Different modulation of common motor information in rat primary and secondary motor cortices

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Saiki, Akiko ^a,b   Kimura, Rie ^a,b   Samura, Toshikazu ^a,c   Fujiwara Tsukamoto, Yoko ^a,b,d   Sakai, Yutaka ^a,b   Isomura, Yoshikazu ^a,b  

^a TAMAGAWA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d DOSHISHA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE BEHAVIOR; AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CAUDAL FORELIMB AREA; COMPARATIVE ANATOMY; CONTROLLED STUDY; FUNCTIONAL ASSESSMENT; LIMB MOVEMENT; MOTOR CORTEX; MOTOR PERFORMANCE; NEUROMODULATION; NONHUMAN; PRIMARY MOTOR CORTEX; RAT; REWARD; ROSTRAL FORELIMB AREA; SECONDARY MOTOR CORTEX; SPIKE WAVE; TASK PERFORMANCE; VOLUNTARY MOVEMENT; ANIMAL; ELECTROPHYSIOLOGY; FORELIMB; MALE; NERVE CELL; PHYSIOLOGY;

ANIMALS; ELECTROPHYSIOLOGY; FORELIMB; MALE; MOTOR CORTEX; NEURONS; RATS;

EID: 84902449485     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098662     Document Type: Article

References (63)

