The roles of monkey M1 neuron classes in movement preparation and execution

Journal of Neurophysiology

Volumn 110, Issue 4, 2013, Pages 817-825

  Kaufman, Matthew T ^a,c   Churchland, Mark M ^d,e   Shenoy, Krishna V ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^d Department of Statistics   (United States)

^e NewYork Presbyterian Hospital   (United States)

Author keywords

Cell type; Gating; Interneurons; Motor cortex; Pyramidal cells

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HAPLORHINI; MALE; MOVEMENT (PHYSIOLOGY); NERVE CELL; NONHUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE;

EID: 84881637055     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00892.2011     Document Type: Article

References (65)

1. Afshar A, Santhanam G, Yu BM, Ryu SI, Sahani M, Shenoy KV. Single-trial neural correlates of arm movement preparation. Neuron 71: 555-564, 2011.
2. Baldissera F, Cavallari P, Craighero L, Fadiga L. Modulation of spinal excitability during observation of hand actions in humans. Eur J Neurosci 13: 190-194, 2001.
3. Bartho P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsaki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92: 600-608, 2004.
4. Benjamin PR, Staras K, Kemenes G. What roles do tonic inhibition and disinhibition play in the control of motor programs? Front Behav Neurosci 4: 30, 2010.
5. Boudrias MH, McPherson RL, Frost SB, Cheney PD. Output properties and organization of the forelimb representation of motor areas on the lateral aspect of the hemisphere in rhesus macaques. Cereb Cortex 20: 169-186, 2010.
6. Brill J, Huguenard JR. Robust short-latency perisomatic inhibition onto neocortical pyramidal cells detected by laser-scanning photostimulation. J Neurosci 29: 7413-7423, 2009.
7. Bullock D, Grossberg S. Neural dynamics of planned arm movements: emergent invariants and speed-accuracy properties during trajectory formation. Psychol Rev 95: 49-90, 1988.
8. Churchland MM, Afshar A, Shenoy KV. A central source of movement variability. Neuron 52: 1085-1096, 2006a.
9. Churchland MM, Cunningham JP, Kaufman MT, Ryu SI, Shenoy KV. Cortical preparatory activity: representation of movement or first cog in a dynamical machine? Neuron 68: 387-400, 2010.
10. Churchland MM, Santhanam G, Shenoy KV. Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. J Neurophysiol 96: 3130-3146, 2006b.
11. Churchland MM, Shenoy KV. Delay of movement caused by disruption of cortical preparatory activity. J Neurophysiol 97: 348-359, 2007.
12. 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, 2006c.
13. Cisek P. Integrated neural processes for defining potential actions and deciding between them: a computational model. J Neurosci 26: 9761-9770, 2006a.
14. Cisek P. Preparing for speed. Focus on "Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach". J Neurophysiol 96: 2842-2843, 2006b.
15. Connors BW, Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99-104, 1990.
16. 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.
17. Diester I, Nieder A. Complementary contributions of prefrontal neuron classes in abstract numerical categorization. J Neurosci 28: 7737-7747, 2008.
18. Dum RP, Strick PL. Motor areas in the frontal lobe of the primate. Physiol Behav 77: 677-682, 2002.
19. Duque J, Ivry RB. Role of corticospinal suppression during motor preparation. Cereb Cortex 19: 2013-2024, 2009.
20. Evarts EV. Pyramidal tract activity associated with a conditioned hand movement in the monkey. J Neurophysiol 29: 1011-1027, 1966.
21. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. J Neurophysiol 73: 2608-2611, 1995.
22. Fetz EE. Are movement parameters recognizably coded in the activity of single neurons? Behav Brain Sci 15: 679-690, 1992.
23. Fetz EE, Perlmutter SI, Prut Y, Seki K, Votaw S. Roles of primate spinal interneurons in preparation and execution of voluntary hand movement. Brain Res Brain Res Rev 40: 53-65, 2002.
24. Ghosh S, Porter R. Corticocortical synaptic influences on morphologically identified pyramidal neurones in the motor cortex of the monkey. J Physiol 400: 617-629, 1988.
25. Godschalk M, Lemon RN, Kuypers HG, van der Steen J. The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements. Behav Brain Res 18: 143-157, 1985.
26. Gonzalez-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA. Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93: 942-953, 2005.
27. Green AM, Kalaska JF. Learning to move machines with the mind. Trends Neurosci 34: 61-75, 2011.
28. Hartigan JA, Hartigan PM. The dip test of unimodality. Ann Stat 13: 70-84, 1985.
29. Hocherman S, Wise SP. Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys. Exp Brain Res 83: 285-302, 1991.
30. Humphrey DR, Corrie WS. Properties of pyramidal tract neuron system within a functionally defined subregion of primate motor cortex. J Neurophysiol 41: 216-243, 1978.
31. Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T. Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12: 1586-1593, 2009.
32. Jackson PR, Tucker GT, Woods HF. Testing for bimodality in frequency distributions of data suggesting polymorphisms of drug metabolism- hypothesis testing. Br J Clin Pharmacol 28: 655-662, 1989.
33. Johnston K, DeSouza JF, Everling S. Monkey prefrontal cortical pyramidal and putative interneurons exhibit differential patterns of activity between prosaccade and antisaccade tasks. J Neurosci 29: 5516-5524, 2009.
34. 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.
35. Kawaguchi Y, Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476-486, 1997.
36. Keller A. Intrinsic synaptic organization of the motor cortex. Cereb Cortex 3: 430-441, 1993.
37. Keller A, Asanuma H. Synaptic relationships involving local axon collaterals of pyramidal neurons in the cat motor cortex. J Comp Neurol 336: 229-242, 1993.
38. Krimer LS, Zaitsev AV, Czanner G, Kroner S, Gonzalez-Burgos G, Povysheva NV, Iyengar S, Barrionuevo G, Lewis DA. Cluster analysis-based physiological classification and morphological properties of inhibitory neurons in layers 2-3 of monkey dorsolateral prefrontal cortex. J Neurophysiol 94: 3009-3022, 2005.
39. Leyton AS, Sherrington CS. Observations on the excitable cortex of the chimpanzee, orang-utan and gorilla. Q J Exp Physiol 11: 135-222, 1917.
40. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
41. Mechler F, Ringach DL. On the classification of simple and complex cells. Vision Res 42: 1017-1033, 2002.
42. Merchant H, de Lafuente V, Pena-Ortega F, Larriva-Sahd J. Functional impact of interneuronal inhibition in the cerebral cortex of behaving animals. Prog Neurobiol 99: 163-178, 2012.
43. 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.
44. Messier J, Kalaska JF. Covariation of primate dorsal premotor cell activity with direction and amplitude during a memorized-delay reaching task. J Neurophysiol 84: 152-165, 2000.
45. Mitchell JF, Sundberg KA, Reynolds JH. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55: 131-141, 2007.
46. Moll L, Kuypers HG. Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior. Science 198: 317-319, 1977.
47. Pruszynski JA, Kurtzer I, Scott SH. The long-latency reflex is composed of at least two functionally independent processes. J Neurophysiol 106: 449-459, 2011.
48. Prut Y, Fetz EE. Primate spinal interneurons show pre-movement instructed delay activity. Nature 401: 590-594, 1999.
49. Rao SG, Williams GV, Goldman-Rakic PS. Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81: 1903-1916, 1999.
50. Riehle A, Requin J. Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. J Neurophysiol 61: 534-549, 1989.
51. 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.
52. Rizzolatti G, Craighero L. The mirror-neuron system. Annu Rev Neurosci 27: 169-192, 2004.
53. Sawaguchi T, Yamane I, Kubota K. Application of the GABA antagonist bicuculline to the premotor cortex reduces the ability to withhold reaching movements by well-trained monkeys in visually guided reaching task. J Neurophysiol 75: 2150-2156, 1996.
54. Scott SH. Inconvenient truths about neural processing in primary motor cortex. J Physiol 586: 1217-1224, 2008.
55. Selen LP, Shadlen MN, Wolpert DM. Deliberation in the motor system: reflex gains track evolving evidence leading to a decision. J Neurosci 32: 2276-2286, 2012.
56. Shenoy KV, Kaufman MT, Sahani M, Churchland MM. A dynamical systems view of motor preparation: implications for neural prosthetic system design. Prog Brain Res 192: 33-58, 2011.
57. Shenoy KV, Sahani M, Churchland MM. Cortical control of arm movements: a dynamical systems perspective. Ann Rev Neurosci 36: 337-359, 2013.
58. Tanji J, Evarts EV. Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J Neurophysiol 39: 1062-1068, 1976.
59. Todorov E, Jordan MI. Optimal feedback control as a theory of motor coordination. Nat Neurosci 5: 1226-1235, 2002.
60. 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.
61. Towe AL, Harding GW. Extracellular microelectrode sampling bias. Exp Neurol 29: 366-381, 1970.
62. Vigneswaran G, Kraskov A, Lemon RN. Large identified pyramidal cells in macaque motor and premotor cortex exhibit "thin spikes": implications for cell type classification. J Neurosci 31: 14235-14242, 2011.
63. Weinrich M, Wise SP. The premotor cortex of the monkey. J Neurosci 2: 1329-1345, 1982.
64. Wilson FA, O'Scalaidhe SP, Goldman-Rakic PS. Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci USA 91: 4009-4013, 1994.
65. Wise SP, Weinrich M, Mauritz KH. Movement-related activity in the premotor cortex of rhesus macaques. Prog Brain Res 64: 117-131, 1986.