In mice lacking V2a interneurons, gait depends on speed of locomotion

Journal of Neuroscience

Volumn 29, Issue 21, 2009, Pages 7098-7109

  Crone, Steven A ^a   Zhong, Guisheng ^b   Harris Warrick, Ronald ^b   Sharma, Kamal ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHX10 GENE; CONTROLLED STUDY; FEMALE; FORELIMB; GAIT; GENE; HINDLIMB; INTERNEURON; LOCOMOTION; MALE; MOTOR ACTIVITY; MOUSE; MOVEMENT (PHYSIOLOGY); NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RUNNING; SPINAL CORD STIMULATION; STANDING; VELOCITY; WILD TYPE;

ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BIRTH WEIGHT; CHOLINESTERASES; DIPHTHERIA TOXIN; EXERCISE TEST; FUNCTIONAL LATERALITY; GAIT; GATA3 TRANSCRIPTION FACTOR; HOMEODOMAIN PROTEINS; INTERNEURONS; LOCOMOTION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, TRANSGENIC; N-METHYLASPARTATE; PEPTIDE FRAGMENTS; PSYCHOMOTOR PERFORMANCE; SEROTONIN; SPINAL CORD; TRANSCRIPTION FACTORS;

EID: 66149168576     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1206-09.2009     Document Type: Article

References (48)

