Serotonergic modulation of locomotion in zebrafish - Endogenous release and synaptic mechanisms

Journal of Neuroscience

Volumn 29, Issue 33, 2009, Pages 10387-10395

  Gabriel, Jens Peter ^a   Mahmood, Riyadh ^a   Kyriakatos, Alexandros ^a   Söll, Iris ^a,b   Hauptmann, Giselbert ^a,b   Calabrese, Ronald L ^c   El Manira, Abdeljabbar ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b School of Life Sciences Södertörn University   (Sweden)

^c EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITALOPRAM; GLYCINE; N METHYL DEXTRO ASPARTIC ACID; SEROTONIN; SEROTONIN UPTAKE INHIBITOR;

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; HYPERPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; LOCOMOTION; NERVE FIBER MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RHYTHM; SEROTONINERGIC SYSTEM; SPINAL CORD NERVE CELL; SYNAPTIC TRANSMISSION; ZEBRA FISH;

ANIMALS; MOTOR ACTIVITY; SEROTONIN; SYNAPSES; ZEBRAFISH;

EID: 69049085614     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1978-09.2009     Document Type: Article

References (44)

1. Beato M, Nistri A (1998) Serotonin-induced inhibition of locomotor rhythm of the rat isolated spinal cord is mediated by the 5-HT1 receptor class. Proc Biol Sci 265:2073-2080.
2. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390-393.
3. Biró Z, Hill RH, Grillner S (2006) 5-HT Modulation of identified segmental premotor interneurons in the lamprey spinal cord. J Neurophysiol 96:931-935.
4. Bracci E, Beato M, Nistri A (1998) Extracellular K+ induces locomotor-like patterns in the rat spinal cord in vitro: comparison with NMDA or 5-HT induced activity. J Neurophysiol 79:2643-2652.
5. Brustein E, Drapeau P (2005) Serotoninergic modulation of chloride homeostasis during maturation of the locomotor network in zebrafish. J Neurosci 25:10607-10616.
6. 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.
7. Cazalets JR, Sqalli-Houssaini Y, Clarac F (1992) Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol 455:187-204.
8. Cohen AH, Harris-Warrick RM (1984) Strychnine eliminates alternating motor output during fictive locomotion in the lamprey. Brain Res 293:164-167.
9. Dale N (1995) Experimentally derived model for the locomotor pattern generator in the Xenopus embryo. J Physiol 489:489-510.
10. El Manira A, Zhang W, Svensson E, Bussières N (1997) 5-HT inhibits calcium current and synaptic transmission from sensory neurons in lamprey. J Neurosci 17:1786-1794.
11. Endo T, Kiehn O (2008) Asymmetric operation of the locomotor central pattern generator in the neonatal mouse spinal cord. J Neurophysiol 100:3043-3054.
12. Fetcho JR, Higashijima S, McLean DL (2008) Zebrafish and motor control over the last decade. Brain Res Rev 57:86-93.
13. Fuller RW, Wong DT (1990) Serotonin uptake and serotonin uptake inhibition. Ann N Y Acad Sci 600:68-78.
14. Gabriel JP, Mahmood R, Walter AM, Kyriakatos A, Hauptmann G, Calabrese RL, El Manira A (2008) Locomotor pattern in the adult zebrafish spinal cord in vitro. J Neurophysiol 99:37-48.
15. Grillner S, Wallén P (1980) Does the central pattern generation for locomotion in lamprey depend on glycine inhibition? Acta Physiol Scand 110:103-105.
16. Hellgren J, Grillner S, Lansner A (1992) Computer simulation of the segmental neural network generating locomotion in lamprey by using populations of network interneurons. Biol Cybern 68:1-13.
17. 2+-channel and BK-channel expression in embryos and larvae of Xenopus laevis. Eur J Neurosci 18:2175-2187.
18. Kaslin J, Panula P (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). J Comp Neurol 440:342-377.
19. Kiehn O, Kjaerulff O (1996) Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol 75:1472-1482.
20. Kjaerulff O, Kiehn O (2001) 5-HT modulation of multiple inward rectifiers in motoneurons in intact preparations of the neonatal rat spinal cord. J Neurophysiol 85:580-593.
