Levels of serotonin the hemolymph of Aplysia are modulated by light/dark cycles and sensitization training

Journal of Neuroscience

Volumn 19, Issue 18, 1999, Pages 8094-8103

  Levenson, Jonathan ^a   Byrne, John H ^b   Eskin, Arnold ^a,c  

^a University of Houston   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

Author keywords

Aplysia; Diurnal rhythms; Emetine; Feeding; Hemolymph; Learning; Mollusk; Sensitization; Serotonin

Indexed keywords

SEROTONIN;

ANIMAL BEHAVIOR; APLYSIA; ARTICLE; FEEDING BEHAVIOR; HEMOLYMPH; LIGHT DARK CYCLE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; TRAINING;

EID: 0033568853     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-18-08094.1999     Document Type: Article

References (105)

1. Abel T, Martin KC, Bartsch D, Kandel ER (1998) Memory suppressor genes: Inhibitory constraints on the storage of long-term memory. Science 279:338-341.
2. Adamo SA, Chase R (1991) "Central arousal" and sexual responsiveness in the snail, Helix aspersa. Behav Neural Biol 55:194-213.
3. Agranoff BW, Davis RE, Casola L, Lim R (1967) Actinomycin D blocks formation of memory of shock avoidance in goldfish. Science 158:1600-1601.
4. Agranoff BW, Burrell HR, Dokas LA, Springer AD (1978) Progress in biochemical approaches to learning and memory. In: Psychopharmacology: a generation of progress (Lipton MA, Di Mascio A, Killam KF, eds), pp 623-635. New York: Raven.
5. Alberini CM, Ghirardi M, Metz R, Kandel ER (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114.
6. Alevizos A, Bailey CH, Chen M, Koester J (1989) Innervation of vascular and cardiac muscle of Aplysia by multimodal motoneuron L7. J Neurophysiol 61:1053-1063.
7. Angers A, Storozhuk M V, Duchaine T, Castellucci VF, DesGroseillers L (1998) Cloning and functional expression of an Aplysia 5-HT receptor negatively coupled to adenylate cyclase. J Neurosci 18:5586-5593.
8. 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.
9. Bailey CH, Montarolo P, Chen M, Kandel ER, Schacher S (1992) Inhibitors of protein and RNA synthesis block structural changes that accompany long-term hcterosynaptic plasticity in Aplysia. Neuron 9:749-758.
10. Barondes SH (1975) Protein synthesis dependent and protein synthesis independent memory storage processes. In: Short-term memory (Deutsch D, Deutsch JA, eds), pp 379-390. New York: Academic.
11. Bernier L, Castellucci VF, Kandel ER, Schwartz JH (1982) Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex inAplysia. J Neurosci 2:1682-1691.
12. B), FMRFamide, acetylcholine, and dopamine. Neurosci Lett 105:200-204.
13. Brunelli M, Castellucci V, Kandel ER (1976) Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194:1178-1181.
14. Bunge SA, Mauelshagen J, Carew TJ (1997) Reversal of relative thresholds for synaptic facilitation and increased excitability induced by serotonin and tail nerve stimulation in Aplysia sensory neurons. Neurobiol Learn Mem 67:259-263.
15. Byrne JH, Baxter DA, Buonomano DV, Cleary LJ, Eskin A, Goldsmith JR, McClendon E, Nazif FA, Noel F, Scholz KP (1991) Neural and molecular bases of nonassociative and associative learning in Aplysia. Ann NY Acad Sci 627:124-149.
16. Cardot J (1971) Variations saisonnières de la 5-hydroxytryptamine dans les tissus nerveux et cardiaque chex la mollusque Helix pomatia. C R Séances Soc Biol Fil 165:338-341.
17. Castellucci VF, Frost WN, Goelet P, Montarolo PG, Schacher S, Morgan JA, Blumenfeld H, Kandel ER (1986) Cell and molecular analysis of long-term sensitization in Aplysia. J Physiol (Paris) 81:349-357.
