Goal-dependent modulation of fast feedback responses in primary motor cortex

Journal of Neuroscience

Volumn 34, Issue 13, 2014, Pages 4608-4617

  Andrew Pruszynski, J ^a,c   Omrani, Mohsen ^a   Scott, Stephen H ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

Feedback; Instruction; Primary motor cortex; Reflex; Single unit recording; Task goal

Indexed keywords

ANIMAL EXPERIMENT; ARM MUSCLE; ARTICLE; BEHAVIOR; BODY POSTURE; ELECTROMYOGRAPHY; FEEDBACK SYSTEM; HAPLORHINI; KINEMATICS; MALE; MECHANICAL STIMULATION; MOTOR PERFORMANCE; MUSCLE CONTRACTION; NEUROMODULATION; NONHUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; SPATIAL BEHAVIOR; TASK PERFORMANCE;

FEEDBACK; INSTRUCTION; PRIMARY MOTOR CORTEX; REFLEX; SINGLE-UNIT RECORDING; TASK-GOAL;

ACTION POTENTIALS; ANIMALS; ARM; BIOMECHANICAL PHENOMENA; ELECTROMYOGRAPHY; FEEDBACK, PHYSIOLOGICAL; GOALS; MACACA MULATTA; MALE; MOTOR CORTEX; MOTOR NEURONS; MUSCLE, SKELETAL; POSTURE; PSYCHOMOTOR PERFORMANCE; REACTION TIME; SPATIAL BEHAVIOR;

EID: 84897837401     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4520-13.2014     Document Type: Article

References (61)