1. Picard N, Strick PL (2001) Imaging the premotor areas. Curr Opin Neurobiol 11: 663-672. (Pubitemid 34014913)
2. Evarts EV (1968) Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol 31: 14-27.
3. Georgopoulos AP, Kalaska JF, Caminiti R, Massey JT (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J Neurosci 2: 1527-1537. (Pubitemid 13178240)
4. Tanji J, Kurata K (1985) 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. (Pubitemid 15174279)
5. Kurata K, Tanji J (1985) Contrasting neuronal activity in supplementary and precentral motor cortex of monkeys. II. Responses to movement triggering vs. nontriggering sensory signals. J Neurophysiol 53: 142-152. (Pubitemid 15174280)
6. Okano K, Tanji J (1987) Neuronal activities in the primate motor fields of the agranular frontal cortex preceding visually triggered and self-paced movement. Exp Brain Res 66: 155-166. (Pubitemid 17039282)
7. Mushiake H, Inase M, Tanji J (1991) Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. J Neurophysiol 66: 705-718.
8. Kalaska JF, Crammond DJ (1995) 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.
9. Shima K, Aya K, Mushiake H, Inase M, Aizawa H, et al. (1991) Two movement-related foci in the primate cingulate cortex observed in signaltriggered and self-paced forelimb movements. J Neurophysiol 65: 188-202.
10. Shima K, Tanji J (1998) Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282: 1335-1338. (Pubitemid 28524499)
11. Isomura Y, Ito Y, Akazawa T, Nambu A, Takada M (2003) Neural coding of "attention for action" and "response selection" in primate anterior cingulate cortex. J Neurosci 23: 8002-8012. (Pubitemid 37082452)
12. Iwaniuk AN, Whishaw IQ (2000) On the origin of skilled forelimb movements. Trends Neurosci 23: 372-376. (Pubitemid 30628814)
13. Paxinos G, Watson C (2007) The Rat Brain in Stereotaxic Coordinates, 6th ed. London: Academic Press.
14. Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, et al. (1986) The organization of the rat motor cortex: a microstimulation mapping study. Brain Res Rev 11: 77-96. (Pubitemid 16126208)
15. Nudo RJ, Jenkins WM, Merzenich MM (1990) Repetitive microstimulation alters the cortical representation of movements in adult rats. Somatosens Mot Res 7: 463-483.
16. Ebrahimi A, Pochet R, Roger M (1992) Topographical organization of the projections from physiologically identified areas of the motor cortex to the striatum in the rat. Neurosci Res 14: 39-60.
17. Liang F, Rouiller EM, Wiesendanger M (1993) Modulation of sustained electromyographic activity by single intracortical microstimuli: comparison of two forelimb motor cortical areas of the rat. Somatosens Mot Res 10: 51-61. (Pubitemid 23136476)
18. Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80: 3321-3325. (Pubitemid 29029253)
19. VandenBerg PM, Hogg TM, Kleim JA, Whishaw IQ (2002) Long-Evans rats have a larger cortical topographic representation of movement than Fischer-344 rats: a microstimulation study of motor cortex in naive and skilled reachingtrained rats. Brain Res Bull 59: 197-203. (Pubitemid 35300455)
20. Gharbawie OA, Karl JM, Whishaw IQ (2007) Recovery of skilled reaching following motor cortex stroke: do residual corticofugal fibers mediate compensatory recovery? Eur J Neurosci 26: 3309-3327. (Pubitemid 350135159)
21. Tennant KA, Adkins DL, Donlan NA, Asay AL, Thomas N, et al. (2011) The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb Cortex 21: 865-876.
22. Bonazzi L, Viaro R, Lodi E, Canto R, Bonifazzi C, et al. (2013) Complex movement topography and extrinsic space representation in the rat forelimb motor cortex as defined by long-duration intracortical microstimulation. J Neurosci 33: 2097-2107.
23. Hira R, Ohkubo F, Ozawa K, Isomura Y, Kitamura K, et al. (2013) Spatiotemporal dynamics of functional clusters of neurons in the mouse motor cortex during a voluntary movement. J Neurosci 33: 1377-1390.
24. Mansoori BK, Jean-Charles L, Touvykine B, Liu A, Quessy S, et al. (2014) Acute inactivation of the contralesional hemisphere for longer durations improves recovery after cortical injury. Exp Neurol 254: 18-28.
25. Rouiller EM, Moret V, Liang F (1993) Comparison of the connectional properties of the two forelimb areas of the rat sensorimotor cortex: support for the presence of a premotor or supplementary motor cortical area. Somatosens Mot Res 10: 269-289. (Pubitemid 23285319)
26. Wang Y, Kurata K (1998) Quantitative analyses of thalamic and cortical origins of neurons projecting to the rostral and caudal forelimb motor areas in the cerebral cortex of rats. Brain Res 781: 137-147. (Pubitemid 28082856)
27. Hira R, Ohkubo F, Tanaka YR, Masamizu Y, Augustine GJ, et al. (2013) In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas. Front Neural Circuits 7: 55.
28. Miller MW (1987) The origin of corticospinal projection neurons in rat. Exp Brain Res 67: 339-351.
29. Hyland B (1998) Neural activity related to reaching and grasping in rostral and caudal regions of rat motor cortex. Behav Brain Res 94: 255-269.
30. Laubach M, Wessberg J, Nicolelis MA (2000) Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405: 567-571. (Pubitemid 30367728)
31. Brown VJ, Bowman EM, Robbins TW (1991) Response-related deficits following unilateral lesions of the medial agranular cortex of the rat. Behav Neurosci 105: 567-578.
32. Brasted PJ, Dunnett SB, Robbins TW (2000) Unilateral lesions of the medial agranular cortex impair responding on a lateralised reaction time task. Behav Brain Res 111: 139-151. (Pubitemid 30326710)
