Desensitization of postsynaptic glutamate receptors contributes to high-frequency homosynaptic depression of Aplysia sensorimotor connections

Learning and Memory

Volumn 10, Issue 5, 2003, Pages 309-313

  Antzoulatos, Evangelos G ^a   Cleary, Leonard J ^a   Eskin, Arnold ^b   Baxter, Douglas A ^a   Byrne, John H ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOTHIAZIDE; GLUTAMATE RECEPTOR; POSTSYNAPTIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APLYSIA; ARTICLE; CONTROLLED STUDY; DEPRESSION; DESENSITIZATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; HABITUATION; LEARNING; LONG TERM POTENTIATION; MEMORY; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SENSORIMOTOR FUNCTION; SYNAPTIC TRANSMISSION; WITHDRAWAL REFLEX;

ANIMALS; APLYSIA; BENZOTHIADIAZINES; DOWN-REGULATION; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM DEPRESSION (PHYSIOLOGY); MOTOR NEURONS; NEURONS, AFFERENT; PRESYNAPTIC TERMINALS; RECEPTORS, AMPA; RECEPTORS, GLUTAMATE; REFLEX; SYNAPTIC TRANSMISSION;

EID: 0142026358     PISSN: 10720502     EISSN: None     Source Type: Journal    
DOI: 10.1101/lm.61403     Document Type: Article

References (52)

