Role of nitric oxide in classical conditioning of siphon withdrawal in Aplysia

Journal of Neuroscience

Volumn 27, Issue 41, 2007, Pages 10993-11002

  Antonov, Igor ^a   Ha, Thomas ^c   Antonova, Irina ^a   Moroz, Leonid L ^c,d   Hawkins, Robert D ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Aplysia; Classical conditioning; Facilitation; Motor neuron; Nitric oxide; Sensory neuron

Indexed keywords

AMPA RECEPTOR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; SCAVENGER;

ANIMAL CELL; APLYSIA; ARTICLE; BEHAVIOR; CONDITIONED REFLEX; CONDITIONING; CONTROLLED STUDY; EXOCYTOSIS; FACILITATION; GANGLION; IN SITU HYBRIDIZATION; MOTONEURON; NERVE CELL; NERVE CELL MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SYNAPSE; WITHDRAWAL REFLEX;

ANIMALS; APLYSIA; CONDITIONING, CLASSICAL; EXCITATORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; NEURONAL PLASTICITY; NITRIC OXIDE; REFLEX;

EID: 35348837301     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2357-07.2007     Document Type: Article

References (85)

1. Abrams TW, Yovell Y, Onyike CU, Cohen JE, Jarrard HE (1998) Analysis of sequence-dependent interactions between calcium and transmitter stimuli in activating adenylyl cyclase in Aplysia: possible contributions to CS-US sequence requirement during conditioning. Learn Mem 4:496-509.
2. Antonov I, Kandel ER, Hawkins RD (1999) The contribution of facilitation of monosynaptic PSPs to dishabituation and sensitization of the Aplysia siphon withdrawal reflex. J Neurosci 19:10438-10450.
3. Antonov I, Antonova I, Kandel ER, Hawkins RD (2001) The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J Neurosci 21:6413-6422.
4. Antonov I, Antonova I, Kandel ER Hawkins RD (2003) Activity-dependent presynaptic facilitation and Hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron 37:135-147.
5. Antonova I, Arancio O, Trillat A-C, Wang H-G, Zablow L, Udo H, Kandel ER, Hawkins RD (2001) Rapid increase in clusters of presynaptic proteins at onset of long-lasting potentiation. Science 294:1547-1550.
6. Bailey CH, Hawkins RD, Chen MC, Kandel ER (1981) Interneurons involved in mediation and modulation of gill-withdrawal reflex in Aplysia. IV. Morphological basis of presynaptic facilitation. J Neurophysiol 45:340-360.
7. Bao J-X, Kandel ER, Hawkins RD (1998) Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning at Aplysia sensory-motor neuron synapses in isolated cell culture. J Neurosci 18:458-466.
8. Bodnarova M, Jezzini S, Weiss KR, Vilim SF, Moroz LL (2002) The distribution of nitric oxide synthase (NOS) in the CNS and peripheral tissues of Aplysia californica. Soc Neurosci Abstr 28:335.5.
9. Bodnarova M, Martasek P, Moroz LL (2005) Calcium/calmodulin-dependent nitric oxide synthase activity in the CNS of Aplysia californica: biochemical characterization and link to cGMP pathways. J Inorg Biochem 99:922-928.
10. Bozdagi O, Shan W, Tanaka H, Benson DL, Huntley GW (2000) Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron 28:245-259.
11. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
12. Byrne JH, Castellucci V, Kandel ER (1974) Receptive fields and response properties of mechanoreceptor neurons innervating skin and mantle shelf of Aplysia. J Neurophysiol 37:1041-1064.
13. Chitwood RA, Li Q, Glanzman DL (2001) Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J Physiol (Lond) 534:501-510.
14. Clark GA, Hawkins RD, Kandel ER (1994) Activity-dependent enhancement of presynaptic facilitation provides a cellular mechanism for the temporal specificity of classical conditioning in Aplysia. Learn Mem 1:243-257.
