Adult spinal V2a interneurons show increased excitability and serotonin-dependent bistability

Journal of Neurophysiology

Volumn 113, Issue 4, 2015, Pages 1124-1134

  Husch, Andreas ^a   Dietz, Shelby B ^a   Hong, Diana N ^a   Harris Warrick, Ronald M ^a  

^a Department of Neurobiology and Behavior Cornell University ^*  (United States)

Author keywords

Locomotion; Maturation; Neuromodulation; Spinal cord

Indexed keywords

SEROTONIN;

ACTION POTENTIAL; ADULT; AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL STRUCTURE; CENTRAL PATTERN GENERATOR; CONTROLLED STUDY; FEMALE; INTERNEURON; LOCOMOTION; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMODULATION; NEUROPHYSIOLOGY; NEWBORN; NONHUMAN; PATCH CLAMP TECHNIQUE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; SPINAL CORD; SPINAL CORD NERVE CELL; ANIMAL; CYTOLOGY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; SEROTONINERGIC NERVE CELL;

ACTION POTENTIALS; ANIMALS; INTERNEURONS; MICE; SEROTONERGIC NEURONS; SEROTONIN; SPINAL CORD;

EID: 84923206924     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00741.2014     Document Type: Article

References (65)

1. Abbinanti MD, Harris-Warrick RM. Serotonin modulates multiple calcium current subtypes in commissural interneurons of the neonatal mouse. J Neurophysiol 107: 2212–2219, 2012.
2. Abbinanti MD, Zhong G, Harris-Warrick RM. Postnatal emergence of serotonin-induced plateau potentials in commissural interneurons of the mouse spinal cord. J Neurophysiol 108: 2191–2202, 2012.
3. Al-Mosawie A, Wilson JM, Brownstone RM. Heterogeneity of V2-derived interneurons in the adult mouse spinal cord. Eur J Neurosci 26: 3003–3015, 2007.
4. Ampatzis K, Song J, Ausborn J, El Manira A. Separate microcircuit modules of distinct v2a interneurons and motoneurons control the speed of locomotion. Neuron 83: 934–943, 2014.
5. Arber S. Motor circuits in action: specification, connectivity, and function. Neuron 74: 975–989, 2012.
6. Ausborn J, Mahmood R, El Manira A. Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network. Proc Natl Acad Sci USA 109: E3631–3639, 2012.
7. Azim E, Jiang J, Alstermark B, Jessell TM. Skilled reaching relies on a V2a propriospinal internal copy circuit. Nature 508: 357–363, 2014.
8. Ballion B, Branchereau P, Chapron J, Viala D. Ontogeny of descending serotonergic innervation and evidence for intraspinal 5-HT neurons in the mouse spinal cord. Brain Res Dev Brain Res 137: 81–88, 2002.
9. Bouhadfane M, Tazerart S, Moqrich A, Vinay L, Brocard F. Sodiummediated plateau potentials in lumbar motoneurons of neonatal rats. J Neurosci 33: 15626–15641, 2013.
10. Brown TG. On the nature of the fundamental activity of the nervous centres; together with an analysis of the conditioning of rhythmic activity in progression, and a theory of the evolution of function in the nervous system. J Physiol 48: 18–46, 1914.
11. Buschges A, Scholz H, El Manira A. New moves in motor control. Curr Biol 21: R513–524, 2011.
12. Carlin KP, Liu J, Jordan LM. Postnatal changes in the inactivation properties of voltage-gated sodium channels contribute to the mature firing pattern of spinal motoneurons. J Neurophysiol 99: 2864–2876, 2008.
13. Cazalets JR, Grillner P, Menard I, Cremieux J, Clarac F. Two types of motor rhythm induced by NMDA and amines in an in vitro spinal cord preparation of neonatal rat. Neurosci Lett 111: 116–121, 1990.
14. Clarac F, Vinay L, Cazalets JR, Fady JC, Jamon M. Role of gravity in the development of posture and locomotion in the neonatal rat. Brain Res Brain Res Rev 28: 35–43, 1998.
15. Crone SA, Quinlan KA, Zagoraiou L, Droho S, Restrepo CE, Lundfald L, Endo T, Setlak J, Jessell TM, Kiehn O, Sharma K. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 60: 70–83, 2008.
16. Crone SA, Zhong G, Harris-Warrick R, Sharma K. In mice lacking V2a interneurons, gait depends on speed of locomotion. J Neurosci 29: 7098– 7109, 2009.
17. Dai Y, Jordan LM. Multiple effects of serotonin and acetylcholine on hyperpolarization-activated inward current in locomotor activity-related neurons in Cfos-EGFP mice. J Neurophysiol 104: 366–381, 2010.
18. Diaz-Rios M, Dombeck DA, Webb WW, Harris-Warrick RM. Serotonin modulates dendritic calcium influx in commissural interneurons in the mouse spinal locomotor network. J Neurophysiol 98: 2157–2167, 2007.
