Two distinct layer-specific dynamics of cortical ensembles during learning of a motor task

Nature Neuroscience

Volumn 17, Issue 7, 2014, Pages 987-994

  Masamizu, Yoshito ^a,b   Tanaka, Yasuhiro R ^a,b   Tanaka, Yasuyo H ^a,b   Hira, Riichiro ^a,b   Ohkubo, Fuki ^a,b,c   Kitamura, Kazuo ^b,d   Isomura, Yoshikazu ^b,e   Okada, Takashi ^f,g   Matsuzaki, Masanori ^a,b,c  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e TAMAGAWA UNIVERSITY   (Japan)

^f NIPPON MEDICAL SCHOOL   (Japan)

^g NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM;

ACCURACY; ANIMAL CELL; ARTICLE; COORDINATION; DYNAMICS; IMAGING; LEARNING; MOTOR PERFORMANCE; MOTOR TASK; MOUSE; MOVEMENT (PHYSIOLOGY); NERVE CELL; NONHUMAN; PHOTON; PREDICTION; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE; ANIMAL EXPERIMENT; BRAIN FUNCTION; BRAIN NERVE CELL; FORELIMB; NEUROSCIENCE;

ANIMALS; CONDITIONING, OPERANT; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; DEPENDOVIRUS; EFFERENT PATHWAYS; FORELIMB; GENETIC VECTORS; IMAGE PROCESSING, COMPUTER-ASSISTED; LEARNING; MALE; MICE; MICE, INBRED C57BL; MOTOR CORTEX; MOTOR NEURONS; MOTOR SKILLS; NEUROIMAGING; NEURONS; PATCH-CLAMP TECHNIQUES; PSYCHOMOTOR PERFORMANCE; REWARD;

EID: 84903395909     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3739     Document Type: Article

References (57)

