Modular deconstruction reveals the dynamical and physical building blocks of a locomotion motor program

Neuron

Volumn 86, Issue 1, 2015, Pages 304-318

  Bruno, Angela M ^a   Frost, William N ^a   Humphries, Mark D ^b  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; APLYSIA; ARTICLE; CENTRAL PATTERN GENERATOR; CONTROLLED STUDY; ESCAPE BEHAVIOR; GANGLION; LOCOMOTION; MOTOR PERFORMANCE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; ROTATION; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BRAIN; BRAIN MAPPING; MOTONEURON; NERVE CELL NETWORK; NONLINEAR SYSTEM; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; APLYSIA; BRAIN; BRAIN MAPPING; LOCOMOTION; MODELS, NEUROLOGICAL; MOTOR NEURONS; NERVE NET; NONLINEAR DYNAMICS;

EID: 84930324540     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.005     Document Type: Article

References (62)

1. Ahrens M.B., Li J.M., Orger M.B., Robson D.N., Schier A.F., Engert F., Portugues R. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 2012, 485:471-477.
2. Ahrens M.B., Orger M.B., Robson D.N., Li J.M., Keller P.J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 2013, 10:413-420.
3. Berg R.W., Alaburda A., Hounsgaard J. Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 2007, 315:390-393.
4. Brezina V., Orekhova I.V., Weiss K.R. The neuromuscular transform: the dynamic, nonlinear link between motor neuron firing patterns and muscle contraction in rhythmic behaviors. J.Neurophysiol. 2000, 83:207-231.
5. Briggman K.L., Kristan W.B. Imaging dedicated and multifunctional neural circuits generating distinct behaviors. J.Neurosci. 2006, 26:10925-10933.
6. Briggman K.L., Abarbanel H.D.I., Kristan W.B. Optical imaging of neuronal populations during decision-making. Science 2005, 307:896-901.
7. Cacciatore T.W., Rozenshteyn R., Kristan W.B. Kinematics and modeling of leech crawling: evidence for an oscillatory behavior produced by propagating waves of excitation. J.Neurosci. 2000, 20:1643-1655.
8. Cash D., Carew T.J. A quantitative analysis of the development of the central nervous system in juvenile Aplysia californica. J.Neurobiol. 1989, 20:25-47.
9. Churchland M.M., Cunningham J.P., Kaufman M.T., Foster J.D., Nuyujukian P., Ryu S.I., Shenoy K.V. Neural population dynamics during reaching. Nature 2012, 487:51-56.
10. Cohen L.B., Lesher S. Optical monitoring of membrane potential: methods of multisite optical measurement. Soc. Gen. Physiol. Ser. 1986, 40:71-99.
11. Compte A., Constantinidis C., Tegner J., Raghavachari S., Chafee M.V., Goldman-Rakic P.S., Wang X.-J. Temporally irregular mnemonic persistent activity in prefrontal neurons of monkeys during a delayed response task. J.Neurophysiol. 2003, 90:3441-3454.
12. Cunningham J.P., Yu B.M. Dimensionality reduction for large-scale neural recordings. Nat. Neurosci. 2014, 17:1500-1509.
13. Eisenhart F.J., Cacciatore T.W., Kristan W.B. A central pattern generator underlies crawling in the medicinal leech. J.Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2000, 186:631-643.
14. Eliasmith C. A unified approach to building and controlling spiking attractor networks. Neural Comput. 2005, 17:1276-1314.
15. Esposito M.S., Capelli P., Arber S. Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 2014, 508:351-356.
16. Fitzgibbon A.W., Pilu M., Fisher R.B. Direct least-squares fitting of ellipses. IEEE Trans. Pattern Anal. Mach. Intell. 1999, 21:476-480.
17. Flood T.F., Iguchi S., Gorczyca M., White B., Ito K., Yoshihara M. A single pair of interneurons commands the Drosophila feeding motor program. Nature 2013, 499:83-87.
18. Fredman S.M., Jahan-Parwar B. Role of pedal ganglia motor neurons in pedal wave generation in Aplysia. Brain Res. Bull. 1980, 5:179-193.
19. Fredman S.M., Jahan-Parwar B. Command neurons for locomotion in Aplysia. J.Neurophysiol. 1983, 49:1092-1117.
20. Frost W.N., Katz P.S. Single neuron control over a complex motor program. Proc. Natl. Acad. Sci. USA 1996, 93:422-426.
21. Getting P.A. Emerging principles governing the operation of neural networks. Annu. Rev. Neurosci. 1989, 12:185-204.
22. Gjorgjieva J., Berni J., Evers J.F., Eglen S.J. Neural circuits for peristaltic wave propagation in crawling Drosophila larvae: analysis and modeling. Front. Comput. Neurosci. 2013, 7:24.
23. Grillner S., Hellgren J., Ménard A., Saitoh K., Wikström M.A. Mechanisms for selection of basic motor programs-roles for the striatum and pallidum. Trends Neurosci. 2005, 28:364-370.
24. Hall J.D., Lloyd P.E. Involvement of pedal peptide in locomotion in Aplysia: modulation of foot muscle contractions. J.Neurobiol. 1990, 21:858-868.
25. Harris K.D. Neural signatures of cell assembly organization. Nat. Rev. Neurosci. 2005, 6:399-407.
26. Hening W.A., Walters E.T., Carew T.J., Kandel E.R. Motorneuronal control of locomotion in Aplysia. Brain Res. 1979, 179:231-253.
27. Hill E.S., Moore-Kochlacs C., Vasireddi S.K., Sejnowski T.J., Frost W.N. Validation of independent component analysis for rapid spike sorting of optical recording data. J.Neurophysiol. 2010, 104:3721-3731.