19. Dietz S, Husch A, Harris-Warrick RM. A comparison of serotonin neuromodulation of mouse spinal V2a interneurons using perforated patch and whole cell recording techniques. Front Cell Neurosci 6: 39, 2012.
20. Dougherty KJ, Kiehn O. Firing and cellular properties of V2a interneurons in the rodent spinal cord. J Neurosci 30: 24–37, 2010.
21. Eccles JC, Fatt P, Landgren S. Central pathway for direct inhibitory action of impulses in largest afferent nerve fibres to muscle. J Neurophysiol 19: 75–98, 1956. Fenelon VS, Casasnovas B, Faumont S, Meyrand P. Ontogenetic alteration in peptidergic expression within a stable neuronal population in lobster stomatogastric nervous system. J Comp Neurol 399: 289–305, 1998.
22. Fetcho JR, Higashijima S, McLean DL. Zebrafish and motor control over the last decade. Brain Res Rev 57: 86–93, 2008.
23. Fetcho JR, McLean DL. Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications. Ann NY Acad Sci 1198: 94–104, 2010.
24. Gao BX, Ziskind-Conhaim L. Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J Neurophysiol 80: 3047–3061, 1998.
25. Gosgnach S, Lanuza GM, Butt SJ, Saueressig H, Zhang Y, Velasquez T, Riethmacher D, Callaway EM, Kiehn O, Goulding M. V1 spinal neurons regulate the speed of vertebrate locomotor outputs. Nature 440: 215–219, 2006.
26. Goulding M. Circuits controlling vertebrate locomotion: moving in a new direction. Nat Rev Neurosci 10: 507–518, 2009.
27. Goulding M, Pfaff SL. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr Opin Neurobiol 15: 14–20, 2005.
28. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4: 573–586, 2003.
29. Grossmann KS, Giraudin A, Britz O, Zhang J, Goulding M. Genetic dissection of rhythmic motor networks in mice. Prog Brain Res 187: 19–37, 2010.
30. Guertin PA. The mammalian central pattern generator for locomotion. Brain Res Rev 62: 45–56, 2009.
31. Harris-Warrick RM. Voltage-sensitive ion channels in rhythmic motor systems. Curr Opin Neurobiol 12: 646–651, 2002.
32. Husch A, Cramer N, Harris-Warrick RM. Long-duration perforated patch recordings from spinal interneurons of adult mice. J Neurophysiol 106: 2783–2789, 2011.
33. Husch A, Van Patten GN, Hong DN, Scaperotti MM, Cramer N, Harris- Warrick RM. Spinal cord injury induces serotonin supersensitivity without increasing intrinsic excitability of mouse V2a interneurons. J Neurosci 32: 13145–13154, 2012.
34. Jiang Z, Rempel J, Li J, Sawchuk MA, Carlin KP, Brownstone RM. Development of L-type calcium channels and a nifedipine-sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci 11: 3481–3487, 1999.
35. Kiehn O. Development and functional organization of spinal locomotor circuits. Curr Opin Neurobiol 21: 100–109, 2011.
36. Kiehn O. Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29: 279–306, 2006.
37. Kimura Y, Satou C, Fujioka S, Shoji W, Umeda K, Ishizuka T, Yawo H, Higashijima S. Hindbrain V2a neurons in the excitation of spinal locomotor circuits during zebrafish swimming. Curr Biol 23: 843–849, 2013.
38. Kudo N, Yamada T. N-methyl-D,L-aspartate-induced locomotor activity in a spinal cord-hindlimb muscles preparation of the newborn rat studied in vitro. Neurosci Lett 75: 43–48, 1987.
39. Lamas JA, Romero M, Reboreda A, Sanchez E, Ribeiro SJ. A riluzole- and valproate-sensitive persistent sodium current contributes to the resting membrane potential and increases the excitability of sympathetic neurones. Pflügers Arch 458: 589–599, 2009.
40. Landry ES, Lapointe NP, Rouillard C, Levesque D, Hedlund PB, Guertin PA. Contribution of spinal 5-HT1Aand 5-HT7receptors to locomotor-like movement induced by 8-OH-DPAT in spinal cord-transected mice. Eur J Neurosci 24: 535–546, 2006.
41. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42: 375–386, 2004. Liu IS, Chen JD, Ploder L, Vidgen D, van der Kooy D, Kalnins VI, McInnes RR. Developmental expression of a novel murine homeobox gene (Chx10): evidence for roles in determination of the neuroretina and inner nuclear layer. Neuron 13: 377–393, 1994.
42. Liu J, Akay T, Hedlund PB, Pearson KG, Jordan LM. Spinal 5-HT7 receptors are critical for alternating activity during locomotion: in vitro neonatal and in vivo adult studies using 5-HT7 receptor knockout mice. J Neurophysiol 102: 337–348, 2009.