1. Abbruzzese G, Berardelli A, Rothwell JC, Day BL, Marsden CD (1985) Cerebral potentials and electromyographic responses evoked by stretch of wrist muscles in man. Exp Brain Res 58:544-551. Medline
2. Batschelet E (1981) Circular statistics in biology. New York: Academic.
3. Bedingham W, Tatton WG (1984) Dependence of EMG responses evoked by imposed wrist displacements on pre-existing activity in the stretched muscles. Can J Neurol Sci 11:272-280. Medline
4. Capaday C, Stein RB (1987) A method for simulating the reflex output of a motoneuron pool. J Neurosci Methods 21:91-104. CrossRef Medline
5. Cheney PD, Fetz EE (1984) Corticomotoneuronal cells contribute to longlatency stretch reflexes in the rhesus monkey. J Physiol 349:249-272. Medline
6. Churchland MM, Shenoy KV (2007) Temporal complexity and heterogeneity of single-neuron activity in premotor and motor cortex. J Neurophysiol 97:4235-4257. CrossRef Medline
7. 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. CrossRef Medline
8. Churchland MM, Cunningham JP, Kaufman MT, Foster JD, Nuyujukian P, Ryu SI, Shenoy KV (2012) Neural population dynamics during reaching. Nature 487:51-56. CrossRef Medline
9. Cohen O, Sherman E, Zinger N, Perlmutter S, Prut Y (2010) Getting ready to move: transmitted information in the corticospinal pathway during preparation for movement. Curr Opin Neurobiol 20:696-703. CrossRef Medline
10. Colebatch JG, Gandevia SC, McCloskey DI, Potter EK (1979) Subject instruction and long latency reflex responses to muscle stretch. J Physiol 292:527-534. Medline
11. Crago PE, Houk JC, Hasan Z (1976) Regulatory actions of human stretch reflex. J Neurophysiol 39:925-935. Medline
12. de Graaf JB, Frolov A, Fiocchi M, Nazarian B, Anton JL, Pailhous J, Bonnard M (2009) Preparing for a motor perturbation: early implication of primary motor and somatosensory cortices. Hum Brain Mapp 30:575-587. CrossRef Medline
13. Dimitriou M, Franklin DW, Wolpert DM (2012) Task-dependent coordination of rapid bimanual motor responses. J Neurophysiol 107:890-901. CrossRef Medline
14. Evarts EV, Granit R (1976) Relations of reflexes and intended movements. Prog Brain Res 44:1-14. CrossRef Medline
15. Evarts EV, Tanji J (1976) Reflex and intended responses in motor cortex pyramidal tract neurons of monkey. J Neurophysiol 39:1069-1080. Medline
16. Fetz EE (1992) Are movement parameters recognizably coded in the activity of single neurons. Behav Brain Sci 15:679-690.
17. Fromm C, Evarts EV (1977) Relation of motor cortex neurons to precisely controlled and ballistic movements. Neurosci Lett 5:259-265. CrossRef Medline
18. Graham KM, Moore KD, Cabel DW, Gribble PL, Cisek P, Scott SH (2003) Kinematics and kinetics of multijoint reaching in nonhuman primates. J Neurophysiol 89:2667-2677. CrossRef Medline
19. Hammond PH (1955) Involuntary activity in biceps following the sudden application of velocity to the abducted forearm. J Physiol 127:23-25P. Medline
20. Hammond PH (1956) The influence of prior instruction to the subject on an apparently involuntary neuro-muscular response. J Physiol 132:17-18P. Medline
21. Hatsopoulos NG, Suminski AJ (2011) Sensing with the motor cortex. Neuron 72:477-487. CrossRef Medline
22. Hatsopoulos NG, Xu Q, Amit Y (2007) Encoding of movement fragments in the motor cortex. J Neurosci 27:5105-5114. CrossRef Medline
23. Herter TM, Kurtzer I, Cabel DW, Haunts KA, Scott SH (2007) Characterization of torque-related activity in primary motor cortex during a multijoint postural task. J Neurophysiol 97:2887-2899. CrossRef Medline
24. 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. CrossRef Medline
25. Kaufman MT, Churchland MM, Ryu SI, Shenoy KV (2014) Cortical activity in the null space: permitting preparation without movement. Nat Neurosci 17:440-448. CrossRef Medline
26. Kimura T, Haggard P, Gomi H (2006) Transcranial magnetic stimulation over sensorimotor cortex disrupts anticipatory reflex gain modulation for skilled action. J Neurosci 26:9272-9281. CrossRef Medline
27. 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. CrossRef Medline
28. Kurtzer I, Pruszynski JA, Herter TM, Scott SH (2006) Primate upper limb muscles exhibit activity patterns that differ from their anatomical action during a postural task. J Neurophysiol 95:493-504. CrossRef Medline
29. Lee RG, Tatton WG (1982) Long latency reflexes to imposed displacements of the human wrist-dependence on duration of movement. Exp Brain Res 45:207-216. Medline
30. Lewis GN, MacKinnon CD, Perreault EJ (2006) The effect of task instruction on the excitability of spinal and supraspinal reflex pathways projecting to the biceps muscle. Exp Brain Res 174:413-425. CrossRef Medline
31. Lillicrap TP, Scott SH (2013) Preference distributions of primary motor cortex neurons reflect control solutions optimized for limb biomechanics. Neuron 77:168-179. CrossRef Medline
