Spatiotemporal dynamics of functional clusters of neurons in the mouse motor cortex during a voluntary movement

Journal of Neuroscience

Volumn 33, Issue 4, 2013, Pages 1377-1390

  Hira, Riichiro ^a,b,c   Ohkubo, Fuki ^a,b,c   Ozawa, Katsuya ^b,c   Isomura, Yoshikazu ^b,d   Kitamura, Kazuo ^b,c   Kano, Masanobu ^c   Kasai, Haruo ^c   Matsuzaki, Masanori ^a,b,c  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d TAMAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FLAVOPROTEIN; MUSCIMOL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROMYOGRAPHY; FLUORESCENCE IMAGING; FORELIMB; LASER MICROSCOPY; LICKING; MICROELECTRODE; MOTOR CORTEX; MOUSE; NERVE CELL; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PREDICTION; PRIORITY JOURNAL; SENSORY STIMULATION; SPIKE WAVE; TASK PERFORMANCE; TRANSGENIC MOUSE; VOLUNTARY MOVEMENT;

ANIMALS; BRAIN MAPPING; ELECTROMYOGRAPHY; FEMALE; MALE; MICE; MICE, INBRED C57BL; MOTOR CORTEX; MOVEMENT; NEURONS;

EID: 84872718341     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2550-12.2013     Document Type: Article

References (57)