15. Cohen-Cory S (2002) The developing synapse: construction and modulation of synaptic structures and circuits. Science 298:770-776.
16. Colicos MA, Collins BE, Sailor MJ, Goda Y (2001) Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107:605-616.
17. Conrad P, Wu F, 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.
18. Cramer KS, Leamey CA, Sur M (1998) Nitric oxide as a signaling molecule in visual system development. Prog Brain Res 118:101-114.
19. Dale N, Kandel ER (1993) L-Glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc Natl Acad Sci USA 90:7163-7167.
20. Eliot LS, Hawkins RD, Kandel ER, Schacher S (1994) Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell cultures. J Neurosci 14:368-383.
21. Fischer TM, Carew TJ (1993) Activity-dependent potentiation of recurrent inhibition: a mechanism for dynamic gain control in the siphon withdrawal reflex of Aplysia. J Neurosci 13:1302-1314.
22. Fischer TM, Carew TJ (1995) Cutaneous activation of the inhibitory L30 interneurons provides a mechanism for regulating adaptive gain control in the siphon withdrawal reflex of Aplysia. J Neurosci 15:762-773.
23. Fischer TM, Blazis DE, Priver NA, Carew TJ (1997) Metaplasticity at identified inhibitory synapses in Aplysia. Nature 389:860-965.
24. Frost WN, Kandel ER (1995) Structure of the network mediating siphon-elicited siphon withdrawal in Aplysia. J Neurophysiol 73:2413-2427.
25. Frost WN, Clark GA, Kandel ER (1988) Parallel processing of short-term memory for sensitization in Aplysia. J Neurobiol 19:297-334.
26. Gingrich KJ, Byrne JH (1985) Simulation of synaptic depression, post-tetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J Neurophysiol 53:652-669.
27. Glanzman DL (1994) Postsynaptic regulation of the development and long-term plasticity of Aplysia sensorimotor synapses in cell culture. J Neurobiol 25:666-693.
28. Glanzman DL, Kandel ER, Schacher S (1990) Target-dependent structural changes accompanying long-term synaptic facilitation in Aplysia neurons. Science 249:799-802.
29. Graves AR, Lewin KA, Lindgren C (2004) Nitric oxide, cAMP and the biphasic muscarinic modulation of ACh release at the lizard neuromuscular junction. J Physiol (Lond) 59:423-432.
30. 2+ current in sensory neurons. J Neurophysiol 45:327-339.
31. Hawkins RD (1989a) Localization of potential serotonergic facilitator neurons in Aplysia by glyoxylic acid histofluorescence combined with retrograde fluorescent labeling. J Neurosci 9:4214-4226.
32. Hawkins RD (1989b) A biologically based computational model for several simple forms of learning. Psychol Learn Motiv 23:65-108.
33. Hawkins RD (1996) NO Honey, I don't remember. Neuron 16:465-467.
34. Hawkins RD (2007) Trans-synaptic signaling by NO during learning-related synaptic plasticity. In: Learning and memory - a comprehensive reference (Byrne JH, ed). Oxford: Elsevier.
35. Hawkins RD, Schacher S (1989) Identified facilitator neurons L29 and L28 are excited by cutaneous stimuli used in dishabituation, sensitization, and classical conditioning in Aplysia. J Neurosci 9:4236-4245.
36. Hawkins RD, Castellucci VF, Kandel ER (1981a) Interneurons involved in mediation and modulation of gill-withdrawal reflex in Aplysia. I. Identification and characterization. J Neurophysiol 45:304-314.
37. Hawkins RD, Castellucci VF, Kandel ER (1981b) Interneurons involved in mediation and modulation of gill-withdrawal reflex in Aplysia. II. Identified neurons produce heterosynaptic facilitation contributing to behavioral sensitization. J Neurophysiol 45:315-326.
38. Hawkins RD, Abrams TW, Carew TJ, Kandel ER (1983) A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219:400-415.
