State-, timing-, and pattern-dependent neuromodulation of synaptic strength by a serotonergic interneuron

Journal of Neuroscience

Volumn 29, Issue 1, 2009, Pages 268-279

  Sakurai, Akira ^a   Katz, Paul S ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Central pattern generator; Depression; Mollusc; Posttetanic; Potentiation; Presynaptic facilitation; Presynaptic mechanisms; Serotonin; Synaptic plasticity; Synaptic transmission

Indexed keywords

SEROTONIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOLLUSC; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SEROTONINERGIC NERVE CELL;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; BRAIN; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; LONG-TERM POTENTIATION; SEROTONIN; SYNAPSES; TIME FACTORS; TRITONIA SEA SLUG;

EID: 58149381560     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4456-08.2009     Document Type: Article

References (54)

1. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
2. Abraham WC, Mason-Parker SE, Bear MF, Webb S, Tate WP (2001) Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP. Proc Natl Acad Sci U S A 98:10924-10929.
3. Atwood HL, Wojtowicz JM (1999) Silent synapses in neural plasticity: current evidence. Learn Mem 6:542-571.
4. Billimoria CP, DiCaprio RA, Birmingham JT, Abbott LF, Marder E (2006) Neuromodulation of spike-timing precision in sensory neurons. J Neurosci 26:5910-5919.
5. Briggman KL, Kristan WB (2008) Multifunctional pattern-generating circuits. Annu Rev Neurosci 31:271-294.
6. Bristol AS, Fischer TM, Carew TJ (2001) Combined effects of intrinsic facilitation and modulatory inhibition of identified interneurons in the siphon withdrawal circuitry of Aplysia. J Neurosci 21:8990-9000.
7. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
8. 4 receptor-mediated signalling in rat prefrontal cortical pyramidal neurons. J Physiol 540:743-759.
9. Calabrese RL (1998) Cellular, synaptic, network, and modulatory mechanisms involved in rhythm generation. Curr Opin Neurobiol 8:710-717.
10. Chen YL, Huang CC, Hsu KS (2001) Time-dependent reversal of long-term potentiation by low-frequency stimulation at the hippocampal mossy fiber-CA3 synapses. J Neurosci 21:3705-3714.
11. Doyère V, Srebro B, Laroche S (1997) Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. J Neurophysiol 77:571-578.
12. Froemke RC, Merzenich MM, Schreiner CE (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450:425-429.
13. Getting PA (1981) Mechanisms of pattern generation underlying swimming in Tritonia. I. Neuronal network formed by monosynaptic connections. J Neurophysiol 46:65-79.
14. Getting PA (1983) Mechanisms of pattern generation underlying swimming in Tritonia. III. Intrinsic and synaptic mechanisms for delayed excitation. J Neurophysiol 49:1036-1050.
15. Getting PA, Lennard PR, Hume RI (1980) Central pattern generator mediating swimming in Tritonia. I. Identification and synaptic interactions. J Neurophysiol 44:151-164.
16. Giocomo LM, Hasselmo ME (2007) Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Mol Neurobiol 36:184-200.
17. Goldsmith BA, Abrams TW (1991) Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylyl cyclase. Proc Natl Acad Sci U S A 88:9021-9025.
18. 4 receptors in prefrontal cortex. Mol Pharmacol 66:948-955.
19. Habets RLP, Borst JG (2007) Dynamics of the readily releasable pool during post-tetanic potentiation in the rat calyx of Held synapse. J Physiol 581:467-478.
20. Huang CC, Hsu KS (2001) Progress in understanding the factors regulating reversibility of long-term potentiation. Rev Neurosci 12:51-68.
21. Huang CC, Liang YC, Hsu KS (1999) A role for extracellular adenosine in time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses. J Neurosci 19:9728-9738.
22. Huang CC, Liang YC, Hsu KS (2001) Characterization of the mechanism underlying the reversal of long term potentiation by low frequency stimulation at hippocampal CA1 synapses. J Biol Chem 276:48108-48117.
23. Huang CC, Chen YL, Liang YC, Hsu KS (2002) Role for cAMP and protein phosphatase in the presynaptic expression of mouse hippocampal mossy fibre depotentiation. J Physiol 543:767-778.
24. Huang Y, Yasuda H, Sarihi A, Tsumoto T (2008) Roles of endocannabinoids in heterosynaptic long-term depression of excitatory synaptic transmission in visual cortex of young mice. J Neurosci 28:7074-7083.