18. Claassen D, Kammer A (1985) Effects of octopamine, dopamine, and serotonin on production of flight motor output by throacic ganglia of Manduca sexta. J Neurobiol 17:1-14.
19. Cleary LJ, Lee WL, Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. J Neurosci 18:5988-5998.
20. Colwell CS (1990) Light and serotonin interact in affecting the arcadian system of Aplysia. J Comp Physiol [A] 167:841-845.
21. Cooper BF, Krontiris-Litowitz JK, Walters ET (1989) Humoral factors released during trauma of Aplysia body wall II. Effects of possible mediators. J Comp Physiol [B] 159:225-235.
22. Corrent G, Eskin A (1982) Transmitterlike action of serotonin in phase shifting a rhythm from the Aplysia eye. Am J Physiol 242:R333-R338.
23. Corrent G, Eskin A, Kay I (1982) Entrainment of the circadian rhythm from the eye of Aplysia: role of serotonin. Am J Physiol 242:R326-R332.
24. Davis HP, Squire LR (1984) Protein synthesis and memory: a review. Psychol Bull 96:518-559.
25. Deguchi T, Axelrod J (1972) Control of circadian change in serotonin JV-acetyltransferase activity in the pineal organ by the β-adrenergic receptor. Proc Natl Acad Sci USA 69:2547-2550.
26. Drummond AH, Benson JA, Levitan IB (1980a) Serotonin-induced hyperpolarization of an identified Aplysia neuron is mediated by cyclic AMP. Proc Natl Acad Sci USA 77:5013-5017.
27. 3H]LSD binding and adenylate cyclase stimulation. Brain Res 184:163-177.
28. Edwards DH, Kravitz EA (1997) Serotonin, social status and aggression. Curr Opin Neurobiol 7:812-819.
29. Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262:253-256.
30. Emptage NJ, Mauelshagen J, Carew TJ (1996) Threshold serotonin concentration required to produce synaptic facilitation differs for depressed and nondepressed synapses in Aplsyia sensory neurons. J Neurophysiol 75:843-854.
31. Eskin A, Maresh RD (1982) Serotonin or electrical optic nerve stimulation increases the photosensitivity of the Aplysia eye. Comp Biochem Physiol 73C:27-31.
32. Flexner JB, Flexner LB, Stellar E (1963) Memory in mice as affected by intracerebral puromycin. Science 141:57-59.
33. Galvez R, Mesches MH, McGaugh JL (1996) Norepinephrine release in the amygdala in response to footshock stimulation. Neurobiol Learn Mem 66:253-257.
34. Glanzman DL, Mackey SL, Hawkins RD, Dyke AM, Lloyd PE, Kandel ER (1989) Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock. J Neurosci 9:4200-4213.
35. Goelet P, Castellucci VF, Schacher S, Kandel ER (1986) The long and short of long term memory-a molecular framework. Nature 322:419-422.
36. 3H]serotonin in the marine mollusc, Aplysia californica. Brain Res 136:77-88.
37. Goldsmith JR, Byrne JH (1993) Bag cell extract inhibits tail-siphon withdrawal reflex, suppresses long-term but not short-term sensitization, and attenuates sensory-to-motor neuron synapses in Aplysia. J Neurosci 13:1688-1700.
38. Goldstein R, Kistler HB, Steinbusch HW, Schwartz JH (1984) Distribution of serotonin-immunoreactivity in juvenile Aplysia. Neuroscience 11:535-547.
39. Hammer M, Cleary LJ, Byrne JH (1989) Serotonin acts in the synaptic region of sensory neurons in Aplysia to enhance transmitter release. Neurosci Lett 104:235-240.
40. Hegde AN, Inokuchi K, Pei W, Casadio A, Ghirardi M, Chain DG, Martin KC, Kandel ER, Schwartz JH (1997) Ubiquitin c-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-126.