43. Ljunggren EE, Haupt S, Ausborn J, Ampatzis K, El Manira A. Optogenetic activation of excitatory premotor interneurons is sufficient to generate coordinated locomotor activity in larval zebrafish. J Neurosci 34: 134–139, 2014.
44. Lowrie MB, Lawson SJ. Cell death of spinal interneurones. Prog Neurobiol 61: 543–555, 2000.
45. Lundfald L, Restrepo CE, Butt SJ, Peng CY, Droho S, Endo T, Zeilhofer HU, Sharma K, Kiehn O. 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, 2007. MacLean JN, Cowley KC, Schmidt BJ. NMDA receptor-mediated oscillatory activity in the neonatal rat spinal cord is serotonin dependent. J Neurophysiol 79: 2804–2808, 1998. Madriaga MA. Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92: 1566–1576, 2004.
46. Marder E, Bucher D. Central pattern generators and the control of rhythmic movements. Curr Biol 11: R986–996, 2001.
47. McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 11: 1419–1429, 2008.
48. Musienko P, van den Brand R, Marzendorfer O, Roy RR, Gerasimenko Y, Edgerton VR, Courtine G. Controlling specific locomotor behaviors through multidimensional monoaminergic modulation of spinal circuitries. J Neurosci 31: 9264–9278, 2011.
49. Neter J, Kutner MH, Nachtsheim CJ, Wasserman W. Applied Linear Regression Models. New York: McGraw-Hill, 1996.
50. Pearlstein E, Ben Mabrouk F, Pflieger JF, Vinay L. Serotonin refines the locomotor-related alternations in the in vitro neonatal rat spinal cord. Eur J Neurosci 21: 1338–1346, 2005.
51. Rae J, Cooper K, Gates P, Watsky M. Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37: 15–26, 1991.
52. Rajaofetra N, Sandillon F, Geffard M, Privat A. Pre- and post-natal ontogeny of serotonergic projections to the rat spinal cord. J Neurosci Res 22: 305–321, 1989.
53. Schmidt BJ, Jordan LM. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53: 689–710, 2000. Sherrington CS. Flexion-reflex of the limb, crossed extension-reflex, and reflex stepping and standing. J Physiol 40: 28–121, 1910.
54. Slawinska U, Majczynski H, Dai Y, Jordan LM. The upright posture improves plantar stepping and alters responses to serotonergic drugs in spinal rats. J Physiol 590: 1721–1736, 2012.
55. Spitzer NC, Lamborghini JE. The development of the action potential mechanism of amphibian neurons isolated in culture. Proc Natl Acad Sci USA 73: 1641–1645, 1976.
56. Talpalar AE, Bouvier J, Borgius L, Fortin G, Pierani A, Kiehn O. Dual-mode operation of neuronal networks involved in left-right alternation. Nature 500: 85–88, 2013.
57. Vallstedt A, Kullander K. Dorsally derived spinal interneurons in locomotor circuits. Ann NY Acad Sci 1279: 32–42, 2013.
58. White SR, Fung SJ. Serotonin depolarizes cat spinal motoneurons in situ and decreases motoneuron afterhyperpolarizing potentials. Brain Res502: 205– 213, 1989.
59. Ye JH, Zhang J, Xiao C, Kong JQ. Patch-clamp studies in the CNS illustrate a simple new method for obtaining viable neurons in rat brain slices: glycerol replacement of NaCl protects CNS neurons. J Neurosci Methods 158: 251–259, 2006.
60. Zhong G, Diaz-Rios M, Harris-Warrick RM. Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse. J Neurosci 26: 6509–6517, 2006a.
61. Zhong G, Droho S, Crone SA, Dietz S, Kwan AC, Webb WW, Sharma K, Harris-Warrick RM. Electrophysiological characterization of V2a interneurons and their locomotor-related activity in the neonatal mouse spinal cord. J Neurosci 30: 170–182, 2010.
62. Zhong G, Masino MA, Harris-Warrick RM. Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27: 4507–4518, 2007.
63. Zhong G, Sharma K, Harris-Warrick RM. Frequency-dependent recruitment of V2a interneurons during fictive locomotion in the mouse spinal cord. Nat Commun 2: 274, 2011.
64. Zhong G, Shevtsova NA, Rybak IA, Harris-Warrick RM. Neuronal activity in the isolated mouse spinal cord during spontaneous deletions in fictive locomotion: insights into locomotor central pattern generator organization. J Physiol 590: 4735–4759, 2012.
65. Zhong GS, Dias-Rios M, Harris-Warrick RM. Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord. J Neurophysiol 95: 1545–1555, 2006b.