1. Al-Mosawie A, Wilson JM, Brownstone RM (2007) Heterogeneity of V2-derived interneurons in the adult mouse spinal cord. Eur J Neurosci 26:3003-3015. (Pubitemid 350135168)
2. Bracci E, Ballerini L, Nistri A (1996) Spontaneous rhythmic bursts induced by pharmacological block of inhibition in lumbar motoneurons of the neonatal rat spinal cord. J Neurophysiol 75:640-647. (Pubitemid 26073462)
3. Butt SJ, Kiehn O (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:953-963. (Pubitemid 36782385)
4. Cazalets JR, Sqalli-Houssaini Y, Clarac F (1994) GABAergic inactivation of the central pattern generators for locomotion in isolated neonatal rat spinal cord. J Physiol 474:173-181. (Pubitemid 24045641)
5. Chevallier S, Jan Ijspeert A, Ryczko D, Nagy F, Cabelguen JM (2008) Organisation of the spinal central pattern generators for locomotion in the salamander: biology and modelling. Brain Res Rev 57:147-161. (Pubitemid 350213104)
6. Clarke KA, Still J (1999) Gait analysis in the mouse. Physiol Behav 66:723-729. (Pubitemid 29281632)
7. Clarke KA, Still J (2001) Development and consistency of gait in the mouse. Physiol Behav 73:159-164. (Pubitemid 32530553)
8. Cohen AH, Harris-Warrick RM (1984) Strychnine eliminates alternating motor output during fictive locomotion in the lamprey. Brain Res 293:164-167. (Pubitemid 14150196)
9. Cowley KC, Schmidt BJ (1995) Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J Neurophysiol 74:1109-1117.
10. Crone SA, Quinlan KA, Zagoraiou L, Droho S, Restrepo CE, Lundfald L, Endo T, Setlak J, Jessell TM, Kiehn O, Sharma K (2008) Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 60:70-83.
11. Forssberg H, Grillner S, Halbertsma J, Rossignol S (1980) The locomotion of the low spinal cat. II. Interlimb coordination. Acta Physiol Scand 108:283-295.
12. Gordon IT, Whelan PJ (2006) Monoaminergic control of cauda-equina-evoked locomotion in the neonatal mouse spinal cord. J Neurophysiol 96:3122-3129.
13. Goulding M, Pfaff SL (2005) Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr Opin Neurobiol 15:14-20. (Pubitemid 40249956)
14. Hagevik A, McClellan AD (1994) Coupling of spinal locomotor networks in larval lamprey revealed by receptor blockers for inhibitory amino acids: neurophysiology and computer modeling. J Neurophysiol 72:1810-1829. (Pubitemid 24325104)
15. Hale ME, Day RD, Thorsen DH, Westneat MW (2006) Pectoral fin coordination and gait transitions in steadily swimming juvenile reef fishes. J Exp Biol 209:3708-3718. (Pubitemid 44682335)
16. Han F, Strohl KP (2000) Inheritance of ventilatory behavior in rodent models. Respir Physiol 121:247-256. (Pubitemid 30645522)
17. Han F, Subramanian S, Dick TE, Dreshaj IA, Strohl KP (2001) Ventilatory behavior after hypoxia in C57BL/6J and A/J mice. J Appl Physiol 91:1962-1970. (Pubitemid 33015043)
18. Han F, Subramanian S, Price ER, Nadeau J, Strohl KP (2002) Periodic breathing in the mouse. J Appl Physiol 92:1133-1140. (Pubitemid 34670971)
19. Herbin M, Hackert R, Gasc JP, Renous S (2007) Gait parameters of treadmill versus overground locomotion in mouse. Behav Brain Res 181:173-179. (Pubitemid 46908752)
20. Higashijima S, Masino MA, Mandel G, Fetcho JR (2004) Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 24:5827-5839. (Pubitemid 38857237)
21. Hildebrand M (1989) The quadrupedal gaits of vertebrates. Bioscience 39:766-775.
22. Hinckley C, Seebach B, Ziskind-Conhaim L (2005) Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience 131:745-758. (Pubitemid 40261228)
23. Juvin L, Simmers J, Morin D (2007) Locomotor rhythmogenesis in the isolated rat spinal cord: a phase-coupled set of symmetrical flexion extension oscillators. J Physiol 583:115-128. (Pubitemid 47244248)
24. Kimura Y, Okamura Y, Higashijima S (2006) alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J Neurosci 26:5684-5697. (Pubitemid 44315260)
25. Kjaerulff O, Kiehn O (1996) Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J Neurosci 16:5777-5794. (Pubitemid 26293400)
26. Kremer E, Lev-Tov A (1997) Localization of the spinal network associated with generation of hindlimb locomotion in the neonatal rat and organization of its transverse coupling system. J Neurophysiol 77:1155-1170. (Pubitemid 27137016)
27. Kriellaars DJ, Brownstone RM, Noga BR, Jordan LM (1994) Mechanical entrainment of fictive locomotion in the decerebrate cat. J Neurophysiol 71:2074-2086. (Pubitemid 24184854)
28. Kullander K, Butt SJ, Lebret JM, Lundfald L, Restrepo CE, Rydström A, Klein R, Kiehn O (2003) Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299:1889-1992. (Pubitemid 36358203)
29. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M (2004) Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42:375-386. (Pubitemid 38610137)
30. Lewis KE (2006) How do genes regulate simple behaviours? Understanding how different neurons in the vertebrate spinal cord are genetically specified. Philos Trans R Soc Lond B Biol Sci 361:45-66.
31. Liao JC, Fetcho JR (2008) Shared versus specialized glycinergic spinal interneurons in axial motor circuits of larval zebrafish. J Neurosci 28:12982-12992.
32. Lundfald L, Restrepo CE, Butt SJ, Peng CY, Droho S, Endo T, Zeilhofer HU, Sharma K, Kiehn O (2007) Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur J Neurosci 26:2989-3002. (Pubitemid 350135167)
33. McLean DL, Fan J, Higashijima S, Hale ME, Fetcho JR (2007) Atopographic map of recruitment in spinal cord. Nature 446:71-75. (Pubitemid 46348046)
34. McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR (2008) Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 11:1419-1429.
35. Nauwelaerts SA, Aerts P (2002) Two distinct gait types in swimming frogs. J Zool 258:183-188. (Pubitemid 35255064)
36. Peng CY, Yajima H, Burns CE, Zon LI, Sisodia SS, Pfaff SL, Sharma K (2007) Notch and MAML signaling drives Scl-dependent interneuron diversity in the spinal cord. Neuron 53:813-827. (Pubitemid 46389564)
37. Quinlan KA, Kiehn O (2007) Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J Neurosci 27:6521-6530. (Pubitemid 46920380)
38. Ritter DA, Bhatt DH, Fetcho JR (2001) In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J Neurosci 21:8956-8965.
39. Rossignol S, Dubuc R, Gossard JP (2006) Dynamic sensorimotor interactions in locomotion. Physiol Rev 86:89-154.
40. Schlenker E, Shi Y, Johnson C, Wipf J (2006) Acetazolamide affects breathing differently in ICR and C57 mice. Respir Physiol Neurobiol 152:119-127. (Pubitemid 43776114)
41. Sillar KT, Roberts A (1993) Control of frequency during swimming in Xenopus embryos: a study on interneuronal recruitment in a spinal rhythm generator. J Physiol 472:557-572.
42. Stettner GM, Zanella S, Huppke P, Gärtner J, Hilaire G, Dutschmann M (2008) Spontaneous central apneas occur in the C57BL/6J mouse strain. Respir Physiol Neurobiol 160:21-27. (Pubitemid 350213547)
43. Thaler J, Harrison K, Sharma K, Lettieri K, Kehrl J, Pfaff SL (1999) Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23:675-687. (Pubitemid 29411558)
44. Thorsen DH, Cassidy JJ, Hale ME (2004) Swimming of larval zebrafish: fin-axis coordination and implications for function and neural control. J Exp Biol 207:4175-4183. (Pubitemid 40099368)
45. Whelan P, Bonnot A, O'Donovan MJ (2000) Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J Neurophysiol 84:2821-2833.
46. Yakovenko S, McCrea DA, Stecina K, Prochazka A (2005) Control of loco-motor cycle durations. J Neurophysiol 94:1057-1065.
47. Zar JH (2000) Biostatistical analysis, Ed 4. Upper Saddle River, NJ: Prentice-Hall.
48. Zhong G, Masino MA, Harris-Warrick RM (2007) Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27:4507-4518. (Pubitemid 46663577)