Phenotypic characterization of speed-associated gait changes in mice reveals modular organization of locomotor networks

Current Biology

Volumn 25, Issue 11, 2015, Pages 1426-1436

  Bellardita, Carmelo ^a   Kiehn, Ole ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MUS;

ANIMAL; BIOMECHANICS; CENTRAL PATTERN GENERATOR; FEMALE; GAIT; LIMB; LOCOMOTION; MOUSE; PHYSIOLOGY;

ANIMALS; BIOMECHANICAL PHENOMENA; CENTRAL PATTERN GENERATORS; EXTREMITIES; FEMALE; GAIT; LOCOMOTION; MICE;

EID: 84930926500     PISSN: 09609822     EISSN: 18790445     Source Type: Journal    
DOI: 10.1016/j.cub.2015.04.005     Document Type: Article

References (42)

1. D.L. McLean, and J.R. Fetcho Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones J. Neurosci. 29 2009 13566 13577
2. D.L. McLean, M.A. Masino, I.Y. Koh, W.B. Lindquist, and J.R. Fetcho Continuous shifts in the active set of spinal interneurons during changes in locomotor speed Nat. Neurosci. 11 2008 1419 1429
3. K. Ampatzis, J. Song, J. Ausborn, and A. El Manira Separate microcircuit modules of distinct v2a interneurons and motoneurons control the speed of locomotion Neuron 83 2014 934 943
4. A.E. Talpalar, J. Bouvier, L. Borgius, G. Fortin, A. Pierani, and O. Kiehn Dual-mode operation of neuronal networks involved in left-right alternation Nature 500 2013 85 88
5. S.A. Crone, K.A. Quinlan, L. Zagoraiou, S. Droho, C.E. Restrepo, L. Lundfald, T. Endo, J. Setlak, T.M. Jessell, O. Kiehn, and K. Sharma Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord Neuron 60 2008 70 83
6. S.A. Crone, G. Zhong, R. Harris-Warrick, and K. Sharma In mice lacking V2a interneurons, gait depends on speed of locomotion J. Neurosci. 29 2009 7098 7109
7. G. Zhong, S. Droho, S.A. Crone, S. Dietz, A.C. Kwan, W.W. Webb, K. Sharma, and R.M. Harris-Warrick Electrophysiological characterization of V2a interneurons and their locomotor-related activity in the neonatal mouse spinal cord J. Neurosci. 30 2010 170 182
8. G. Zhong, K. Sharma, and R.M. Harris-Warrick Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord Nat. Commun. 2 2011 274
9. K.J. Dougherty, and O. Kiehn Functional organization of V2a-related locomotor circuits in the rodent spinal cord Ann. N Y Acad. Sci. 1198 2010 85 93
10. K.J. Dougherty, L. Zagoraiou, D. Satoh, I. Rozani, S. Doobar, S. Arber, T.M. Jessell, and O. Kiehn Locomotor rhythm generation linked to the output of spinal shox2 excitatory interneurons Neuron 80 2013 920 933
11. M. Hildebrand Symmetrical gaits of horses Science 150 1965 701 708
12. H. Leblond, M. L'Esperance, D. Orsal, and S. Rossignol Treadmill locomotion in the intact and spinal mouse J. Neurosci. 23 2003 11411 11419
13. M. Herbin, J.P. Gasc, and S. Renous Symmetrical and asymmetrical gaits in the mouse: patterns to increase velocity J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190 2004 895 906
14. M. Herbin, R. Hackert, J.P. Gasc, and S. Renous Gait parameters of treadmill versus overground locomotion in mouse Behav. Brain Res. 181 2007 173 179
15. K.A. Clarke, and J. Still Gait analysis in the mouse Physiol. Behav. 66 1999 723 729
16. N. Serradj, and M. Jamon The adaptation of limb kinematics to increasing walking speeds in freely moving mice 129/Sv and C57BL/6 Behav. Brain Res. 201 2009 59 65
17. T. Akay, H.J. Acharya, K. Fouad, and K.G. Pearson Behavioral and electromyographic characterization of mice lacking EphA4 receptors J. Neurophysiol. 96 2006 642 651
18. R.J. Batka, T.J. Brown, K.P. Mcmillan, R.M. Meadows, K.J. Jones, and M.M. Haulcomb The need for speed in rodent locomotion analyses Anat. Rec. (Hoboken) 297 2014 1839 1864
19. N.C. Heglund, and C.R. Taylor Speed, stride frequency and energy cost per stride: how do they change with body size and gait? J. Exp. Biol. 138 1988 301 318
20. K. Kullander, S.J. Butt, J.M. Lebret, L. Lundfald, C.E. Restrepo, A. Rydström, R. Klein, and O. Kiehn Role of EphA4 and EphrinB3 in local neuronal circuits that control walking Science 299 2003 1889 1892