1. Antonov, I., Kandel, E.R., and Hawkins, R.D. 1999. The contribution of facilitation of monosynaptic PSPs to dishabituation and sensitization of the Aplysia siphon withdrawal reflex. J. Neurosci. 19: 10438-10450.
2. Antonov, I., Antonova, I., Kandel, E.R., and Hawkins, R.D. 2003. Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37: 135-147.
3. Arai, A. and Lynch, G. 1998a. The waveform of synaptic transmission at hippocampal synapses is not determined by AMPA receptor desensitization. Brain Res. 799: 230-234.
4. -. 1998b. AMPA receptor desensitization modulates synaptic responses induced by repetitive afferent stimulation in hippocampal slices. Brain Res. 799: 235-242.
5. Armitage, B.A. and Siegelbaum, S.A. 1998. Presynaptic induction and expression of homosynaptic depression at Aplysia sensorimotor neuron synapses. J. Neurosci. 18: 8770-8779.
6. Bailey, C.H. and Chen, M. 1983. Morphological basis of long-term habituation and sensitization in Aplysia. Science 220: 91-93.
7. -. 1988. Morphological basis of short-term habituation in Aplysia. J. Neurosci. 8: 2452-2459.
8. Bellingham, M.C. and Walmsley, B. 1999. A novel presynaptic inhibitory mechanism underlies paired pulse depression at a fast central synapse. Neuron 23: 159-170.
9. Byrne, J.H. 1982. Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica. J. Neurophysiol. 48: 431-438.
10. Byrne, J.H. and Kandel, E.R. 1996. Presynaptic facilitation revisited: State and time dependence. J. Neurosci. 16: 425-435.
11. Byrne, J., Castellucci, V., and Kandel, E.R. 1974. Receptive fields and response properties of mechanoreceptor neurons innervating siphon skin and mantle shelf in Aplysia. J. Neurophysiol. 37: 1041-1064.
12. Byrne, J.H., Castellucci, V.F., Carew, T.J., and Kandel, E.R. 1978a. Stimulus-response relations and stability of mechanoreceptor and motor neurons mediating defensive gill-withdrawal reflex in Aplysia. J. Neurophysiol. 41: 402-417.
13. Byrne, J.H., Castellucci, V.F., and Kandel, E.R. 1978b. Contribution of individual mechanoreceptor sensory neurons to defensive gill-withdrawal reflex in Aplysia. J. Neurophysiol. 41: 418-431.
14. Byrne, J.H., Baxter, D.A., Buonomano, D.V., Cleary, L.J., Eskin, A., Goldsmith, J.R., McClendon, E., Nazif, F.A., Noel, F., and Scholz, K.P. 1991. Neural and molecular bases of nonassociative and associative learning in Aplysia. Ann. NY Acad. Sci. 627: 124-149.
15. Castellucci, V.F. and Kandel, E.R. 1974. A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. 71: 5004-5008.
16. Chin, J., Burdohan, J.A., Eskin, A., and Byrne, J.H. 2002. Inhibitor of glutamate transport alters synaptic transmission at sensorimotor synapses in Aplysia. J. Neurophysiol. 87: 3165-3169.
17. Chitwood, R.A., Li, Q., and Glanzman, D.L. 2001. Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J. Physiol. 534: 501-510.
18. Christoffersen, G.R.J. 1997. Habituation: Events in the history of its characterization and linkage to synaptic depression. Prog. Neurobiol. 53: 45-66.
19. Clatworthy, A.L. and Walters, E.T. 1993. Rapid amplification and facilitation of mechanosensory discharge in Aplysia by noxious stimulation. J. Neurophysiol. 70: 1181-1194.
20. Cleary, L.J., Byrne, J.H., and Frost, W.N. 1995. Role of interneurons in defensive withdrawal reflexes in Aplysia. Learn. Mem. 2: 133-151.
21. Conrad, P., Wu, F., and Schacher, S. 1999. Changes in functional glutamate receptors on a postsynaptic neuron accompany formation and maturation of an identified synapse. J. Neurobiol. 39: 237-248.
22. 3H]-noradrenaline from hippocampal slices. Br. J. Pharmacol. 123: 473-480.
23. Dale, N. and Kandel, E.R. 1993. L-Glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc. Natl. Acad. Sci. 90: 7163-7167.
24. Dale, N., Schacher, S., and Kandel, E.R. 1988. Long-term facilitation in Aplysia involves increase in transmitter release. Science 239: 282-285.
25. Diamond, J.S. and Jahr, C.E. 1995. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15: 1097-1107.
26. Eliot, L.S., Kandel, E.R., and Hawkins, R.D. 1994. Modulation of spontaneous transmitter release during depression and posttetanic potentiation of Aplysia sensory-motor neuron synapses isolated in culture. J. Neurosci. 14: 3280-3292.
27. Fedele, E. and Raiteri, M. 1996. Desensitization of AMPA receptors and AMPA-NMDA receptor interaction: An in vivo cyclic GMP microdialysis study in rat cerebellum. Br. J. Pharmacol. 117: 1133-1138.
28. Frost, L., Kaplan, S.W., Cohen, T.E., Henzi, V., Kandel, E.R., and Hawkins, R.D. 1997. A simplified preparation for relating cellular events to behavior: Contribution of LE and unidentified siphon sensory neurons to mediation and habituation of the Aplysia gill-and siphon-withdrawal reflex. J. Neurosci. 17: 2900-2913.
