Protein kinase C acts as a molecular detector of firing patterns to mediate sensory gating in Aplysia

Nature Neuroscience

Volumn 15, Issue 8, 2012, Pages 1144-1152

  Wan, Qin ^a   Jiang, Xue Ying ^a   Negroiu, Andreea M ^a   Lu, Shao Gang ^a   McKay, Kimberly S ^a   Abrams, Thomas W ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN KINASE C;

ACTION POTENTIAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; APLYSIA; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; HABITUATION; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NERVE STIMULATION; NONHUMAN; PDZ DOMAIN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSORY GATING; SENSORY NERVE CELL; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; APLYSIA; BEHAVIOR, ANIMAL; CALCIUM; CALCIUM CHANNELS; HABITUATION, PSYCHOPHYSIOLOGIC; ISOENZYMES; NEURONAL PLASTICITY; PROTEIN KINASE C; SENSORY GATING; SENSORY RECEPTOR CELLS; SYNAPTIC TRANSMISSION;

EID: 84864426470     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3158     Document Type: Article

References (51)

1. Byrne, J.H. Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica. J. Neurophysiol. 48, 431-438 (1982).
2. Eliot, L.S., Kandel, E.R. & Hawkins, R.D. Modulation of spontaneous transmitter release during depression and posttetanic potentiation of Aplysia sensory-motor neuron synapses isolated in culture. J. Neurosci. 14, 3280-3292 (1994).
3. Castellucci, V.F. & Kandel, E.R. A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia. Proc. Natl. Acad. Sci. USA 71, 5004-5008 (1974).
4. Cohen, T.E., Kaplan, S.W., Kandel, E.R. & Hawkins, R.D. A simplified preparation for relating cellular events to behavior: mechanisms contributing to habituation, dishabituation and sensitization of the Aplysia gill-withdrawal reflex. J. Neurosci. 17, 2886-2899 (1997).
5. Frost, L. et al. 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 (1997).
6. Antonov, I., Kandel, E.R. & Hawkins, R.D. The contribution of facilitation of monosynaptic PSPs to dishabituation and sensitization of the Aplysia siphon withdrawal reflex. J. Neurosci. 19, 10438-10450 (1999).
7. Gover, T.D., Jiang, X.Y. & Abrams, T.W. Persistent, exocytosis-independent silencing of release sites underlies homosynaptic depression at sensory synapses in Aplysia. J. Neurosci. 22, 1942-1955 (2002).
8. Illich, P.A. & Walters, E.T. Mechanosensory neurons innervating Aplysia siphon encode noxious stimuli and display nociceptive sensitization. J. Neurosci. 17, 459-469 (1997).
9. Byrne, J.H. & Kandel, E.R. Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16, 425-435 (1996).
10. Walters, E.T. & Byrne, J.H. Post-tetanic potentiation in Aplysia sensory neurons. Brain Res. 293, 377-380 (1984).
11. Zucker, R.S. & Regehr, W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002).
12. Hawkins, R.D., Abrams, T.W., Carew, T.J. & Kandel, E.R. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219, 400-405 (1983).
13. Walters, E.T. & Byrne, J.H. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219, 405-408 (1983).
14. Jiang, X.Y. & Abrams, T.W. 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 (1998).
15. Marinesco, S. & Carew, T.J. Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: characterization and relationship to heterosynaptic plasticity. J. Neurosci. 22, 2299-2312 (2002).
16. Stark, L.L., Mercer, A.R., Emptage, N.J. & Carew, T.J. Pharmacological and kinetic characterization of two functional classes of serotonergic modulation in Aplysia sensory neurons. J. Neurophysiol. 75, 855-866 (1996).
17. Jarrard, H.E., Goldsmith, B.A. & Abrams, T.W. In Aplysia sensory neurons, the neuropeptide SCPB and serotonin differ in efficacy both in modulating cellular properties and in activating adenylyl cyclase: implications for mechanisms underlying presynaptic facilitation. Brain Res. 616, 188-199 (1993).
18. + channels in Aplysia sensory neurones. Nature 299, 413-417 (1982).
19. Royer, S., Coulson, R.L. & Klein, M. Switching off and on of synaptic sites at Aplysia sensorimotor synapses. J. Neurosci. 20, 626-638 (2000).
20. Adler, E.M., Augustine, G.J., Duffy, S.N. & Charlton, M.P. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11, 1496-1507 (1991).
