 2007.
17. Churchland MM, Yu BM, Ryu SI, Santhanam G, Shenoy KV. Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci 26: 3697-3712, 2006.
18. Cisek P, Kalaska JF. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45: 801-814, 2005.
19. Coxon JP, Stinear CM, Byblow WD. Intracortical inhibition during volitional inhibition of prepared action. J Neurophysiol 95: 3371-3383, 2006.
20. Crammond DJ, Kalaska JF. Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. J Neurophysiol 84: 986-1005, 2000.
21. Di Pellegrino G, Wise SP. Effects of attention on visuomotor activity in the premotor and prefrontal cortex of a primate. Somatosens Mot Res 10: 245-262, 1993.
22. Dum RP, Strick PL. Spinal cord terminations of the medial wall motor areas in macaque monkeys. J Neurosci 16: 6513-6525, 1996.
23. Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav 77: 677-682, 2002.
24. Evarts EV. Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31: 14-27, 1968.
25. Floden D, Stuss DT. Inhibitory control is slowed in patients with right superior medial frontal damage. J Cogn Neurosci 18: 1843-1849, 2006.
26. Fuchs AF, Robinson DA. A method for measuring horizontal and vertical eye movement chronically in the monkey. J Appl Physiol 21: 1068-1070, 1966.
27. Fujii N, Mushiake H, Tanji J. Rostrocaudal distinction of the dorsal premotor area based on oculomotor involvement. J Neurophysiol 83: 1764-1769, 2000.
28. Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT. Interruption of motor cortical discharge subserving aimed arm movements. Exp Brain Res 49: 327-340, 1983.
29. Ghosh S, Porter R. Corticocortical synaptic influences on morphologically identified pyramidal neurons in the motor cortex of the monkey. J Physiol 400: 617-629, 1988.
30. Hanes DP, Patterson WF, Schall JD. Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J Neurophysiol 79: 817-834, 1998.
31. Hanes DP, Schall JD. Countermanding saccades in macaque. Vis Neurosci 12: 929-937, 1995.
32. Hoshi E, Tanji J. Differential involvement of neurons in the dorsal and ventral premotor cortex during processing of visual signals for action planning. J Neurophysiol 95: 3596-3616, 2006.
33. Ito S, Stuphorn V, Brown JW, Schall JD. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302: 120-122, 2003.
34. Johnson PB, Ferraina S, Bianchi L, Caminiti R. Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6: 102-119, 1996.
35. Kalaska JF, Crammond DJ. Deciding not to GO: neuronal correlates of response selection in a GO/NOGO task in primate premotor and parietal cortex. Cereb Cortex 5: 410-428, 1995.
36. Kaufman MT, Churchland MM, Santhanam G, Yu BM, Afshar A, Ryu SI, Shenoy KV. Roles of monkey premotor neuron classes in movement preparation and execution. J Neurophysiol 104: 799-810, 2010.
37. Kudo K, Ohtsuki T. Functional modification of agonist-antagonist electromyographic activity for rapid movement inhibition. Exp Brain Res 122: 23-30, 1998.
38. Lemon RN, Mantel GW, Muir RB. Corticospinal facilitation of hand muscles during voluntary movement in the conscious monkey. J Physiol 381: 497-527, 1986.
39. Lemon RN, Muir RB, Mantel GW. The effects upon the activity of hand and forearm muscles of intracortical stimulation in the vicinity of corticomotor neurones in the conscious monkey. Exp Brain Res 66: 621-637, 1987.
40. Levitt H. Transformed up-down method in psychoacoustics. J Acoust Soc Am 49: 467-477, 1971.
41. Li CS, Yan P, Sinha R, Lee TW. Subcortical processes of motor response inhibition during a stop signal task. Neuroimage 41: 1352-1363, 2008.
42. Logan GD. On the ability to inhibit thought and action: a users' guide to the stop signal paradigm. In: Inhibitory Processes in Attention, Memory and Language, edited by Dagenbach D, Carr TH. San Diego, CA: Academic, 1994, p. 189-239.
43. Logan GD, Cowan WB. On the ability to inhibit thought and action: a theory of an act of control. Psychol Rev 91: 295-327, 1984.
44. Logothetis NK. The underpinnings of the BOLD functional magnetic resonance imaging signal. J Neurosci 23: 3963-3971, 2003.
45. Mattia M, Ferraina S, Del Giudice P. Dissociated multi-unit activity and local field potentials: a theory inspired analysis of a motor decision task. Neuroimage 52: 812-823, 2010.
46. McKiernan BJ, Marcario JK, Karrer JH, Cheney PD. Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit and intrinsic hand muscles during a reach and prehension task. J Neurophysiol 80: 1961-1980, 1998.
47. Merchant H, Naselaris T, Georgopoulos AP. Dynamic sculpting of directional tuning in the primate motor cortex during three-dimensional reaching. J Neurosci 28: 9164-9172, 2008.
48. Miller J, Riehle A, Requin J. Effects of preliminary perceptual output on neuronal activity of the primary motor cortex. J Exp Psychol Hum Percept Perform 18: 1121-1138, 1992.
49. Mirabella G, Pani P, Paré M, Ferraina S. Inhibitory control of reaching movements in humans. Exp Brain Res 174: 240-255, 2006.