33. Smith NJ, Horst NK, Liu B, Caetano MS, Laubach M (2010) Reversible inactivation of rat premotor cortex impairs temporal preparation, but not inhibitory control, during simple reaction-time performance. Front Integr Neurosci 4: 124.
34. Zeiler SR, Gibson EM, Hoesch RE, Li MY, Worley PF, et al. (2013) Medial premotor cortex shows a reduction in inhibitory markers and mediates recovery in a mouse model of focal stroke. Stroke 44: 483-489.
35. Passingham RE, Myers C, Rawlins N, Lightfoot V, Fearn S (1998) Premotor cortex in the rat. Behav Neurosci 102: 101-109.
36. Ostlund SB, Winterbauer NE, Balleine BW (2009) Evidence of action sequence chunking in goal-directed instrumental conditioning and its dependence on the dorsomedial prefrontal cortex. J Neurosci 29: 8280-8287.
37. Sul JH, Jo S, Lee D, Jung MW (2011) Role of rodent secondary motor cortex in value-based action selection. Nat Neurosci 14: 1202-1208.
38. Brecht M, Krauss A, Muhammad S, Sinai-Esfahani L, Bellanca S, et al. (2004) Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells. J Comp Neurol 479: 360-373. (Pubitemid 39453142)
39. Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T (2009) Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12: 1586-1593.
40. Kimura R, Saiki A, Fujiwara-Tsukamoto Y, Ohkubo F, Kitamura K, et al. (2012) Reinforcing operandum: rapid and reliable learning of skilled forelimb movements by head-fixed rodents. J Neurophysiol 108: 1781-1792.
41. Isomura Y, Takekawa T, Harukuni R, Handa T, Aizawa H, et al. (2013) Reward-modulated motor information in identified striatum neurons. J Neurosci 33: 10209-10220.
42. Schwarz C, Hentschke H, Butovas S, Haiss F, Stüttgen MC, et al. (2011) The head-fixed behaving rat-procedures and pitfalls. Somatosens Mot Res 27: 131-148.
43. Igarashi J, Isomura Y, Arai K, Harukuni R, Fukai T (2013) A θ-γ oscillation code for neuronal coordination during motor behavior. J Neurosci 33: 18515-18530.
44. Takekawa T, Isomura Y, Fukai T (2010) Accurate spike sorting for multi-unit recordings. Eur J Neurosci 31: 263-272.
45. Takekawa T, Isomura Y, Fukai T (2012) Spike sorting of heterogeneous neuron types by multimodality-weighted PCA and explicit robust variational Bayes. Front Neuroinform 6: 5.
46. Hazan L, Zugaro M, Buzsáki G (2006) Klusters, NeuroScope, NDManager: a free software suite for neurophysiological data processing and visualization. J Neurosci Methods 155: 207-216. (Pubitemid 44233005)
47. van Kan PL, Scobey RP, Gabor AJ (1985) Response covariance in cat visual cortex. Exp Brain Res 60: 559-563. (Pubitemid 16191801)
48. Zohary E, Shadlen MN, Newsome WT (1994) Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370: 140-143. (Pubitemid 24229125)
49. Chapin JK, Woodward DJ (1986) Distribution of somatic sensory and activemovement neuronal discharge properties in the MI-SI cortical border area in the rat. Exp Neurol 91: 502-523. (Pubitemid 16164325)
50. Chapin JK, Moxon KA, Markowitz RS, Nicolelis MA (1999) Real-time control of a robot arm using simultaneously recorded neurons in the motor cortex. Nat Neurosci 2: 664-670. (Pubitemid 30491219)
51. Hermer-Vazquez L, Hermer-Vazquez R, Moxon KA, Kuo KH, Viau V, et al. (2004) Distinct temporal activity patterns in the rat M1 and red nucleus during skilled versus unskilled limb movement. Behav Brain Res 150: 93-107. (Pubitemid 38368961)
52. Anderson CT, Sheets PL, Kiritani T, Shepherd GM (2010). Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat Neurosci 13: 739-744.
53. Morishima M, Morita K, Kubota Y, Kawaguchi Y (2011) Highly differentiated projection-specific cortical subnetworks. J Neurosci 31: 10380-10391.
54. Donoghue JP (1985) Contrasting properties of neurons in two parts of the primary motor cortex of the awake rat. Brain Res 333: 173-177.
55. Sievert CF, Neafsey EJ (1986) A chronic unit study of the sensory properties of neurons in the forelimb areas of rat sensorimotor cortex. Brain Res 381: 15-23. (Pubitemid 16049652)
56. Watanabe M (1986) Prefrontal unit activity during delayed conditional Go/No-Go discrimination in the monkey. I. Relation to the stimulus. Brain Res 382: 1-14.
57. Watanabe M (1986) Prefrontal unit activity during delayed conditional Go/No-Go discrimination in the monkey. II. Relation to Go and No-Go responses. Brain Res 382: 15-27.
58. Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212: 76-88. (Pubitemid 13208310)
59. Cho RH, Segawa S, Mizuno A, Kaneko T (2004) Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord. I. Electrophysiological properties of pyramidal neurons. Neurosci Res 50: 381-394. (Pubitemid 39572985)
60. Cho RH, Segawa S, Okamoto K, Mizuno A, Kaneko T (2004) Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord. II. Intra- and juxta-columnar projection of pyramidal neurons to corticospinal neurons. Neurosci Res 50: 395-410. (Pubitemid 39572986)
61. Reep RL, Goodwin GS, Corwin JV (1990) Topographic organization in the corticocortical connections of medial agranular cortex in rats. J Comp Neurol 294: 262-280. (Pubitemid 20101602)
62. Umeda T, Isa T (2011) Differential contributions of rostral and caudal frontal forelimb areas to compensatory process after neonatal hemidecortication in rats. Eur J Neurosci 34: 1453-1460.
63. Guggenmos DJ, Azin M, Barbay S, Mahnken JD, Dunham C, et al. (2013) Restoration of function after brain damage using a neural prosthesis. Proc Natl Acad Sci USA 110: 21177-21182.