21. K.A. Quinlan, and O. Kiehn Segmental, synaptic actions of commissural interneurons in the mouse spinal cord J. Neurosci. 27 2007 6521 6530
22. O. Kjaerulff, and O. Kiehn Crossed rhythmic synaptic input to motoneurons during selective activation of the contralateral spinal locomotor network J. Neurosci. 17 1997 9433 9447
23. C.E. Restrepo, L. Lundfald, G. Szabó, F. Erdélyi, H.U. Zeilhofer, J.C. Glover, and O. Kiehn Transmitter-phenotypes of commissural interneurons in the lumbar spinal cord of newborn mice J. Comp. Neurol. 517 2009 177 192
24. C.E. Restrepo, G. Margaryan, L. Borgius, L. Lundfald, D. Sargsyan, and O. Kiehn Change in the balance of excitatory and inhibitory midline fiber crossing as an explanation for the hopping phenotype in EphA4 knockout mice Eur. J. Neurosci. 34 2011 1102 1112
25. S.J. Butt, J.M. Lebret, and O. Kiehn Organization of left-right coordination in the mammalian locomotor network Brain Res. Brain Res. Rev. 40 2002 107 117
26. O. Kiehn Development and functional organization of spinal locomotor circuits Curr. Opin. Neurobiol. 21 2011 100 109
27. G.M. Lanuza, S. Gosgnach, A. Pierani, T.M. Jessell, and M. Goulding Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements Neuron 42 2004 375 386
28. L.S. Andersson, M. Larhammar, F. Memic, H. Wootz, D. Schwochow, C.J. Rubin, K. Patra, T. Arnason, L. Wellbring, and G. Hjälm Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice Nature 488 2012 642 646
29. Y. Zhang, S. Narayan, E. Geiman, G.M. Lanuza, T. Velasquez, B. Shanks, T. Akay, J. Dyck, K. Pearson, and S. Gosgnach V3 spinal neurons establish a robust and balanced locomotor rhythm during walking Neuron 60 2008 84 96
30. A. Pierani, L. Moran-Rivard, M.J. Sunshine, D.R. Littman, M. Goulding, and T.M. Jessell Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1 Neuron 29 2001 367 384
31. O. Kiehn Locomotor circuits in the mammalian spinal cord Annu. Rev. Neurosci. 29 2006 279 306
32. M. Goulding Circuits controlling vertebrate locomotion: moving in a new direction Nat. Rev. Neurosci. 10 2009 507 518
33. P.J. Whelan Shining light into the black box of spinal locomotor networks Philos. Trans. R. Soc. Lond. B Biol. Sci. 365 2010 2383 2395
34. S. Grillner, and T.M. Jessell Measured motion: searching for simplicity in spinal locomotor networks Curr. Opin. Neurobiol. 19 2009 572 586
35. A.E. Talpalar, and O. Kiehn Glutamatergic mechanisms for speed control and network operation in the rodent locomotor CpG Front. Neural Circuits 4 2010 19
36. L. Borgius, H. Nishimaru, V. Caldeira, Y. Kunugise, P. Löw, R. Reig, S. Itohara, T. Iwasato, and O. Kiehn Spinal glutamatergic neurons defined by EphA4 signaling are essential components of normal locomotor circuits J. Neurosci. 34 2014 3841 3853
37. M.L. Andermann, A.M. Kerlin, D.K. Roumis, L.L. Glickfeld, and R.C. Reid Functional specialization of mouse higher visual cortical areas Neuron 72 2011 1025 1039
38. G.B. Keller, T. Bonhoeffer, and M. Hübener Sensorimotor mismatch signals in primary visual cortex of the behaving mouse Neuron 74 2012 809 815
39. J. Berger, S. Eckert, R. Scardigli, F. Guillemot, P. Gruss, and A. Stoykova E1-Ngn2/Cre is a new line for regional activation of Cre recombinase in the developing CNS Genesis 40 2004 195 199
40. B.A. Strange, M.P. Witter, E.S. Lein, and E.I. Moser Functional organization of the hippocampal longitudinal axis Nat. Rev. Neurosci. 15 2014 655 669
41. F. Bielle, A. Griveau, N. Narboux-Nême, S. Vigneau, M. Sigrist, S. Arber, M. Wassef, and A. Pierani Multiple origins of Cajal-Retzius cells at the borders of the developing pallium Nat. Neurosci. 8 2005 1002 1012
42. L. Borgius, C.E. Restrepo, R.N. Leao, N. Saleh, and O. Kiehn A transgenic mouse line for molecular genetic analysis of excitatory glutamatergic neurons Mol. Cell. Neurosci. 45 2010 245 257