25. Hume RI, Getting PA (1982) Motor organization of Tritonia swimming. II. Synaptic drive to flexion neurons from premotor interneurons. J Neurophysiol 47:75-90.
26. Jiang XY, Abrams TW (1998) Use-dependent decline of paired-pulse facilitation at Aplysia sensory neuron synapses suggests a distinct vesicle pool or release mechanism. J Neurosci 18:10310-10319.
27. Katz PS (1999) Beyond neurotransmission: neuromodulation and its importance for information processing. Oxford: Oxford UP.
28. Katz PS, Frost WN (1995) 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. Koh HY, Weiss KR (2005) Peptidergic contribution to posttetanic potentiation at a central synapse of Aplysia. J Neurophysiol 94:1281-1286.
30. 4 receptors of long-term potentiation and depotentiation in the dentate gyrus of freely moving rats. Cereb Cortex 12:150-162.
31. Kulla A, Manahan-Vaughan D (2008) Modulation by group 1 metabotropic glutamate receptors of depotentiation in the dentate gyrus of freely moving rats. Hippocampus 18:48-54.
32. Kulla A, Reymann KG, Manahan-Vaughan D (1999) Time-dependent induction of depotentiation in the dentate gyrus of freely moving rats: involvement of group 2 metabotropic glutamate receptors. Eur J Neurosci 11:3864-3872.
33. Levy WB, Steward O (1979) Synapses as associative memory elements in the hippocampal formation. Brain Res 175:233-245.
34. 2-like receptors. Cereb Cortex 13:123-135.
35. 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.
36. Mongillo G, Barak O, Tsodyks M (2008) Synaptic theory of working memory. Science 319:1543-1546.
37. Nagai T, Kim DJ, Roper SD (1996) Neuromodulation of transduction and signal processing in the end organs of taste. Chem Senses 21:353-365.
38. Philpot BD, Bear MF, Abraham WC (1999) Metaplasticity: The plasticity of synaptic plasticity. In: Beyond neurotransmission: neuromodulation and its importance for information processing (Katz PS, ed), pp 160-197. Oxford: Oxford UP.
39. Philpot BD, Cho KK, Bear MF (2007) Obligatory role of NR2A for metaplasticity in visual cortex. Neuron 53:495-502.
40. Poncer JC (2003) Hippocampal long term potentiation: silent synapses and beyond. J Physiol Paris 97:415-422.
41. Popescu IR, Frost WN (2002) Highly dissimilar behaviors mediated by a multifunctional network in the marine mollusk Tritonia diomedea. J Neurosci 22:1985-1993.
42. Qian SM, Delaney KR (1997) Neuromodulation of activity-dependent synaptic enhancement at crayfish neuromuscular junction. Brain Res 771:259-270.
43. Reid CA, Dixon DB, Takahashi M, Bliss TV, Fine A (2004) Optical quantal analysis indicates that long-term potentiation at single hippocampal mossy fiber synapses is expressed through increased release probability, recruitment of new release sites, and activation of silent synapses. J Neurosci 24:3618-3626.
44. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS (2002) Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33:411-424.
45. Sakurai A, Katz PS (2003) Spike timing-dependent serotonergic neuromodulation of synaptic strength intrinsic to a central pattern generator circuit. J Neurosci 23:10745-10755.
46. Sakurai A, Darghouth NR, Butera RJ, Katz PS (2006) Serotonergic enhancement of a 4-AP-sensitive current mediates the synaptic depression phase of spike timing-dependent neuromodulation. J Neurosci 26:2010-2021.
47. Sakurai A, Calin-Jageman RJ, Katz PS (2007) Potentiation phase of spike timing-dependent neuromodulation by a serotonergic interneuron involves an increase in the fraction of transmitter release. J Neurophysiol 98:1975-1987.
48. Sanchez JA, Kirk MD (2000) Short-term synaptic enhancement modulates ingestion motor programs of Aplysia. J Neurosci 20:RC85.
49. Schneggenburger R, Forsythe ID (2006) The calyx of Held. Cell Tissue Res 326:311-337.
50. Seol GH, Ziburkus J, Huang S, Song L, Kim IT, Takamiya K, Huganir RL, Lee HK, Kirkwood A (2007) Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55:919-929.
51. Willows AO, 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.
52. Zhao Y, Klein M (2004) Changes in the readily releasable pool of transmitter and in efficacy of release induced by high-frequency firing at Aplysia sensorimotor synapses in culture. J Neurophysiol 91:1500-1509.
53. Zho WM, You JL, Huang CC, Hsu KS (2002) The group I metabotropic glutamate receptor agonist (S)-3,5-dihydroxyphenylglycine induces a novel form of depotentiation in the CA1 region of the hippocampus. J Neurosci 22:8838-8849.
54. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.