Spike Timing-Dependent Serotonergic Neuromodulation of Synaptic Strength Intrinsic to a Central Pattern Generator Circuit

Journal of Neuroscience

Volumn 23, Issue 34, 2003, Pages 10745-10755

  Sakurai, Akira ^a   Katz, Paul S ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Bidirectional; Biphasic; Facilitation; Motor pattern; Opisthobranch mollusk; Serotonin; Synaptic depression

Indexed keywords

METHYSERGIDE; SEROTONIN; SEROTONIN ANTAGONIST;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FACILITATION; INTERNEURON; MOLLUSC; MOTOR ACTIVITY; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PATTERN GENERATOR; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL; SPIKE; SYNAPSE; SYNAPTIC POTENTIAL; TRITONIA SEA SLUG;

EID: 0344198019     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-34-10745.2003     Document Type: Article

References (56)

1. Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci [Suppl] 3:1178-1183.
2. + currents. J Neurosci 13:5139-5152.
3. Bennett MR (2000) The concept of long term potentiation of transmission at synapses. Prog Neurobiol 60:109-137.
4. Bi GQ, Poo MM (2001) Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24:139-166.
5. Bocchiaro CM, Saywell SA, Feldman JL (2003) Dynamic modulation of inspiratory drive currents by protein kinase A and protein phosphatases in functionally active motoneurons. J Neurosci 23:1099-1103.
6. Burrell BD, Sahley CL, Muller KJ (2001) Non-associative learning and serotonin induce similar bi-directional changes in excitability of a neuron critical for learning in the medicinal leech. J Neurosci 21:1401-1412.
7. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
8. A receptor channels by the 5-HT4 receptor-mediated signalling in rat prefrontal cortical pyramidal neurons. J Physiol (Lond) 540:743-759.
9. Calabrese RL (1998) Cellular, synaptic, network, and modulatory mechanisms involved in rhythm generation. Curr Opin Neurobiol 8:710-717.
10. Clemens S, Katz PS (2001) Identified serotonergic neurons in the Tritonia swim CPG activate both ionotropic and metabotropic receptors. J Neurophysiol 85:476-479.
11. Clemens S, Katz PS (2003) G Protein signaling in a neuronal network is necessary for rhythmic motor pattern production. J Neurophysiol 89:762-772.
12. Daniel H, Levenes C, Crépel F (1998) Cellular mechanisms of cerebellar LTD. Trends Neurosci 21:401-407.
13. Fickbohm DJ, Katz PS (2000) Paradoxical actions of the serotonin precursor 5-hydroxytryptophan on the activity of identified serotonergic neurons in a simple motor circuit. J Neurosci 20:1622-1634.
14. Froemke RC, Dan Y (2002) Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416:433-438.
15. Frost WN, Katz PS (1996) Single neuron control over a complex motor program. Proc Natl Acad Sci USA 93:422-426.
16. Frost WN, Hoppe TA, Wang J, Tian LM (2001) Swim initiation neurons in Tritonia diomedea. Am Zool 41:952-961.
17. Getting PA (1981) Mechanisms of pattern generation underlying swimming in Tritonia. I. Neuronal network formed by monosynaptic connections. J Neurophysiol 46:65-79.
18. Getting PA (1983) Mechanisms of pattern generation underlying swimming in Tritonia. III. Intrinsic and synaptic mechanisms for delayed excitation. J Neurophysiol 49:1036-1050.
19. Getting PA (1989) A network oscillator underlying swimming in Tritonia. In: Neuronal and cellular oscillators (Jacklet JW, ed), pp 215-236. New York: Marcel Dekker.
20. Getting PA, Lennard PR, Hume RI (1980) Central pattern generator mediating swimming in Tritonia. I. Identification and synaptic interactions. J Neurophysiol 44:151-164.
21. Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815-835.
22. Hammer M (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci 20:245-252.
23. Hasselmo ME, Linster C (1999) Neuromodulation and memory function. In: Beyond neurotransmission: neuromodulation and its importance for information processing (Katz PS, ed), pp 318-348. Oxford: Oxford UP.
24. Hume RI, Getting PA (1982a) Motor organization of Tritonia swimming. II. Synaptic drive to flexion neurons from premotor interneurons. J Neurophysiol 47:75-90.
25. Hume RI, Getting PA (1982b) Motor organization of Tritonia swimming. III. Contribution of intrinsic membrane properties to flexion neuron burst formation. J Neurophysiol 47:91-102.
