The largest response component in the motor cortex reflects movement timing but not movement type

eNeuro

Volumn 3, Issue 4, 2016, Pages

  Kaufman, Matthew T ^a,b,c   Seely, Jeffrey S ^d   Sussillo, David ^a,b   Ryu, Stephen I ^b,e   Shenoy, Krishna V ^a,b   Churchland, Mark M ^d  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c Simons Center for Quantitative Biology   (United States)

^d Department of Medicine   (United States)

^e PALO ALTO MEDICAL FOUNDATION   (United States)

Author keywords

Condition invariant signal; dPCA; Movement initiation; Movement triggering; Reaction time; State space

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BODY MOVEMENT; CONTROLLED STUDY; ELECTROMYOGRAPHY; MALE; MOTOR CORTEX; MUSCLE CONTRACTION; NERVE POTENTIAL; NONHUMAN; PREMOTOR CORTEX; PRIORITY JOURNAL; RHESUS MONKEY; SIGNAL NOISE RATIO; SPIKE; ACTION POTENTIAL; ANIMAL; ARM; MICROELECTRODE; MOTOR ACTIVITY; NERVE CELL; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; REACTION TIME; SKELETAL MUSCLE; TIME FACTOR;

ACTION POTENTIALS; ANIMALS; ARM; ELECTROMYOGRAPHY; MACACA MULATTA; MALE; MICROELECTRODES; MOTOR ACTIVITY; MOTOR CORTEX; MUSCLE, SKELETAL; NEURONS; NEUROPSYCHOLOGICAL TESTS; REACTION TIME; TIME FACTORS;

EID: 85029219745     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0085-16.2016     Document Type: Article

References (76)