29. Gingrich, K.J. and Byrne, J.H. 1985. Simulation of synaptic depression, posttetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J. Neurophysiol. 53: 652-669.
30. Gover, T.D., Jiang, X.Y., and Abrams, T.W. 2002. Persistent, exocytosis-independent silencing of release sites underlies homosynaptic depression at sensory synapses in Aplysia. J. Neurosci. 22: 1942-1955.
31. Isaacson, J.S. and Walmsley, B. 1996. Amplitude and time course of spontaneous and evoked excitatory postsynaptic currents in bushy cells of the anteroventral cochlear nucleus. J. Neurophysiol. 76: 1566-1571.
32. Ishikawa, T. and Takahashi, T. 2001. Mechanisms underlying presynaptic facilitatory effect of cyclothiazide at the Calyx of Held of juvenile rats. J. Physiol. 533 (Pt 2): 423-431.
33. Jiang, X.Y. and Abrams, T.W. 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.
34. Jones, M.V. and Westbrook, G.L. 1996. The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci. 19: 96-101.
35. Levenson, J., Endo, S., Kategaya, L.S., Fernandez, R.I., Brabham, D.G., Chin, J., Byrne, J.H., and Eskin, A. 2000a. Long-term regulation of neuronal high-affinity glutamate and glutamine uptake in Aplysia. Proc. Natl. Acad. Sci. 97: 12858-12863.
36. Levenson, J., Sherry, D.M., Dryer, L., Chin, J., Byrne, J.H., and Eskin, A. 2000b. Localization of glutamate and glutamate transporters in the sensory neurons of Aplysia. J. Comp. Neurol. 423: 121-131.
37. Partin, K.M., Patneau, D.K., and Mayer, M.L. 1994. Cyclothiazide differentially modulates desensitization of α -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor splice variants. Mol. Pharmacol. 46: 129-138.
38. Patneau, D.K., Vyklicky Jr., L., and Mayer, M.L. 1993. Hippocampal neurons exhibit cyclothiazide-sensitive rapidly desensitizing responses to kainate. J. Neurosci. 13: 3496-3509.
39. Phares G.A., Antzoulatos, E.G., Baxter, D.A., and Byrne, J.H. 2003. Burst-induced synaptic depression and its modulation contribute to information transfer at Aplysia sensorimotor synapses: Empirical and computational analyses. J. Neurosci. (in press).
40. Rammes, G., Swandulla, D., Collingridge, G.L., Hartmann, S., and Parsons, C.G. 1996. Interactions of 2,3-benzodiazepines and cyclothiazide at AMPA receptors: Patch clamp recordings in cultured neurones and area CA1 in hippocampal slices. Br. J. Pharmacol. 117: 1209-1221.
41. Royer, S., Coulson, R.L., and Klein, M. 2000. Switching off and on of synaptic sites at Aplysia sensorimotor synapses. J. Neurosci. 20: 626-638.
42. Rozov, A., Jerecic, J., Sakmann, B., and Burnashev, N. 2001. AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/3 of rat neocortex. J. Neurosci. 21: 8062-8071.
43. Schacher, S., Wu, F., and Sun, Z.Y. 1997. Pathway-specific synaptic plasticity: Activity-dependent enhancement and suppression of long-term heterosynaptic facilitation at converging inputs on a single target. J. Neurosci. 17: 597-606.
44. Stopfer, M. and Carew, T.J. 1996. Heterosynaptic facilitation of tail sensory neuron synaptic transmission during habituation in tail-induced tail and siphon withdrawal reflexes of Aplysia. J. Neurosci. 16: 4933-4948.
45. Storozhuk, M.V. and Castellucci, V.F. 1999. Some receptor properties in motor neurons of an Aplysia withdrawal reflex. Neurochem. Res. 24: 1443-1447.
46. Trudeau, L.E. and Castellucci, V.F. 1993. Excitatory amino acid neurotransmission at sensory-motor and interneuronal synapses of Aplysia californica. J. Neurophysiol. 70: 1221-1230.
47. -. 1995. Postsynaptic modifications in long-term facilitation in Aplysia: Upregulation of excitatory amino acid receptors. J. Neurosci. 15: 1275-1284.
48. Trussell, L.O., Zhang, S., and Raman, I.M. 1993. Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10: 1185-1196.
49. Walters, E.T., Byrne, J.H., Carew, T.J., and Kandel, E.R. 1983. Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J. Neurophysiol. 50: 1522-1542.
50. Zhang, F., Goldsmith, J.R., and Byrne, J.H. 1994. Neural analogue of long-term sensitization training produces long-term (24 and 48 h) facilitation of the sensory-to-motor neuron connection in Aplysia. J. Neurophysiol. 72: 778-784.
51. Zhao, Y. and Klein, M. 2002. Modulation of the readily releasable pool of transmitter and of excitation-secretion coupling by activity and by serotonin at Aplysia sensorimotor synapses in culture. J. Neurosci. 22: 10671-10679.
52. Zhu, H., Wu, F., and Schacher, S. 1997. Site-specific and sensory neuron-dependent increases in postsynaptic glutamate sensitivity accompany serotonin-induced long-term facilitation at Aplysia sensorimotor synapses. J. Neurosci. 17: 4976-4986.