Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse

Journal of Neuroscience

Volumn 26, Issue 24, 2006, Pages 6509-6517

  Zhong, Guisheng ^a   Díaz Ríos, Manuel ^a   Harris Warrick, Ronald M ^a  

^a Department of Molecular Biology and Genetics   (United States)

Author keywords

Commissural interneuron; Locomotion; Mouse; NMDA; Serotonin; Spinal cord

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; SEROTONIN; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; N METHYLASPARTIC ACID;

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITABILITY; HYPERPOLARIZATION; INTERNEURON; LOCOMOTION; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEROTONINERGIC SYSTEM; SPINAL CORD; SYNAPTIC TRANSMISSION; ANIMAL; ANIMAL BEHAVIOR; CELL MEMBRANE POTENTIAL; CLASSIFICATION; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; IN VITRO STUDY; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; METHODOLOGY; NEWBORN; PATCH CLAMP; PERIODICITY; PHYSIOLOGY; RADIATION RESPONSE;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; INTERNEURONS; LOCOMOTION; MEMBRANE POTENTIALS; MICE; MICE, INBRED ICR; N-METHYLASPARTATE; PATCH-CLAMP TECHNIQUES; PERIODICITY; SEROTONIN; SPINAL CORD;

EID: 33745766714     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1410-06.2006     Document Type: Article

References (53)