39. Hawkins RD, Son H, Arancio O (1998) Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118:155-172.
40. Hickie C, Cohen LB, Balaban PM (1997) The synapse between LE sensory neurons and gill motoneurons makes only a small contribution to the Aplysia gill-withdrawal reflex. Eur J Neurosci 9:627-636.
41. Huang Y, Man HY, Sekine-Aizawa Y, Han Y, Juluri J, Luo H, Cheah J, Lowenstein C, Huganir RL, Snyder SH (2005) S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors. Neuron 46:533-540.
42. Jezzini SH, Bodnarova M, Moroz LL (2005) Two-color in situ hybridization in the CNS of Aplysia californica. J Neurosci Methods 149:15-25.
43. Jin I, Hawkins RD (2003) Presynaptic and postsynaptic mechanisms of a novel form of homosynaptic potentiation at Aplysia sensory-motor neuron synapses. J Neurosci 23:7288-7297.
44. Jin I, Udo H, Kandel ER, Hawkins RD (2003) Rapid increase in synaptophysin puncta at onset of homosynaptic potentiation in Aplysia. Soc Neurosci Abstr 29:291.22.
45. Kandel ER, Abrams T, Bernier L, Carew TJ, Hawkins RD, Schwartz JH (1983) Classical conditioning and sensitization share aspects of the same molecular cascade in Aplysia. Cold Spring Harbor Symp Quant Biol 48:821-830.
46. Katzoff A, Ben-Gedalya T, Susswein AJ (2002) Nitric oxide is necessary for multiple memory processes after learning that food is inedible in Aplysia. J Neurosci 22:9581-9594.
47. Kim J-H, Udo H, Li H-L, Toun TY, Chen M, Kandel ER, Bailey CH (2003) Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40:151-165.
48. Koh HY, Jacklet JW (1999) Nitric oxide stimulates cGMP production and mimics synaptic responses in metacerebral neurons of Aplysia. J Neurosci 19:3818-3826.
49. Koh HY, Jacklet JW (2001) Nitric oxide induces cGMP immunoreactivity and modulates membrane conductance in identified central neurons of Aplysia. Eur J Neurosci 13:553-560.
50. 2+ transients. Neuron 15:407-415.
51. Lewin MR, Walters ET (1999) Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2:18-23.
52. Li H, Huang BSH, Kandel ER (2004) Innervation-dependent clustering of glutamate receptors during regeneration and plasticity-associated synaptogenesis in Aplysia. Soc Neurosci Abstr 30:614.18.
53. 2+ from postsynaptic intracellular stores, postsynaptic exocytosis, and modulation of postsynaptic AMPA receptor efficacy. J Neurosci 25:5623-5637.
54. Lin XY, Glanzman DL (1994a) Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of a NMDA-related receptor. Proc R Soc Lond B Biol Sci 255:215-221.
55. Lin XY, Glanzman DL (1994b) Long-term potentiation of Aplysia sensorimotor synapses in cell culture: regulation by postsynaptic voltage. Proc R Soc Lond B Biol Sci 255:113-118.
56. Luscher C, Nicoll RA, Malenka RC, Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550.
57. Mackey SL, Kandel ER, Hawkins RD (1989) Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia of Aplysia produce presynaptic facilitation of siphon sensory neurons. J Neurosci 9:4227-4235.
58. Martasek P, Sadreev RI, Bodnarova M, Uvarov P, Panchin YV, Moroz LL (2002) Two neuronal-like nitric oxide synthases in Aplysia californica: cloning and characterization. Soc Neurosci Abstr 28:335.6.
59. Martasek P, Bodnarova M, Panchin YV, Sadreyev RI, Uvarov PN, Jezzini SH, Moroz LL (2004) Characterization of NO/cGMP signaling in the CNS of Aplysia californica. Soc Neurosci Abstr 30:497.10.
60. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761-766.
61. Moroz LL (2000) Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Tech 49:557-569.
62. Moroz LL (2006) Localization of putative nitrergic neurons in peripheral chemosensory areas and the central nervous system of Aplysia californica. J Comp Neurol 495:10-20.