41. Hernádi L, Rózsa KS-, Jahan-Parwar B, Carpenter DO (1992) A topography and ultrastructural characterization of in vivo 5,7-dihydroxytryptamine-labeled serotonin-containing neurons in the central nervous system of Aplysia californica. Cell Mol Neurobiol 12:317-325.
42. Jacklet JW (1969) Circadian rhythm of optic nerve impulses recorded in darkness from isolated eye of Aplysia. Science 164:562-563.
43. Kaczmarek LK, Jennings K, Strumwasser F (1978) Neurotransmitter modulation, phosphodiesterase inhibitor effects, and cyclic AMP correlates of afterdischarge in peptidergic neurites. Proc Natl Acad Sci USA 75:5200-5204.
44. Kanyicska B, Livingstone JD, Freeman ME (1995) Long term exposure to dopamine reverses the inhibitory effect of endothelin-1 on prolactin secretion. Endocrinology 136:990-994.
45. + channels in rat lactotrophs: reversal by long-term exposure to dopamine agonist. Endocrinology 138:3141-3153.
46. Kistler HB, Hawkins RD, Koester J, Steinbusch HW, Kandel ER, Schwartz JH (1985) Distribution of serotonin-immunoreactive cell bodies and processes in the abdominal ganglion of mature Aplysia. J Neurosci 5:72-80.
47. Klein DC, Weller JL (1972) Rapid light-induced decrease in pineal serotonin N-acetyltransferase activity. Science 177:532-533.
48. Klein M, Camardo J, Kandel ER (1982) Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation in Aplysia. Proc Natl Acad Sci USA 79:5713-5717.
49. Krontiris-Litowitz JK, Cooper BF, Walters ET (1989) Humoral factors released during trauma of Aplysia body wall: I. Body wall contraction, cardiac modulation, and central reflex suppression. J Comp Physiol [B] 159:211-223.
50. Kupfermann I (1974) Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol 10:1-26.
51. Kupfermann I, Weiss KR (1982) Activity of an identified serotonergic neuron in free maving Aplysia correlates with behavioral arousal. Brain Res 241:334-337.
52. Kupfermann I, Cohen JL, Mandelbaum DE, Schonberg M, Susswein AJ, Weiss KR (1979) Functional role of serotonergic neuromodulation in Aplysia. Fed Proc 38:2095-2102.
53. Laurienti PJ, Blankenship JE (1997) Serotonergic modulation of a voltage-gated calcium current in parapodial swim muscle from Aplysia brasiliana. J Neurophysiol 77:496-502.
54. Li XC, Giot JF, Kühl D, Hen R, Kandel ER (1995) Cloning and characterization of two related serotonergic receptors from the brain and the reproductive system of Aplysia that activate phospholipase C. J Neurosci 15:7585-7591.
55. Lickey ME, Wozniak JA, Block GD, Hudson DJ, Augter GK (1977) The consequences of eye removal for the circadian rhythm of behavioral activity in Aplysia. J Comp Physiol 118:121-143.
56. Liebeswar G, Goldman JE, Koester J, Mayeri E (1975) Neural control of circulation in Aplysia III. Neurotransmitters. J Neurophysiol 38:767-779.
57. Livingstone MS, Harris-Warrick RM, Kravitz EA (1980) Serotonin and octopamine produce opposite postures in lobsters. Science 208:76-79.
58. Longley RD, Longley AJ (1986) Serotonin immunoreactivity of neurons in the gastropod Aplysia californica. J Neurobiol 17:339-358.
59. Mackey S, Carew TJ (1983) Locomotion in Aplysia: triggering by serotonin and modulation by bag cell extract. J Neurosci 3:1469-1477.
60. Malyshev A, Bravarenko N, Balaban P (1997) Dependence of synaptic facilitation postsynaptically induced in snail neurones on season and serotonin level. NeuroReport 8:1179-1182.
61. Mangan PS, Curran GA, Hurney CA, Friesen WO (1994) Modulation of swimming behavior in the medicinal leech. III. Control of cellular properties in motor neurons by serotonin. J Comp Physiol [A] 175:709-722.