21. 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.
22. Liu J, Akay T, Hedlund PB, Pearson KG, Jordan LM (2009) 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.
23. MacLean JN, Cowley KC, Schmidt BJ (1998) NMDAreceptor-mediated oscillatory activity in the neonatal rat spinal cord is serotonin dependent. J Neurophysiol 79:2804-2808.
24. 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.
25. Masino MA, Fetcho JR (2005) Fictive swimming motor patterns in wild type and mutant larval zebrafish. J Neurophysiol 93:3177-3188.
26. McDearmid JR, Drapeau P (2006) Rhythmic motor activity evoked by NMDA in the spinal zebrafish larva. J Neurophysiol 95:401-417.
27. McDearmid JR, Scrymgeour-Wedderburn JF, Sillar KT (1997) Aminergic modulation of glycine release in a spinal network controlling swimming in Xenopus laevis. J Physiol 503:111-117.
28. McLean DL, Fetcho JR (2004) Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish. J Comp Neurol 480:38-56.
29. 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.
30. Rauscent A, Einum J, Le Ray D, Simmers J, Combes D (2009) Opposing aminergic modulation of distinct spinal locomotor circuits and their functional coupling during amphibian metamorphosis. J Neurosci 29:1163-1174.
31. Russell DF, Wallén P (1983) On the control of myotomal motoneurones during "fictive swimming" in the lamprey spinal cord in vitro. Acta Physiol Scand 117:161-170.
32. Schmidt BJ, Jordan LM (2000) The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53:689-710.
33. Schwartz EJ, Gerachshenko T, Alford S (2005) 5-HT prolongs ventral root bursting via presynaptic inhibition of synaptic activity during fictive locomotion in lamprey. J Neurophysiol 93:980-988.
34. Scrymgeour-Wedderburn JF, Reith CA, Sillar KT (1997) Voltage oscillations in Xenopus spinal cord neurons: developmental onset and dependence on co-activation of NMDA and 5HT receptors. Eur J Neurosci 9:1473-1482.
35. Sillar KT, Wedderburn JF, Simmers AJ (1992) Modulation of swimming rhythmicity by 5-hydroxytryptamine during post-embryonic development in Xenopus laevis. Proc Biol Sci 250:107-114.
36. Sillar KT, Reith CA, McDearmid JR (1998) Development and aminergic neuromodulation of a spinal locomotor network controlling swimming in Xenopus larvae. Ann N Y Acad Sci 860:318-332.
37. Sun Q, Dale N (1998) Developmental changes in expression of ion currents accompany maturation of locomotor pattern in frog tadpoles. J Physiol 507:257-264.
38. Van Raamsdonk W, Bosch TJ, Smit-Onel MJ, Maslam S (1996) Organisation of the zebrafish spinal cord: distribution of motoneuron dendrites and 5-HT containing cells. Eur J Morphol 34:65-77.
39. Wallén P, Christenson J, Brodin L, Hill R, Lansner A, Grillner S (1989a) Mechanisms underlying the serotonergic modulation of the spinal circuitry for locomotion in lamprey. Prog Brain Res 80:321-327.
40. Wallén P, Buchanan JT, Grillner S, Hill RH, Christenson J, Hökfelt T (1989b) Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. J Neurophysiol 61:759-768.
41. Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio), Ed 4. Eugene, OR: University of Oregon.
42. Zhang W, Pombal MA, el Manira A, Grillner S (1996) Rostrocaudal distribution of 5-HT innervation in the lamprey spinal cord and differential effects of 5-HT on fictive locomotion. J Comp Neurol 374:278-290.
43. Zhong G, Díaz-Ríos M, Harris-Warrick RM (2006a) Intrinsic and functional differences among commissural interneurons during fictive locomotion and serotonergic modulation in the neonatal mouse. J Neurosci 26:6509-6517.
44. Zhong G, Díaz-Ríos M, Harris-Warrick RM (2006b) Serotonin modulates the properties of ascending commissural interneurons in the neonatal mouse spinal cord. J Neurophysiol 95:1545-1555.