50. Mirabella G, Pani P, Ferraina S. Context influences on the preparation and execution of reaching movements. Cogn Neuropsychol 25: 996-1010, 2008.
51. Mirabella G, Pani P, Ferraina S. The presence of visual gap affects the duration of stopping process. Exp Brain Res 192: 199-209, 2009.
52. Mitchell JF, Sundberg KA, Reynolds JH. Differential attention-dependent response modulation across cell classes in macaque visual area v4. Neuron 55: 131-141, 2007.
53. Moll L, Kuypers HG. Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior. Science 198: 317-319, 1977.
54. Morrow MM, Miller LE. Prediction of muscle activity by populations of sequentially recorded primary motor cortex neurons. J Neurophysiol 89: 2279-2288, 2003.
55. Munoz DP, Wurtz RH. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70: 559-575, 1993.
56. Nachev P, Wydell H, O'neill K, Husain M, Kennard C. The role of the pre-supplementary motor area in the control of action. Neuroimage 36, Suppl 2: T155-T163, 2007.
57. Osman A, Kornblum S, Meyer DE. The point of no return in choice reaction time: controlled and ballistic stages of response preparation. J Exp Psychol Hum Percept Perform 12: 243-258, 1986.
58. Osman A, Kornblum S, Meyer DE. Does motor programming necessitate response execution? J Exp Psychol Hum Percept Perform 16: 183-198, 1990.
59. Paré M, Hanes DP. Controlled movement processing: superior colliculus activity associated with countermanded saccades. J Neurosci 23: 6480-6489, 2003.
60. Paxinos G, Huang XF, Toga AW. The Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 2000.
61. Pesaran B, Nelson MJ, Andersen RA. Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning. Neuron 51: 125-134, 2006.
62. Pesaran B, Nelson MJ, Andersen RA. A relative position code for saccades in dorsal premotor cortex. J Neurosci 30: 6527-6537, 2010.
63. Picton TW, Stuss DT, Alexander MP, Shallice T, Binns MA, Gillingham S. Effects of focal frontal lesions on response inhibition. Cereb Cortex 17: 826-838, 2007.
64. Port NL, Kruse W, Lee D, Georgopoulos AP. Motor cortical activity during interception of moving targets. J Cogn Neurosci 13: 306-318, 2001.
65. Prut Y, Fetz EE. Primate spinal interneurons show pre-movement instructed delay activity. Nature 401: 590-594, 1999.
66. Ray S, Pouget P, Schall JD. Functional distinction between visuomovement and movement neurons in macaque frontal eye field during saccade countermanding. J Neurophysiol 102: 3091-100, 2009.
67. Riehle A, Requin J. The predictive value for performance speed of preparatory changes in neuronal activity of the monkey motor and premotor cortex. Behav Brain Res 53: 35-49, 1993.
68. Robinson DA. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10: 137-145, 1963.
69. Rubia K, Smith AB, Brammer MJ, Taylor E. Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage 20: 351-358, 2003.
70. Scangos KW, Stuphorn V. Medial frontal cortex motivates but does not control movement initiation in the countermanding task. J Neurosci 30: 1968-1982, 2010.
71. Stuphorn V, Taylor TL, Schall JD. Performance monitoring by the supplementary eye field. Nature 408: 857-860, 2000.
72. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S, DiSano M, Aron AR. Intracranial EEG reveals a time-and frequencyspecific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J Neurosci 29: 12675-12685, 2009.
73. Tanji J, Kurata K. Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. I. Responses to instructions determining motor responses to forthcoming signals of different modalities. J Neurophysiol 53: 129-141, 1985.
74. Thach WT. Timing of activity in cerebellar dentate nucleus and cerebral motor cortex during prompt volitional movement. Brain Res 88: 233-241, 1975.
75. Tokuno H, Nambu A. Organization of nonprimary motor cortical inputs on pyramidal and nonpyramidal tract neurons of primary motor cortex: an electrophysiological study in the macaque monkey. Cereb Cortex 10: 58-68, 2000.
76. Toma K, Honda M, Hanakawa T, Okada T, Fukuyama H, Ikeda A, Nishizawa S, Konishi J, Shibasaki H. Activities of the primary and supplementary motor areas increase in preparation and execution of voluntary muscle relaxation: an event-related fMRI study. J Neurosci 19: 3527-3534, 1999.
77. van den Wildenberg WP, van Boxtel GJ, van der Molen MW, Bosch DA, Speelman JD, Brunia CH. Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson's disease. J Cogn Neurosci 18: 626-636, 2006.
78. Weinrich M, Wise SP. The premotor cortex of the monkey. J Neurosci 2: 1329-1245, 1982.
79. Weinrich M, Wise SP, Mauritz KH. A neurophysiological study of the premotor cortex in the rhesus monkey. Brain 107: 385-414, 1984.
80. Wetherill GB. Sequential Methods in Statistics. London: Methuen, 1966
81. Wetherill GB, Levitt H. Sequential estimation of points on a psychometric function. Br J Math Stat Psychol 18: 1-10, 1965.
82. Wise SP, Weinrich M, Mauritz KH. Motor aspects of cue-related neuronal activity in premotor cortex of the rhesus monkey. Brain Res 260: 301-305, 1993.