62. Manseau F, Sossin WS, Castellucci VF (1998) Long-term changes in excitability induced by protein kinase C activation in Aplysia sensory neurons. J Neurophysiol 79:1210-1218.
63. Marder E, Hooper SL, Siwicki KK (1986) Modulatory action and distribution of the neuropeptide proctolin in the crustacean stomatogastric nervous system. J Comp Neurol 243:454-467.
64. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91:927-938.
65. McCarty R, Gold PE (1981) Plasma catecholamines: effects of footshock level and hormonal modulators of memory storage. Horm Behav 15:168-182.
66. McGaugh JL, Cahill L, Roozendaal B (1996) Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci USA 93:13508-13514.
67. McPherson DR, Blankenship JE (1991) Neuronal control of swimming in Aplysia brasiliana. III. Serotonergic modulatory neurons. J Neurophysiol 66:1366-1379.
68. McPherson DR, Blankenship JE (1992) Neuronal modulation of foot and body-wall contractions in Aplysia californica. J Neurophysiol 7:23-28.
69. Milner B, Squire LR, Kandel ER (1998) Cognitive neuroscience and the study of memory. Neuron 20:445-468.
70. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation inAplysia. Science 234:1249-1254.
71. Moore RY, Klein DC (1974) Visual pathways and the central neural control of a circadian rhythm in pineal serotonin N-acetyltransferase activity. Brain Res 71:17-33.
72. Mulloney B, Acevedo L, Bradbury A (1987) Modulation of the crayfish swimmeret rhythm by octopamine and the neuropeptide proctolin. J Neurophysiol 58:584-597.
73. Nusbaum MP, Marder E (1988) A neuronal role for a crustacean red pigment concentrating hormone-like peptide: neuromodulation of the pyloric rhythm in the crab, Cancer borealis. J Exp Biol 135:165-181.
74. O'Leary FA, Byrne JH, Cleary LJ (1995) Long-term structural remodeling in Aplysia sensory neurons requires de novo protein synthesis during a critical time period. J Neurosci 15:3519-3525.
75. Ono JK, McCaman RE (1984) Immunocyotchemical localization and direct assays of serotonin-containing neurons in Aplysia. Neuroscience 11:549-560.
76. Ottaviani E, Cossarizza A (1990) Immunocytochemical evidence of vertebrate bioactive peptide-like molecules in the immuno cell types of the freshwater snail Planorbarius corneus (L.) (gastropoda, pulmonata). FEBS Lett 267:250-252.
77. Ottaviani E, Franchini A, Fontanili P (1992) The presence of immunoreactive vertebrate bioactive peptide substances in hemocytes of the freshwater snail Viviparus ater. Cell Mol Neurobiol 12:455-462.
78. Palovcik RA, Basberg BA, Ram JL (1982) Behavioral state changes induced in Pleurobranchaea and Aplysia by serotonin. Behav Neural Biol 35:383-394.
79. Parsons DW, Pinsker HM (1989) Swimming in Aplysia brasiliana: behavioral and cellular effects of serotonin. J Neurophysiol 62:1163-1176.
80. Peretz B, Estes J (1974) Histology and histochemistry of the peripheral neural plexus in the Aplysia gill. J Neurobiol 5:3-19.
81. Pinsker HM, Hening WA, Carew TJ, Kandel ER (1973) Long-term sensitization of a defensive withdrawal reflex in Aplysia. Science 182:1039-1042.
82. Poon M (1980) Induction of swimming in lamprey by L-DOPA and amino acids. J Comp Physiol 136:337-344.
83. Raju U, Koumenis C, Nunez-Regueiro M, Eskin A (1991) Alteration of the phase and period of a circadian oscillator by a reversible transcription inhibitor. Science 253:673-675.