1. Weiler, N., Wood, L., Yu, J., Solla, S.A. & Shepherd, G.M.G. Top-down laminar organization of the excitatory network in motor cortex. Nat. Neurosci. 11, 360-366 (2008).
2. Anderson, C.T., Sheets, P.L., Kiritani, T. & Shepherd, G.M.G. Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat. Neurosci. 13, 739-744 (2010).
3. Thoroughman, K.A. & Shadmehr, R. Learning of action through adaptive combination of motor primitives. Nature 407, 742-747 (2000).
4. Todorov, E. & Jordan, M.I. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226-1235 (2002).
5. Sing, G.C., Joiner, W.M., Nanayakkara, T., Brayanov, J.B. & Smith, M.A. Primitives for motor adaptation reflect correlated neural tuning to position and velocity. Neuron 64, 575-589 (2009).
6. Scott, S.H. The computational and neural basis of voluntary motor control and planning. Trends Cogn. Sci. 16, 541-549 (2012).
7. Mitz, A.R., Godschalk, M. & Wise, S.P. Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations. J. Neurosci. 11, 1855-1872 (1991).
8. Nudo, R.J., Milliken, G.W., Jenkins, W.M. & Merzenich, M.M. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J. Neurosci. 16, 785-807 (1996).
9. Sanes, J.N. & Donoghue, J.P. Plasticity and primary motor cortex. Annu. Rev. Neurosci. 23, 393-415 (2000).
10. Ungerleider, L.G., Doyon, J. & Karni, A. Imaging brain plasticity during motor skill learning. Neurobiol. Learn. Mem. 78, 553-564 (2002).
11. Kleim, J.A. et al. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 24, 628-633 (2004).
12. Laubach, M., Wessberg, J. & Nicolelis, M.A.L. Cortical ensemble activity increasingly predicts behavior outcomes during learning of a motor task. Nature 405, 567-571 (2000).
13. Carmena, J.M. et al. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol. 1, e42 (2003).
14. Cohen, D. & Nicolelis, M.A.L. Reduction of single-neuron firing uncertainty by cortical ensembles during motor skill learning. J. Neurosci. 24, 3574-3582 (2004).
15. Paz, R. & Vaadia, E. Learning-induced improvement in encoding and decoding of specific movement directions by neurons in the primary motor cortex. PLoS Biol. 2, e45 (2004).
16. Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473-478 (2012).
17. Rokni, U., Richardson, A.G., Bizzi, E. & Seung, H.S. Motor learning with unstable neural representations. Neuron 54, 653-666 (2007).
18. Chestek, C.A. et al. Single-neuron stability during repeated reaching in macaque premotor cortex. J. Neurosci. 27, 10742-10750 (2007).
19. Lütcke, H., Margolis, D.J. & Helmchen, F. Steady or changing? Long-term monitoring of neuronal population activity. Trends Neurosci. 36, 375-384 (2013).
20. Carmena, J.M., Lebedev, M.A., Henriquez, C.S. & Nicolelis, M.A.L. Stable ensemble performance with single-neuron variability during reaching movements in primates. J. Neurosci. 25, 10712-10716 (2005).
21. Hira, R. et al. Spatiotemporal dynamics of functional clusters of neurons in the mouse motor cortex during a voluntary movement. J. Neurosci. 33, 1377-1390 (2013).
22. Tennant, K.A. et al. 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 (2011).
23. 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).
24. Tian, L. et al. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat. Methods 6, 875-881 (2009).
25. Thévenaz, P., Ruttimann, U.E. & Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27-41 (1998).
26. Dombeck, D.A., Khabbaz, A.N., Collman, F., Adelman, T.L. & Tank, D.W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56, 43-57 (2007).
27. Vogelstein, J.T. et al. Spike inference from calcium imaging using sequential monte carlo methods. Biophys. J. 97, 636-655 (2009).
28. Drucker, H., Burges, C.J.C., Kaufman, L., Smola, A. & Vapnik, V. Support vector regression machines. Adv. Neural Inf. Process. Syst. 9, 155-161 (1997).
29. Nelson, R.B. An Introduction to Copulas, 2nd edn. (Springer, New York, 2006).
30. Davy, M. & Doucet, A. Copulas: a new insight into positive time-frequency distributions. IEEE Signal Process. Lett. 10, 215-218 (2003).
31. Wessberg, J. et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 408, 361-365 (2000).
32. Isomura, Y. et al. Reward-modulated motor information in identified striatum neurons. J. Neurosci. 33, 10209-10220 (2013).
33. Yin, H.H. et al. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12, 333-341 (2009).
34. Kiritani, T., Wickersham, I.R., Seung, H.S. & Shepherd, G.M. Hierarchical connectivity and connection-specific dynamics in the corticospinal-corticostriatal microcircuit in mouse motor cortex. J. Neurosci. 32, 4992-5001 (2012).
35. Masamizu, Y. et al. Local and retrograde gene transfer into primate neuronal pathways via adeno-associated virus serotype 8 and 9. Neuroscience 193, 249-258 (2011).
36. Abbott, L.F. & Nelson, S.B. Synaptic plasticity: taming the beast. Nat. Neurosci. 3, 1178-1183 (2000).
37. Mao, T. et al. Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72, 111-123 (2011).
38. Thorn, C.A., Atallah, H., Howe, M. & Graybiel, A.M. Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 66, 781-795 (2010).
39. Yin, H.H. & Knowlton, B.J. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 7, 464-476 (2006).
40. Iwaniuk, A.N. & Whishaw, I.Q. On the origin of skilled forelimb movements. Trends Neurosci. 23, 372-376 (2000).
41. Kimura, R. et al. Reinforcing operandum: rapid and reliable learning of skilled forelimb movements by head-fixed rodents. J. Neurophysiol. 108, 1781-1792 (2012).
42. Morishima, M. & Kawaguchi, Y. Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci. 26, 4394-4405 (2006).
43. Hira, R. et al. In vivo optogenetic tracing of functional corticocortical connections between motor forelimb areas. Front. Neural Circuits 7, 55 (2013).
44. Xiao, W. et al. Gene therapy vectors based on adeno-associated virus type 1. J. Virol. 73, 3994-4003 (1999).
45. Okada, T. et al. Scalable purification of adeno-associated virus serotype 1 (AAV1) and AAV8 vectors, using dual ion-exchange adsorptive membranes. Hum. Gene Ther. 20, 1013-1021 (2009).
46. Holtmaat, A. et al. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nat. Protoc. 4, 1128-1144 (2009).
47. Mittmann, W. et al. Two-photon calcium imaging of evoked activity from L5 somatosensory neurons in vivo. Nat. Neurosci. 14, 1089-1093 (2011).
48. Glickfeld, L.L., Andermann, M.L., Bonin, V. & Reid, R.C. Cortico-cortical projections in mouse visual cortex are functionally target specific. Nat. Neurosci. 16, 219-226 (2013).
49. Keck, T. et al. Synaptic scaling and homeostatic plasticity in the mouse visual cortex in vivo. Neuron 80, 327-334 (2013).
50. Helmchen, F. & Denk, W. Deep tissue two-photon microscopy. Nat. Methods 2, 932-940 (2005).
51. Oheim, M., Beaurepaire, E., Chaigneau, E., Mertz, J. & Charpak, S. Two-photon microscopy in brain tissue: parameters influencing the imaging depth. J. Neurosci. Methods 111, 29-37 (2001).
52. Kitamura, K., Judkewitz, B., Kano, M., Denk, W. & Häusser, M. Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat. Methods 5, 61-67 (2008).
53. Zariwala, H.A. et al. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32, 3131-3141 (2012).
54. Tanaka, Y., Tanaka, Y., Furuta, T., Yanagawa, Y. & Kaneko, T. The effects of cutting solutions on the viability of GABAergic interneurons in cerebral cortical slices of adult mice. J. Neurosci. Methods 171, 118-125 (2008).
55. O'Connor, D.H., Peron, S.P., Huber, D. & Svoboda, K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67, 1048-1061 (2010).
56. Gonchar, Y., Wang, Q. & Burkhalter, A. Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front. Neuroanat. 1, 3 (2007).
57. Zhao, Y. et al. An expanded palette of genetically encoded Ca2+ indicators. Science 333, 1888-1891 (2011).