21. Bao, J.X., Kandel, E.R. & Hawkins, R.D. Involvement of pre-and postsynaptic mechanisms in posttetanic potentiation at Aplysia synapses. Science 275, 969-973 (1997).
22. Antonov, I., Antonova, I., Kandel, E.R. & Hawkins, R.D. Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37, 135-147 (2003).
23. +. Proc. Natl. Acad. Sci. USA 93, 9931-9936 (1996).
24. Bougie, J.K. et al. The atypical protein kinase C in Aplysia can form a protein kinase M by cleavage. J. Neurochem. 109, 1129-1143 (2009).
25. Sossin, W.S. Isoform specificity of protein kinase Cs in synaptic plasticity. Learn. Mem. 14, 236-246 (2007).
26. Dominguez, I. et al. Inhibition of protein kinase C zeta subspecies blocks the activation of an NF-κB-like activity in Xenopus laevis oocytes. Mol. Cell. Biol. 13, 1290-1295 (1993).
27. Guizzetti, M. & Costa, L.G. Possible role of protein kinase C zeta in muscarinic receptor-induced proliferation of astrocytoma cells. Biochem. Pharmacol. 60, 1457-1466 (2000).
28. + influx in presynaptic facilitation. Nature 361, 634-637 (1993).
29. Kohout, S.C., Corbalan-Garcia, S., Torrecillas, A., Gomez-Fernandez, J.C. & Falke, J.J. C2 domains of protein kinase C isoforms alpha, beta, and gamma: activation parameters and calcium stoichiometries of the membrane-bound state. Biochemistry 41, 11411-11424 (2002).
30. Staudinger, J., Lu, J. & Olson, E.N. Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J. Biol. Chem. 272, 32019-32024 (1997).
31. +-independent PKCs expressed in Aplysia sensory cells. J. Neurosci. 11, 2303-2313 (1991).
32. Sossin, W.S., Diaz-Arrastia, R. & Schwartz, J.H. Characterization of two isoforms of protein kinase C in the nervous system of Aplysia californica. J. Biol. Chem. 268, 5763-5768 (1993).
33. Dumitriu, B., Cohen, J.E., Wan, Q., Negroiu, A.M. & Abrams, T.W. Serotonin receptor antagonists discriminate between PKA-and PKC-mediated plasticity in Aplysia sensory neurons. J. Neurophysiol. 95, 2713-2720 (2006).
34. Antonov, I., Ha, T., Antonova, I., Moroz, L.L. & Hawkins, R.D. Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia. J. Neurosci. 27, 10993-11002 (2007).
35. Frost, W.N., Clark, G.A. & Kandel, E.R. Parallel processing of short-term memory for sensitization in Aplysia. J. Neurobiol. 19, 297-334 (1988).
36. Gingrich, K.J. & Byrne, J.H. 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 (1985).
37. Zhao, Y. & Klein, M. 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 (2002).
38. Bailey, C.H. & Chen, M. Morphological basis of short-term habituation in Aplysia. J. Neurosci. 8, 2452-2459 (1988).
39. Tang, Y., Schlumpberger, T., Kim, T., Lueker, M. & Zucker, R.S. Effects of mobile buffers on facilitation: experimental and computational studies. Biophys. J. 78, 2735-2751 (2000).
40. Tank, D.W., Regehr, W.G. & Delaney, K.R. A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement. J. Neurosci. 15, 7940-7952 (1995).
41. Oancea, E. & Meyer, T. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95, 307-318 (1998).
42. +-dependent PKC APL I in the induction of intermediate-term facilitation. J. Neurosci. 26, 8847-8856 (2006).
43. + current. J. Exp. Biol. 89, 117-157 (1980).
44. +-independent protein kinase C Apl II mediates the serotonin-induced facilitation at depressed Aplysia sensorimotor synapses. J. Neurosci. 21, 1247-1256 (2001).
45. Pinsker, H., Kupfermann, I., Castellucci, V. & Kandel, E. Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science 167, 1740-1742 (1970).
46. Moore, T. & Armstrong, K.M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370-373 (2003).
47. Winkowski, D.E. & Knudsen, E.I. Top-down control of multimodal sensitivity in the barn owl optic tectum. J. Neurosci. 27, 13279-13291 (2007).
48. Pashler, H., Johnston, J.C. & Ruthruff, E. Attention and performance. Annu. Rev. Psychol. 52, 629-651 (2001).
49. Knudsen, E.I. Control from below: the role of a midbrain network in spatial attention. Eur. J. Neurosci. 33, 1961-1972 (2011).
50. Murphy, G.G. & Glanzman, D.L. Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278, 467-471 (1997).
51. Lin, A.H. et al. Serotonin stimulation of cAMP-dependent plasticity in Aplysia sensory neurons is mediated by calmodulin-sensitive adenylyl cyclase. Proc. Natl. Acad. Sci. USA 107, 15607-15612 (2010).