28. Hill E.S., Vasireddi S.K., Bruno A.M., Wang J., Frost W.N. Variable neuronal participation in stereotypic motor programs. PLoS ONE 2012, 7:e40579.
29. Humphries M.D. Spike-train communities: finding groups of similar spike trains. J.Neurosci. 2011, 31:2321-2336.
30. Jahan-Parwar B., Fredman S.M. Neural control of locomotion in Aplysia: role of the central ganglia. Behav. Neural Biol. 1979, 27:39-58.
31. Jahan-Parwar B., Fredman S.M. Motor program for pedal waves during Aplysia locomotion is generated in the pedal ganglia. Brain Res. Bull. 1980, 5:169-177.
32. Jing J., Cropper E.C., Hurwitz I., Weiss K.R. The construction of movement with behavior-specific and behavior-independent modules. J.Neurosci. 2004, 24:6315-6325.
33. Katz P.S., Getting P.A., Frost W.N. Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 1994, 367:729-731.
34. Koch C. Systems biology. Modular biological complexity. Science 2012, 337:531-532.
35. Kupfermann I., Weiss K.R. Motor program selection in simple model systems. Curr. Opin. Neurobiol. 2001, 11:673-677.
36. Larsch J., Ventimiglia D., Bargmann C.I., Albrecht D.R. High-throughput imaging of neuronal activity in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 2013, 110:E4266-E4273.
37. Levi R., Varona P., Arshavsky Y.I., Rabinovich M.I., Selverston A.I. The role of sensory network dynamics in generating a motor program. J.Neurosci. 2005, 25:9807-9815.
38. Machens C.K. Demixing population activity in higher cortical areas. Front. Comput. Neurosci. 2010, 4:126.
39. Mattia M., Pani P., Mirabella G., Costa S., Del Giudice P., Ferraina S. Heterogeneous attractor cell assemblies for motor planning in premotor cortex. J.Neurosci. 2013, 33:11155-11168.
40. McPherson D.R., Blankenship J.E. Neuronal modulation of foot and body-wall contractions in Aplysia californica. J.Neurophysiol. 1992, 67:23-28.
41. Mink J.W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 1996, 50:381-425.
42. Newman M.E.J. Finding community structure in networks using the eigenvectors of matrices. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2006, 74:036104.
43. Newman M.E.J. Modularity and community structure in networks. Proc. Natl. Acad. Sci. USA 2006, 103:8577-8582.
44. Niessing J., Friedrich R.W. Olfactory pattern classification by discrete neuronal network states. Nature 2010, 465:47-52.
45. Peyrache A., Khamassi M., Benchenane K., Wiener S.I., Battaglia F.P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 2009, 12:919-926.
46. Rokni U., Sompolinsky H. How the brain generates movement. Neural Comput. 2012, 24:289-331.
47. Schöner G., Kelso J.A. Dynamic pattern generation in behavioral and neural systems. Science 1988, 239:1513-1520.
48. Schoofs A., Hückesfeld S., Schlegel P., Miroschnikow A., Peters M., Zeymer M., Spie R., Chiang A.S., Pankratz M.J. Selection of motor programs for suppressing food intake and inducing locomotion in the Drosophila brain. PLoS Biol. 2014, 12:e1001893.
49. Seelig J.D., Chiappe M.E., Lott G.K., Dutta A., Osborne J.E., Reiser M.B., Jayaraman V. Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior. Nat. Methods 2010, 7:535-540.
50. Selverston A.I. Invertebrate central pattern generator circuits. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010, 365:2329-2345.
51. Summers J.J., Anson J.G. Current status of the motor program: revisited. Hum. Mov. Sci. 2009, 28:566-577.
52. Traud A.L., Frost C., Mucha P.J., Porter M.A. Visualization of communities in networks. Chaos 2009, 19:041104.
53. Tsau Y., Wu J.Y., Höpp H.P., Cohen L.B., Schiminovich D., Falk C.X. Distributed aspects of the response to siphon touch in Aplysia: spread of stimulus information and cross-correlation analysis. J.Neurosci. 1994, 14:4167-4184.
54. Wehr M., Laurent G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 1996, 384:162-166.
55. Wickens J., Hyland B., Anson G. Cortical cell assemblies: a possible mechanism for motor programs. J.Mot. Behav. 1994, 26:66-82.
56. Wohrer A., Humphries M.D., Machens C.K. Population-wide distributions of neural activity during perceptual decision-making. Prog. Neurobiol. 2013, 103:156-193.
57. Wu J.Y., Cohen L.B., Falk C.X. Neuronal activity during different behaviors in Aplysia: a distributed organization?. Science 1994, 263:820-823.
58. Xin Y., Weiss K.R., Kupfermann I. An identified interneuron contributes to aspects of six different behaviors in Aplysia. J.Neurosci. 1996, 16:5266-5279.
59. Yoon K., Buice M.A., Barry C., Hayman R., Burgess N., Fiete I.R. Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 2013, 16:1077-1084.
60. Yuste R., MacLean J.N., Smith J., Lansner A. The cortex as a central pattern generator. Nat. Rev. Neurosci. 2005, 6:477-483.
61. Zhang K. Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J.Neurosci. 1996, 16:2112-2126.
62. Zochowski M., Wachowiak M., Falk C.X., Cohen L.B., Lam Y.W., Antic S., Zecevic D. Imaging membrane potential with voltage-sensitive dyes. Biol. Bull. 2000, 198:1-21.