63. Moroz LL, Kohn AB (2007) On the comparative biology of NO synthetic pathways: parallel evolution of NO mediated signaling. In: Nitric oxide, advances in experimental biology (Trimmer B, Tota B, Wang T, eds), pp 1-45. Amsterdam: Elsevier.
64. Moroz LL, Chen D, Gillette MU, Gillette R (1996) Nitric oxide synthase activity in the molluscan CNS. J Neurochem 66:873-876.
65. Moroz LL, Dahlgren RL, Boudko D, Sweedler JV, Lovell P (2005) Direct single cell determination of nitric oxide synthase related metabolites in identified nitrergic neurons. J Inorg Biochem 99:929-939.
66. Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T, Sheng H, Shaw R, Kalachikov S, Panchin YV, Farmerie W, et al. (2006) Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell 127:1453-1467.
67. Mothet JP, Fossier P, Tauc L, Baux G (1996a) Opposite actions of nitric oxide on cholinergic synapses: which pathways. Proc Natl Acad Sci USA 93:8721-8726.
68. 2+ influx and protein kinase G. J Physiol (Lond) 493:769-784.
69. 2+. Proc Natl Acad Sci USA 93:9931-9936.
70. Murphy GG, Glanzman DL (1997) Mediation of classical conditioning in Aplysia californica by long-term potentiation of sensorimotor synapses. Science 278:467-471.
71. Murphy GG, Glanzman DL (1999) Cellular analog of differential classical conditioning in Aplysia: disruption by the NMDA receptor antagonist DL-2-amino-5-phosphono-valerate. J Neurosci 19:10595-10602.
72. Nikonenko I, Jourdain P, Muller D (2003) Presynaptic remodeling contributes to activity-dependent synaptogenesis. J Neurosci 24:8498-8505.
73. Ocorr KA, Walters ET, Byrne JH (1985) Associative conditioning analog selectively increases cAMP levels of tail sensory neurons in Aplysia. Proc Natl Acad Sci USA 82:2548-2552.
74. Roberts AC, Glanzman DL (2003) Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci 26:662-670.
75. Sadreyev RI, Panchin Y, Uvarov P, Belyavski A, Matz M, Moroz LL (2000) Cloning of nitric oxide synthase (NOS) from Aplysia californica. Soc Neurosci Abstr 26:343.16.
76. Schwarte RC, Godfrey EW (2004) Nitric oxide synthase activity is required for postsynaptic differentiation of the embryonic neuromuscular junction. Dev Biol 273:276-284.
77. Sugita S, Baxter DA, Byrne JH (1997) Differential effects of 4-aminopyridine, serotonin, and phorbol esters on facilitation of sensorimotor connections in Aplysia. J Neurophysiol 77:177-185.
78. Sung Y-J, Walters ET, Ambron RT (2004) A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J Neurosci 24:7583-7595.
79. Sunico CR, Portillo F, Gonzalez-Forero D, Moreno-Lopez B (2005) Nitric-oxide-directed synaptic remodeling in the adult mammalian CNS. J Neurosci 25:1448-1458.
80. Truman JW, de Vente J, Ball EE (1996) Nitric oxide-sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development in insects. Development 122:3949-3958.
81. Tsukada S, Keino-Masu K, Masu M, Fukada J (2002) Activation of protein kinase A by nitric oxide in cultured dorsal root ganglion neurites of the rat, examined by a fluorescence probe, ARII. Neurosci Lett 318:17-20.
82. Walters ET, Byrne JH (1983) Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219:405-408.
83. Wang H-G, Lu F-M, Jin I, Udo H, Kandel ER, de Vente J, Walter U, Lohmann SM, Hawkins RD, Antonova I (2005) Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45:389-403.
84. Winer BJ, Brown DR, Kenneth MM (1991) Statistical principles in experimental design. New York: McGraw-Hill.
85. Zhang N, Beuve A, Townes-Anderson E (2005) The nitric oxide-cGMP signaling pathway differentially regulates presynaptic structural plasticity in cone and rod cells. J Neurosci 25:2761-2770.