84. Rathouz MM, Kirk MD (1988) Localization of catecholamines in the buccal ganglia of Aplysia californica. Brain Res 458:170-175.
85. Rosen SC, Kupfermann I, Goldstein RS, Weiss KR (1983) Lesion of a serotonergic modulatory neuron inAplysia produces a specific defect in feeding behavior. Brain Res 260:151-155.
86. 2+ movements in anterior aorta and ventricle of Aplysia. J Neurophysiol 51:361-374.
87. Schacher S, Montarolo P, Kandel ER (1990) Selective short- and long-term effects of serotonin, small cardioactive peptide, and tetanic stimulation on sensorimotor synapses of Aplysia in culture. J Neurosci 10:3286-3294.
88. Scholz KP, Byrne JH (1987) Long-term sensitization in Aplysia: Biophysical correlates in tail sensory neurons. Science 235:685-687.
89. Schwartz JH, Castellucci VF, Kandel ER (1971) Functioning of identified neurons and synapses in abdominal ganglion of Aplysia in absence of protein synthesis. J Neurophysiol 34:939-953.
90. Schwarz TL, Lee GM-H, Siwicki KK, Standaert DG, Kravitz EA (1984) Proctolin in the lobster: the distribution, release and chemical characterization of a likely neurohormone. J Neurosci 4:1300-1312.
91. Skelton ME, Koester J (1992) The morphology, innervation and neural control of the anterior arterial system of Aplysia californica. J Comp Physiol [A] 171:141-155.
92. Sokal RR, Rohlf FJ (1995) Biometry. New York: Freeman.
93. Stefano GB, Zhao X, Bailey D, Metlay M, Leung MK (1989) High affinity dopamine binding to mouse thymocytes and Mytilus edulis (bivalvia) hemocytes. J Neuroimmunol 21:67-74.
94. Strumwasser F (1973) Neural and humoral factors in the temporal organization of behavior. Physiologist 16:9-42.
95. Takahashi JS, Nelson DE, Eskin A (1988) Immunocytochemical localization of serotonergic fibers innervating the ocular circadian system of Aplysia. Neuroscience 28:139-147.
96. Tritt SH, Lowe IP, Byrne JH (1983) A modification of the glyoxylic acid induced histofluorescence technique for demonstration of catecholamines and serotonin in tissues of Aplysia californica. Brain Res 259:159-162.
97. Trudeau LE, Castellucci VF (1993) Sensitization of the gill and siphon withdrawal reflex of Aplysia: multiple sites of change in the neuronal network. J Neurophysiol 70:1210-1220.
98. Tuersley M, McCrohan C (1987) Serotonergic modulation of patterned motor output in Lymnaea stagnalis. J Exp Biol 135:473-486.
99. Walters ET, Byrne JH, Carew TJ, Kandel ER (1983) Mechanoafferent neurons innervating tail of Aplysia. H. Modulation by sensitizing stimulation. J Neurophysiol 50:1543-59.
100. Weiss KR, Cohen J, Kupfermann I (1975) Potentiation of muscle contraction: a possible modulatory function of an identified serotonergic cell in Aplysia. Brain Res 99:381-386.
101. Weiss KR, Cohen JL, Kupfermann I (1978) Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) inAplysia. J Neurophysiol 41:181-203.
102. Willard A (1981) Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J Neurosci 1:936-944.
103. Xu Y, Pieroni JP, Cleary LJ, Byrne JH (1995) Modulation of an inhibitory interneuron in the neural circuitry for the tail withdrawal reflex of Aplysia. J Neurophysiol 73:1313-1318.
104. Zhang F, Endo S, Cleary LJ, Eskin A, Byrne JH (1997) Role of transforming growth factor-β in long-term synaptic facilitation in Aplysia. Science 275:1318-1320.
105. Zhang ZS, Fang B, Marshak DW, Byrne JH, Cleary LJ (1991) Serotoninergic varicosities make synaptic contacts with pleural sensory neurons of Aplysia. J Comp Neurol 311:259-270.