26. Katz PS (1999) Beyond neurotransmission: neuromodulation and its importance for information processing. Oxford: Oxford UP.
27. Katz PS, Frost WN (1995a) Intrinsic neuromodulation in the Tritonia swim CPG: serotonin mediates both neuromodulation and neurotransmission by the dorsal swim interneurons. J Neurophysiol 74:2281-2294.
28. Katz PS, Frost WN (1995b) Intrinsic neuromodulation in the Tritonia swim CPG: the serotonergic dorsal swim interneurons act presynaptically to enhance transmitter release from interneuron C2. J Neurosci 15:6035-6045.
29. Katz PS, Frost WN (1997) Removal of spike frequency adaptation via neuromodulation intrinsic to the Tritonia escape swim central pattern generator. J Neurosci 17:7703-7713.
30. Katz PS, Getting PA, Frost WN (1994) Dynamic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. Nature 367:729-731.
31. Kiehn O, Katz PS (1999) Making circuits dance: neuromodulation of motor systems. In: Beyond neurotransmission: neuromodulation and its importance for information processing (Katz PS, ed), pp 275-317. Oxford: Oxford UP.
32. Lynn-Bullock CP, Clemens S, Sakurai A, Katz PS (2002) Functional anatomy of the escape swim CPG in Tritonia. Soc Neurosci Abstr 28:67.25.
33. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
34. Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986-R996.
35. Marder E, Calabrese RL (1996) Principles of rhythmic motor pattern generation. Physiol Rev 76:687-717.
36. Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213-215.
37. Mauelshagen J, Sherff CM, Carew TJ (1998) Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. Learn Mem 5:246-256.
38. McClellan AD, Brown GD, Getting PA (1994) Modulation of swimming in Tritonia: excitatory and inhibitory effects of serotonin. J Comp Physiol [A] 174:257-266.
39. Mercer AR (1999) Changing the way we perceive things: sensory systems modulation. In: Beyond neurotransmission: neuromodulation and its importance for information processing (Katz PS, ed), pp 198-240. Oxford: Oxford UP.
40. Mercer AR, Emptage NJ, Carew TJ (1991) Pharmacological dissociation of modulatory effects of serotonin in Aplysia sensory neurons. Science 254:1811-1813.
41. Nagai T, Kim DJ, Delay RJ, Roper SD (1996) Neuromodulation of transduction and signal processing in the end organs of taste. Chem Senses 21:353-365.
42. Pasztor VM (1989) Modulation of sensitivity in invertebrate sensory receptors. Semin Neurosci 1:5-14.
43. Pearson KG (1993) Common principles of motor control in vertebrates and invertebrates. Annu Rev Neurosci 16:265-297.
44. Popescu IR, Frost WN (2002) Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22:1985-1993.
45. Powis, DA and Bunn, SJ (eds) (1995) Neurotransmitter release and its modulation: biochemical mechanisms, physiological function and clinical relevance. Cambridge, UK: Cambridge UP.
46. Quinlan EM, Halpain S (1996) Postsynaptic mechanisms for bidirectional control of MAP2 phosphorylation by glutamate receptors. Neuron 16:357-368.
47. Sakurai A, Katz PS (2002) Serotonergic interneurons in Tritonia evoke a biphasic neuromodulatory action. Soc Neurosci Abstr 28:270.13.
48. Seamans JK, Gorelova N, Durstewitz D, Yang CR (2001) Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21:3628-3638.
49. Shimahara T, Tauc L (1975) Multiple interneuronal effects to the giant cells in Aplysia. J Physiol (Lond) 247:299-319.
50. Sjöström PJ, Nelson SB (2002) Spike timing, calcium signals and synaptic plasticity. Curr Opin Neurobiol 12:305-314.
51. Skydsgaard M, Hounsgaard J (1996) Multiple actions of iontophoretically applied serotonin on motorneurones in the turtle spinal cord in vitro. Acta Physiol Scand 158:301-310.
52. Sutton MA, Carew TJ (2000) Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia. Neuron 26:219-231.
53. Taghert PH, Willows AOD (1978) Control of a fixed action pattern by single, central neurons in the marine mollusk, Tritonia diomedea. J Comp Physiol 123:253-259.
54. Teshiba T, Shamsian A, Yashar B, Yeh SR, Edwards DH, Krasne FB (2001) Dual and opposing modulatory effects of serotonin on crayfish lateral giant escape command neurons. J Neurosci 21:4523-4529.
55. Willows AOD, Dorsett DA, Hoyle G (1973) The neuronal basis of behavior in Tritonia. I. Functional organization of the central nervous system. J Neurobiol 4:207-237.
56. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.