1. Amirikian B., Georgopoulos AP. (2003). Modular organization of directionally tuned cells in the motor cortex: is there a short-range order? Proc Natl Acad Sci U S A 100:12474-12479. CrossRef Medline
2. Asanuma H., Rosén I. (1972). Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp Brain Res 14:243-256. CrossRef Medline
3. Ashe J., Georgopoulos AP. (1994). Movement parameters and neural activity in motor cortex and area 5. Cereb Cortex 4:590-600. CrossRef Medline
4. Ayling OG., Harrison TC, Boyd JD, Goroshkov A, Murphy TH. (2009). Automated light-based mapping of motor cortex by photoactivation of channelrhodopsin-2 transgenic mice. Nat Methods 6:219-224. CrossRef Medline
5. Ben-Shaul Y, Stark E, Asher I, Drori R, Nadasdy Z, AbelesM. (2003). Dynamical organization of directional tuning in the primate premotor and primary motor cortex. J Neurophysiol 89:1136-1142. Medline
6. Berridge KC., Whishaw IQ. (1992). Cortex, striatum and cerebellum: control of serial order in a grooming sequence. Exp Brain Res 90:275-290. Medline
7. de la Rocha J, Doiron B, Shea-Brown E, Josić K, Reyes A. (2007). Correlation between neural spike trains increases with firing rate. Nature 448: 802-806. CrossRef Medline
8. Denève S, Duhamel JR, Pouget A. (2007). Optimal sensorimotor integration in recurrent cortical networks: a neural implementation of Kalman filters. J Neurosci 27:5744-5756. CrossRef Medline
9. Dombeck DA., Khabbaz AN, Collman F, Adelman TL, Tank DW. (2007). Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56:43-57. CrossRef Medline
10. Dombeck DA., Graziano MS, Tank DW. (2009). Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice. J Neurosci 29:13751-13760. CrossRef Medline
11. Fenno L., Yizhar O, Deisseroth K. (2011). The development and application of optogenetics. Annu Rev Neurosci 34:389-412. CrossRef Medline
12. Gao P., Hattox AM, Jones LM, Keller A, Zeigler HP. (2003). Whisker motor cortex ablation and whisker movement patterns. Somatosens Mot Res 20:191-198. CrossRef Medline
13. Georgopoulos AP., Merchant H, Naselaris T, Amirikian B. (2007). Mapping of the preferred direction in the motor cortex. Proc Natl Acad Sci U S A 104:11068-11072. CrossRef Medline
14. Graziano MS., Taylor CS, Moore T. (2002). Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841-851. CrossRef Medline
15. Greenberg DS., Kerr JN. (2009). Automated correction of fast motion artifacts for two-photon imaging of awake animals. J Neurosci Methods 176: 1-15. CrossRef Medline
16. Harvey CD., Coen P, Tank DW. (2012). Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484:62-68.
17. Hastie T., Tibshirani R, Friedman J. (2009). The elements of statistical learning, Ed 2. New York: Springer.
18. Hira R., Honkura N, Noguchi J, Maruyama Y, Augustine GJ, Kasai H, MatsuzakiM (2009) Transcranial optogenetic stimulation for functional mapping of the motor cortex. J Neurosci Methods 179:258-263. CrossRef Medline
19. Hofer SB., Ko H, Pichler B, Vogelstein J, Ros H, Zeng H, Lein E, Lesica NA, Mrsic-Flogel TD. (2011). Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat Neurosci 14:1045-1052. CrossRef Medline
20. Holmgren C., Harkany T, Svennenfors B, Zilberter Y. (2003). Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551:139-153. CrossRef Medline
21. Hopfield JJ. (1982). Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci U S A 79:2554-2558. CrossRef Medline
22. Huber D., Gutnisky DA, Peron S, O'Connor DH, Wiegert JS, Tian L, Oertner TG, Looger LL, Svoboda K. (2012). Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484:473-478. CrossRef Medline
23. Humphrey DR., Schmidt EM, Thompson WD. (1970). Predicting measures of motor performance from multiple cortical spike trains. Science 170: 758-762. CrossRef Medline
24. Isomura Y., Harukuni R, Takekawa T, Aizawa H, Fukai T. (2009). Microcir-cuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12:1586-1593. CrossRef Medline
25. Iwaniuk AN., Whishaw IQ. (2000). On the origin of skilled forelimb movements. Trends Neurosci 23:372-376. CrossRef Medline
26. Kampa BM., Roth MM, Göbel W, Helmchen F. (2011). Representation of visual scenes by local neuronal populations in layer 2/3 of mouse visual cortex. Front Neural Circuits 5:18. Medline
27. 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. CrossRef Medline
28. Kerr JND., Greenberg D, Helmchen F. (2005). Imaging input and output of neocortical networks in vivo. Proc Natl Acad Sci U S A 102:14063-14068. CrossRef Medline
29. Kerr JND., de Kock CPJ, Greenberg DS, Bruno RM, Sakmann B, Helmchen F (2007) Spatial organization of neuronal population responses in layer 2/3 of rat barrel cortex. J Neurosci 27:13316-13328. CrossRef Medline