1. Ames KC, Ryu SI, Shenoy KV (2014) Neural dynamics of reaching following incorrect or absent motor preparation. Neuron 81:438-451
2. Bastian A, Schöner G, Riehle A (2003) Preshaping and continuous evolution of motor cortical representations during movement preparation. Eur J Neurosci 18:2047-2058
3. Brendel W, Romo R, Machens C (2011) Demixed principal component analysis. Adv Neural Info Process Syst 24:1-9.
4. Chase SM, Schwartz AB (2011) Inference from populations: going beyond models. Prog Brain Res 192:103-112
5. Churchland AK, Kiani R, Shadlen MN (2008) Decision-making with multiple alternatives. Nat Neurosci 11:693-702
6. Churchland MM, Shenoy KV (2007) Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J Neurophysiol 97:4235-4257
7. Churchland MM, Cunningham JP (2014) A dynamical basis set for generating reaches. Cold Spring Harb Symp Quant Biol 79:67-80
8. Churchland MM, Yu BM, Ryu SI, Santhanam G, Shenoy KV (2006a) Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci 26:3697-3712
9. Churchland MM, Santhanam G, Shenoy KV (2006b) Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. J Neurophysiol 96:3130-3146
10. Churchland MM, Cunningham JP, Kaufman MT, Ryu SI, Shenoy KV (2010) Cortical preparatory activity: representation of movement or first cog in a dynamical machine? Neuron 68:387-400
11. Churchland MM, Cunningham JP, Kaufman MT, Foster JD, Nuyujukian P, Ryu SI, Shenoy KV (2012) Neural population dynamics during reaching. Nature 487:51-56
12. Cluff T, Scott SH (2016) Online corrections are faster because movement initiation must disengage postural control. Motor Control 20:162-170
13. Cluff T, Crevecoeur F, Scott SH (2015) A perspective on multisensory integration and rapid perturbation responses. Vision Res 110:215-222
14. Confais J, Kilavik BE, Ponce-Alvarez A, Riehle A (2012) On the anticipatory precue activity in motor cortex. J Neurosci 32:15359-15368
15. Crammond DJ, Kalaska JF (1994) Modulation of preparatory neuronal activity in dorsal premotor cortex due to stimulus-response compatibility. J Neurophysiol 71:1281-1284
16. Crammond DJ, Kalaska JF (2000) Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. J Neurophysiol 84:986-1005
17. Eccles JC (1982) The initiation of voluntary movements by the supplementary motor area. Arch Psychiatr Nervenkr 231:423-441.
18. Erlhagen W, Schöner G (2002) Dynamic field theory of movement preparation. Psychol Rev 109:545-572
19. Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31:14-27
20. Evarts EV, Tanji J (1976) Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. J Neurophysiol 39: 1069-1080
21. Fortier PA, Smith AM, Kalaska JF (1993) Comparison of cerebellar and motor cortex activity during reaching: directional tuning and response variability. J Neurophysiol 69:1136-1149
22. Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233:1416-1419.
23. Godschalk M, Lemon RN, Kuypers HG, van der Steen J (1985) The involvement of monkey premotor cortex neurones in preparation of visually cued arm movements. Behav Brain Res 18:143-157.
24. Golub MD, Yu BM, Schwartz AB, Chase SM (2014) Motor cortical control of movement speed with implications for brain-machine interface control. J Neurophysiol 112:411-429
25. Haith AM, Pakpoor J, Krakauer JW (2016) Independence of movement preparation and movement initiation. J Neurosci 36:3007-3015
26. Hanks TD, Mazurek ME, Kiani R, Hopp E, Shadlen MN (2011) Elapsed decision time affects the weighting of prior probability in a perceptual decision task. J Neurosci 31:6339-6352
27. Hauber W (1998) Involvement of basal ganglia transmitter systems in movement initiation. Prog Neurobiol 56:507-540
28. Hennequin G, Vogels TP, Gerstner W (2014) Optimal control of transient dynamics in balanced networks supports generation of complex movements. Neuron 82:1394-1406
29. Herter TM, Korbel T, Scott SH (2009) Comparison of neural responses in primary motor cortex to transient and continuous loads during posture. J Neurophysiol 101:150-163
30. Hocherman S, Wise SP (1991) Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys. Exp Brain Res 83:285-302
31. Johnson MT, Coltz JD, Hagen MC, Ebner TJ (1999) Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons. J Neurophysiol 81:875-894.
32. Kaufman MT, Churchland MM, Santhanam G, Yu BM, Afshar A, Ryu SI, Shenoy KV (2010) Roles of monkey premotor neuron classes in movement preparation and execution. J Neurophysiol 104:799-810
33. Kaufman MT, Churchland MM, Shenoy KV (2013) The roles of monkey M1 neuron classes in movement preparation and execution. J Neurophysiol 110:817-825
34. Kobak D, Brendel W, Constantinidis C, Feierstein CE, Kepecs A, Mainen ZF, Qi XL, Romo R, Uchida N, Machens CK (2016) Demixed principal component analysis of neural population data. eLife 5
35. Kurata K (1989) Distribution of neurons with setand movementrelated activity before hand and foot movements in the premotor cortex of rhesus monkeys. Exp Brain Res 77:245-256
36. Kurata K, Wise SP (1988) Premotor and supplementary motor cortex in rhesus monkeys: neuronal activity during externallyand internally-instructed motor tasks. Exp Brain Res 72:237-248
37. Kurtzer I, Herter TM, Scott SH (2005) Random change in cortical load representation suggests distinct control of posture and movement. Nat Neurosci 8:498-504
38. Machens CK, Romo R, Brody CD (2010) Functional, but not anatomical, separation of “what” and “when” in prefrontal cortex. J Neurosci 30:350-360
39. Martens J, Sutskever I (2011) Learning recurrent neural networks with hessian-free optimization. Paper presented at 28th International Conference on Machine Learning (ICML-11), Bellevue, WA, June.