1. Angstadt JD, Calabrese RL (1989) A hyperpolarization-activated inward current in heart interneurons of the medicinal leech. J Neurosci 9:2846-2857.
2. Bannatyne BA, Edgley SA, Hammar I, Jankowska E, Maxwell DJ (2003) Networks of inhibitory and excitatory commissural interneurons mediating crossed reticulospinal actions. Eur J Neurosci 18:2273-2284.
3. Berkowitz A, Stein PSG (1994) Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: phase analyses. J Neurosci 14:5105-5119.
4. Birinyi A, Viszokay K, Weber I, Kiehn O, Antal M (2003) Synaptic targets of commissural interneurons in the lumbar spinal cord of neonatal rats. J Comp Neurol 461:429-440.
5. Bonnot A, Morin D (1998) Hemisegmental localisation of rhythmic networks in the lumbosacral spinal cord of neonate mouse. Brain Res 793:136-148.
6. Branchereau P, Morin D, Bonnot A, Ballion B, Chapron J, Viala D (2000) Development of lumbar rhythmic networks: from embryonic to neonate locomotor-like patterns in the mouse. Brain Res Bull 53: 711-718.
7. Brustein E, Chong M, Holmqvist B, Drapeau P (2003) Serotonin patterns locomotor network activity in the developing zebrafish by modulating quiescent periods. J Neurobiol 57:303-322.
8. Buchanan JT (1999) Commissural interneurons in rhythmic generation and intersegmental coupling in the lamprey spinal cord. J Neurophysiol 81:2037-2045.
9. Buchanan JT, McPherson DR (1995) The neuronal network for locomotion in the lamprey spinal cord: evidence for the involvement of commissural interneurons. J Physiol (Paris) 89:221-234.
10. Butt SJ, Kiehn O (2003) Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:953-963.
11. Butt SJ, Harris-Warrick RM, Kiehn O (2002) Firing properties of identified interneuron population in the mammalian hindlimb central pattern generator. J Neurosci 22:9961-9971.
12. Carlin KP, Dai Y, Jordan LM (2006) Cholinergic and serotonergic excitation of ascending commissural neurons in the thoraco-lumbar spinal cord of the neonatal mouse. J Neurophysiol 95:1278-1284.
13. Cazalets JR, Squalli-Houssaini Y, Clarac F (1992) Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol (Lond) 455:187-204.
14. Cazalets JR, Borde M, Clarac F (1995) Localization and organization of the central pattern generator for hindlimb locomotion in newborn rat. J Neurosci 15:4943-4951.
15. Christie KJ, Whelan PJ (2005) Monoaminergic establishment of rostrocaudal gradients of rhythmicity in the neonatal mouse spinal cord. J Neurophysiol 94:1554-1564.
16. Cowley KC, Schmidt BJ (1997) Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J Neurophysiol 77:247-259.
17. Eide AL, Glover J, Kjaerulff O, Kiehn O (1999) Characterization of commissural interneurons in the lumbar region of the neonatal rat spinal cord. J Comp Neurol 403:332-345.
18. Fedirchuk B, Dai Y (2004) Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J Physiol (Lond) 557:355-361.
19. Flamm RE, Harris-Warrick RM (1986a) Aminergic modulation in lobster stomatogastric ganglion. I. Effects on motor pattern and activity of neurons within the pyloric circuit. J Neurophysiol 55:847-865.
20. Flamm RE, Harris-Warrick RM (1986b) Aminergic modulation in lobster stomatogastric ganglion. II. Target neurons of dopamine, octopamine, and serotonin within the pyloric circuit. J Neurophysiol 55:866-881.
21. Gilmore J, Fedirchuk B (2004) The excitability of lumbar motoneurones in the neonatal rat is increased by a hyperpolarization of their voltage threshold for activation by descending serotonergic fibres. J Physiol (Lond) 558:213-224.
22. Golowasch J, Marder E (1992) Ionic current of the lateral pyloric neuron of the stomatogastric ganglion of the crab. J Neurophysiol 67:318-331.
23. Grillner S (2003) The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4:573-586.
24. Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14:39-57.
25. Kiehn O, Kjaerulff O (1998) Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 860:110-129.
26. 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.
27. 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.
28. 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.
29. Liu J, Jordan LM (2005) Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. J Neurophysiol 94:1392-1404.
30. h. J Neurophysiol 79:3284-3289.
31. MacLean JN, Cowley KC, Schmidt BJ (1998) NMDA receptor-mediated oscillatory activity in the neonatal rat spinal cord is serotonin dependent. J Neurophysiol 79:2804-2808.
32. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ (2004) Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92:1566-1576.
33. Matsuyama K, Nakajima K, Mori F, Aoki M, Mori S (2004) Lumbar commissural interneurons with reticulospinal inputs in the cat: morphology and discharge patterns during fictive locomotion. J Comp Neurol 474:546-561.
34. McCormick DA, Pape HC (1990) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurons. J Physiol (Lond) 431:291-318.
35. McLean DL, Merrywest SD, Sillar KT (2000) The development of neuromodulatory systems and the maturation of motor patterns in amphibian tadpoles. Brain Res Bull 53:595-603.
36. Nakayama K, Nishimaru H, Kudo N (2002) Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22:10388-10398.
37. Nissen UV, Mochida H, Glover JC (2005) Development of projection-specific interneurons and projection neurons in the embryonic mouse and rat spinal cord. J Comp Neurol 483:30-47.
38. Pearlstein E, Ben Mabrouk F, Pflieger JF, Vinay L (2005) Serotonin refines the locomotor related alternations in the in vitro neonatal rat spinal cord. Eur J Neurosci 21:1338-1346.
39. 2+ channels. J Neurophysiol 93:2507-2519.
40. Quinlan KA, Kiehn O (2005) Synaptic effects of intrasegmental commissural interneurons in the mouse spinal cord. Soc Neurosci Abstr 31:516.1.
41. Shefchyk SJ, Jordan LM (1985) Motoneuron input-resistance changes during fictive locomotion produced by stimulation of the mesencephalic locomotor region. J Neurophysiol 54:1101-1108.
42. Soffe SR, Clarke JD, Roberts A (1984) Activity of commissural interneurons in spinal cord of Xenopus embryos. J Neurophysiol 51:1257-1267.
43. Sourdet V, Russier M, Daoudal G, Ankri N, Debanne D (2003) Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci 23:10238-10248.
44. Stokke MF, Nissen UV, Glover JC, Kiehn O (2002) Projection patterns of commissural interneurons in the lumbar spinal cord of the neonatal rat. J Comp Neurol 446:349-359.
45. Swensen AM, Marder E (2000) Multiple peptides converge to activate the same voltage-dependent current in a central pattern-generating circuit. J Neurosci 20:6752-6759.
46. Swensen AM, Marder E (2001) Modulators with convergent cellular actions elicit distinct circuit outputs. J Neurosci 21:4050-4058.
47. Taccola G, Marchetti C, Nistri A (2003) Effect of metabotropic glutamate receptor activity on rhythmic discharges of the neonatal rat spinal cord in vitro. Exp Brain Res 153:388-393.
48. Taccola G, Marchetti C, Nistri A (2004) Modulation of rhythmic patterns and cumulative depolarization by group I metabotropic glutamate receptors in the neonatal rat spinal cord in vitro. Eur J Neurosci 19:533-541.
49. Thoby-Brisson M, Telgkamp P, Ramirez JM (2000) The role of the hyperpolarization-activated current in modulating rhythmic activity in the isolated respiratory network of mice. J Neurosci 20:2994-3005.
50. Wallen P, Buchanan JT, Grillner S, Hill RH, Christenson J, Hokfelt T (1989) Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. J Neurophysiol 61:759-768.
51. Zar JH (2000) Biostatistical analysis. Englewood Cliffs, NJ: Prentice-Hall.
52. Zhang W, Grillner S (2000) The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey. Brain Res 879:188-192.
53. Zhong G, Diaz-Rios M, Harris-Warrick RM (2006) Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord. J Neurophysiol 95:1545-1555.