30. Kimura R., Saiki A, Fujiwara-Tsukamoto Y, Ohkubo F, Kitamura K, Matsuzaki M, Sakai Y, Isomura Y. (2012). Reinforcing operandum: rapid and reliable learning of skilled forelimb movements by head-fixed rodents. J Neurophysiol 108:1781-1792. CrossRef Medline
31. Ko H., Hofer SB, Pichler B, Buchanan KA, Sjöström PJ, Mrsic-Flogel TD (2011) Functional specificity of local synaptic connections in neocortical networks. Nature 473:87-91. CrossRef Medline
32. Komiyama T., Sato TR, O'Connor DH, Zhang YX, Huber D, Hooks BM, Gabitto M., Svoboda K. (2010). Learning-related fine-scale specificity imaged in motor cortex circuits of behaving mice. Nature 464:1182-1186. CrossRef Medline
33. Laubach M., Wessberg J, Nicolelis MAL. (2000). Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405:567-571. CrossRef Medline
34. Lee D., Port NL, Kruse W, Georgopoulos AP. (1998). Variability and correlated noise in the discharge of neurons in motor and parietal areas of the primate cortex. J Neurosci 18:1161-1170. Medline
35. Mukamel EA., Nimmerjahn A, Schnitzer MJ. (2009). Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63:747-760. CrossRef Medline
36. Narayanan NS., Kimchi EY, Laubach M. (2005). Redundancy and synergy of neuronal ensembles in motor cortex. J Neurosci 25:4207-4216. CrossRef Medline
37. Neafsey EJ., Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR. (1986). The organization of the rat motor cortex: a microstimulation mapping study. Brain Res 396:77-96. CrossRef Medline
38. Paninski L., Fellows MR, Hatsopoulos NG, Donoghue JP. (2004). Spatiotemporal tuning of motor cortical neurons for hand position and velocity. J Neurophysiol 91:515-532. Medline
39. Paz R., Vaadia E. (2004). Learning-induced improvement in encoding and decoding of specific movement directions by neurons in the primary motor cortex. PLoS Biol 2:e45. CrossRef Medline
40. Podgorski K., Dunfield D, Haas K. (2012). Functional clustering drives encoding improvement in a developing brain network during awake visual learning. PLoS Biol 10:e1001236. CrossRef Medline
41. Renart A., de la Rocha J, Bartho P, Hollender L, Parga N, Reyes A, Harris KD (2010) The asynchronous state in cortical circuits. Science 327:587-590. CrossRef Medline
42. Rossignol S., Dubuc R, Gossard JP. (2006). Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89-154. CrossRef Medline
43. Rothschild G., Nelken I, Mizrahi A. (2010). Functional organization and population dynamics in the mouse primary auditory cortex. Nat Neurosci 13:353-360. CrossRef Medline
44. Smith WS., Fetz EE. (2009). Synaptic interactions between forelimb-related motor cortex neurons in behaving primates. J Neurophysiol 102: 1026-1039. CrossRef Medline
45. 2+ imaging in transgenic mice. J Neurosci 27:2145-2149. CrossRef Medline
46. Song S., Sjöström PJ, Reigl M, Nelson S, Chklovskii DB. (2005). Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3:e68. CrossRef Medline
47. Stark E., Globerson A, Asher I, Abeles M. (2008). Correlations between groups of premotor neurons carry information about prehension. J Neurosci 28:10618-10630. CrossRef Medline
48. Stark E., Drori R, Abeles M. (2009). Motor cortical activity related to movement kinematics exhibits local spatial organization. Cortex 45:418-431. CrossRef Medline
49. Tennant KA., Adkins DL, Donlan NA, Asay AL, Thomas N, Kleim JA, Jones TA. (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. CrossRef Medline
50. Thévenaz P, Ruttimann UE, Unser M. (1998). A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7:27-41. CrossRef Medline
51. Tian L., Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J., McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K., Looger LL. (2009). Imaging neural activity in worms, flies and mice with improvedGCaMPcalcium indicators. Nat Methods 6:875-881. CrossRef Medline
52. Todorov E., Jordan MI. (2002). Optimal feedback control as a theory of motor coordination. Nat Neurosci 5:1226-1235. CrossRef Medline
53. Tohmi M., Takahashi K, Kubota Y, Hishida R, Shibuki K. (2009). Transcranial flavoprotein fluorescence imaging of mouse cortical activity and plasticity. J Neurochem 109:3-9. CrossRef Medline
54. Travers JB., Dinardo LA, Karimnamazi H. (1997). Motor and premotor mechanisms of licking. Neurosci Biobehav Rev 21:631-647. CrossRef Medline
55. Wang H., Peca J, Matsuzaki M, Matsuzaki K, Noguchi J, Qiu L, Wang D, Zhang F., Boyden E, Deisseroth K, Kasai H, Hall WC, Feng G, Augustine GJ. (2007). High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc Natl Acad Sci U S A 104:8143-8148. CrossRef Medline
56. Wessberg J., Stambaugh CR, Kralik JD, Beck PD, Laubach M, Chapin JK, Kim J, Biggs SJ, Srinivasan MA, Nicolelis MAL. (2000). Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408:361-365. CrossRef Medline
57. Yoshimura Y., Dantzker JLM, Callaway EM. (2005). Excitatory cortical neurons form fine-scale functional networks. Nature 433:868-873. CrossRef Medline