40. Messier J, Kalaska JF (2000) Covariation of primate dorsal premotor cell activity with direction and amplitude during a memorized-delay reaching task. J Neurophysiol 84:152-165
41. Meyer-Lohmann J, Hore J, Brooks VB (1977) Cerebellar participation in generation of prompt arm movements. J Neurophysiol 40:1038-1050
42. Mirabella G, Pani P, Ferraina S (2011) Neural correlates of cognitive control of reaching movements in the dorsal premotor cortex of rhesus monkeys. J Neurophysiol 106:1454-1466
43. Moran DW, Schwartz AB (1999) Motor cortical representation of speed and direction during reaching. J Neurophysiol 82:2676-2692
44. Murakami M, Mainen ZF (2015) Preparing and selecting actions with neural populations: toward cortical circuit mechanisms. Curr Opin Neurobiol 33:40-46
45. Murakami M, Vicente MI, Costa GM, Mainen ZF (2014) Neural antecedents of self-initiated actions in secondary motor cortex. Nat Neurosci 17:1574-1582
46. Orgogozo JM, Larsen B (1979) Activation of the supplementary motor area during voluntary movement in man suggests it works as a supramotor area. Science 206:847-850
47. Perfiliev S, Isa T, Johnels B, Steg G, Wessberg J (2010) Reflexive limb selection and control of reach direction to moving targets in cats, monkeys, and humans. J Neurophysiol 104:2423-2432.
48. Pesaran B, Nelson MJ, Andersen RA (2008) Free choice activates a decision circuit between frontal and parietal cortex. Nature 453: 406-409
49. Philipp R, Hoffmann K-P (2014) Arm movements induced by electrical microstimulation in the superior colliculus of the macaque monkey. J Neurosci 34:3350-3363
50. Pruszynski JA, Kurtzer I, Scott SH (2008) Rapid motor responses are appropriately tuned to the metrics of a visuospatial task. J Neurophysiol 100:224-238
51. Reimer J, Hatsopoulos NG (2009) The problem of parametric neural coding in the motor system. Adv Exp Med Biol 629:243-259
52. Riehle A, Requin J (1989) 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
53. Riehle A, MacKay WA, Requin J (1994) Are extent and force independent movement parameters? Preparationand movementrelated neuronal activity in the monkey cortex. Exp Brain Res 99:56-74
54. Riehle A, Grammont F, MacKay WA (2006) Cancellation of a planned movement in monkey motor cortex. Neuroreport 17:281-285
55. Romo R, Schultz W (1987) Neuronal activity preceding self-initiated or externally timed arm movements in area 6 of monkey cortex. Exp Brain Res 67:656-662
56. Romo R, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. III. Neuronal activity in the supplementary motor area. Exp Brain Res 91:396-407
57. Romo R, Scarnati E, Schultz W (1992) Role of primate basal ganglia and frontal cortex in the internal generation of movements. II. Movement-related activity in the anterior striatum. Exp Brain Res 91:385-395
58. Rosenbaum DA (1980) Human movement initiation: specification of arm, direction, and extent. J Exp Psychol Gen 109:444-474
59. Scangos KW, Stuphorn V (2010) Medial frontal cortex motivates but does not control movement initiation in the countermanding task. J Neurosci 30:1968-1982
60. Scherberger H, Andersen RA (2007) Target selection signals for arm reaching in the posterior parietal cortex. J Neurosci 27:2001-2012
61. Schurger A, Sitt JD, Dehaene S (2012) An accumulator model for spontaneous neural activity prior to self-initiated movement. Proc Natl Acad Sci U S A 109:E2904-E2913
62. Shen L, Alexander GE (1997) Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. J Neurophysiol 77:1195-1212
63. Shenoy KV, Sahani M, Churchland MM (2013) Cortical control of arm movements: a dynamical systems perspective. Annu Rev Neurosci 36:337-359
64. Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386:167-170
65. Sussillo D, Abbott LF (2009) Generating coherent patterns of activity from chaotic neural networks. Neuron 63:544-557
66. Sussillo D, Churchland MM, Kaufman MT, Shenoy KV (2015) A neural network that finds a naturalistic solution for the production of muscle activity. Nat Neurosci 18:1025-1033
67. Tanji J, Evarts EV (1976) Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J Neurophysiol 39:1062-1068
68. Thaler DE, Rolls ET, Passingham RE (1988) Neuronal activity of the supplementary motor area (SMA) during internally and externally triggered wrist movements. Neurosci Lett 93:264-269
69. Thura D, Cisek P (2014) Deliberation and commitment in the premotor and primary motor cortex during dynamic decision making. Neuron 81:1401-1416
70. Thura D, Beauregard-Racine J, Fradet CW, Cisek P (2012) Decision making by urgency gating: theory and experimental support. J Neurophysiol 108:2912-2930
71. Velliste M, Kennedy SD, Schwartz AB, Whitford AS, Sohn JW, McMorland AJ (2014) Motor cortical correlates of arm resting in the context of a reaching task and implications for prosthetic control. J Neurosci 34:6011-6022
72. Weinrich M, Wise SP (1982) The premotor cortex of the monkey. J Neurosci 2:1329-1345
73. Weinrich M, Wise SP, Mauritz KH (1984) A neurophysiological study of the premotor cortex in the rhesus monkey. Brain 107:385-414.
74. Werner W (1993) Neurons in the primate superior colliculus are active before and during arm movements to visual targets. Eur J Neurosci 5:335-340
75. Wise SP, Weinrich M, Mauritz KH (1986) Movement-related activity in the premotor cortex of rhesus macaques. Prog Brain Res 64:117-131
76. Yu BM, Cunningham JP, Santhanam G, Ryu SI, Shenoy KV, Sahani M (2009) Gaussian-process factor analysis for low-dimensional single-trial analysis of neural population activity. J Neurophysiol 102:614-635