32. McKinnon CD, Verrier MC, Tatton WG (2000) Motor cortical potentials precede long-latency EMG activity evoked by imposed displacements of the human wrist. Exp Brain Res 131:477-490. CrossRef Medline
33. Marsden CD, Merton PA, Morton HB (1976) Stretch reflex and servo action in a variety of human muscles. J Physiol 259:531-560. Medline
34. Matthews PB (1986) Observations on the automatic compensation of reflex gain on varying the pre-existing level of motor discharge in man. J Physiol 374:73-90. Medline
35. Nashed JY, Crevecoeur F, Scott SH (2014) Rapid online selection between multiple motor plans. J Neurosci 34:1769-1780. CrossRef Medline
36. Omrani M, Diedrichsen J, Scott SH (2013) Rapid feedback corrections during a bimanual postural task. J Neurophysiol 109:147-161. CrossRef Medline
37. Picard N, Smith AM (1992) Primary motor cortical responses to perturbations of prehension in the monkey. J Neurophysiol 68:1882-1894. Medline
38. Porter R, Lemon RN (1993) Corticospinal function and voluntary movement. New York: Oxford UP.
39. Pruszynski JA, Scott SH (2012) Optimal feedback control and the longlatency stretch response. Exp Brain Res 218:341-359. CrossRef Medline
40. 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. CrossRef Medline
41. Pruszynski JA, Kurtzer I, Lillicrap TP, Scott SH (2009) Temporal evolution of "automatic gain-scaling. " J Neurophysiol 102:992-1003. CrossRef Medline
42. Pruszynski JA, Kurtzer I, Nashed JY, Omrani M, Brouwer B, Scott SH (2011a) Primary motor cortex underlies multi-joint integration for fast feedback control. Nature 478:387-390. CrossRef Medline
43. Pruszynski JA, Kurtzer I, Scott SH (2011b) The long-latency reflex is composed of at least two functionally independent processes. J Neurophysiol 106:449-459. CrossRef Medline
44. Robinson DA (1992) Implications of neural networks for how we think about brain function. Behav Brain Sci 15:644-655.
45. Rothwell JC, Traub MM, Marsden CD (1980) Influence of voluntary intent on the human long-latency stretch reflex. Nature 286:496-498. CrossRef Medline
46. Scott SH (1999) Apparatus for measuring and perturbing shoulder and elbow joint positions and torques during reaching. J Neurosci Methods 89:119-127. CrossRef Medline
47. Scott SH (2004) Optimal feedback control and the neural basis of volitional motor control. Nat Rev Neurosci 5:532-546. CrossRef Medline
48. Scott SH (2012) The computational and neural basis of voluntary motor control and planning. Trends Cogn Sci 16:541-549. CrossRef Medline
49. Sergio LE, Hamel-Pâquet C, Kalaska JF (2005) Motor cortex neural correlates of output kinematics and kinetics during isometric-force and armreaching tasks. J Neurophysiol 94:2353-2378. CrossRef Medline
50. Shapiro MB, Gottlieb GL, Moore CG, Corcos DM (2002) Electromyographic responses to an unexpected load in fast voluntary movements: descending regulation of segmental reflexes. J Neurophysiol 88:1059-1063. Medline
51. Shemmell J, An JH, Perreault EJ (2009) The differential role of motor cortex in stretch reflex modulation induced by changes in environmental mechanics and verbal instruction. J Neurosci 29:13255-13263. CrossRef Medline
52. Shemmell J, Krutky MA, Perreault EJ (2010) Stretch sensitive reflexes as an adaptive mechanism for maintaining limb stability. Clin Neurophysiol 121:1680-1689. CrossRef Medline
53. Shenoy KV, Sahani M, Churchland MM (2013) Cortical control of arm movements: a dynamical systems perspective. Annu Rev Neurosci 36: 337-359. CrossRef Medline
54. Spieser L, Meziane HB, Bonnard M (2010) Cortical mechanisms underlying stretch reflex adaptation to intention: a combined EEG-TMS study. Neuroimage 52:316-325. CrossRef Medline
55. Strick PL (1983) The influence of motor preparation on the response of cerebellar neurons to limb displacements. J Neurosci 3:2007-2020. Medline
56. Tanji J, Evarts EV (1976) Anticipatory activity of motor cortex neurons in relation to direction of an intended movement. J Neurophysiol 39:1062-1068. Medline
57. Terao Y, Ugawa Y (2002) Basic mechanisms of TMS. J Clin Neurophysiol 19:322-343. CrossRef Medline
58. Thompson KG, Hanes DP, Bichot NP, Schall JD (1996) Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. J Neurophysiol 76:4040-4055. Medline
59. Todorov E (2000) Direct cortical control of muscle activation in voluntary arm movements: a model. Nat Neurosci 3:391-398. CrossRef Medline
60. Vilis T, Hore J, Meyer-Lohmann J, Brooks VB (1976) Dual nature of the precentral responses to limb perturbations revealed by cerebellar cooling. Brain Res 117:336-340. CrossRef Medline
61. Werhahn KJ, Kunesch E, Noachtar S, Benecke R, Classen J (1999) Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. J Physiol 517:591-597. CrossRef Medline