Stressful stimuli modulate memory formation in Lymnaea stagnalis

Neurobiology of Learning and Memory

Volumn 87, Issue 3, 2007, Pages 391-403

  Martens, Kara R ^a   Caigny, Pascaline De ^a   Parvez, Kashif ^a   Amarell, Martin ^a   Wong, Carolyn ^a   Lukowiak, Ken ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Invertebrate; Learning; Long term memory; Lymnaea stagnalis; Mollusk; Operant training; Stress

Indexed keywords

POTASSIUM CHLORIDE; QUININE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; INSTRUMENTAL CONDITIONING; LYMNAEA; MEMORY; NEUROMODULATION; NONHUMAN; PHYSICAL STRESS; PROTEIN SYNTHESIS; REINFORCEMENT; STIMULUS RESPONSE; STRESS; STRESS STRAIN RELATIONSHIP; TRAINING; WORKING MEMORY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AVOIDANCE LEARNING; CONDITIONING, OPERANT; GANGLIA, INVERTEBRATE; LYMNAEA; NEURONS; REINFORCEMENT (PSYCHOLOGY); RETENTION (PSYCHOLOGY); STRESS;

EID: 33846341147     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2006.10.005     Document Type: Article

References (54)

1. Andrew RJ., and Savage H. Appetitive learning using visual conditioned stimuli in the pond snail, lymnaea. Neurobiology of Learning and Memory 73 (2000) 258-273
2. Bailey CH., Bartsch D., and Kandel ER. Toward a molecular definition of long-term memory storage. Proceedings of the National Academy of Sciences of the United States of America 93 (1996) 13445-13452
3. Benjamin PR., Staras K., and Kemenes G. A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learning & Memory 7 (2000) 124-131
4. Bikson M., Id Bihi R., Vreugdenhil M., Kohling R., Fox JE., and Jefferys JG. Quinine suppresses extracellular potassium transients and ictal epileptiform activity without decreasing neuronal excitability in vitro. Neuroscience 115 (2002) 251-261
5. Cahill L., Gorski L., and Le K. Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learning & Memory 10 (2003) 270-274
6. Diamond DM., Park CR., Heman KL., and Rose GM. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 9 (1999) 542-552
7. El Hage W., Griebel G., and Belzung C. Long-term impaired memory following predatory stress in mice. Physiology & Behavior 87 (2006) 45-50
8. Feng ZP., Klumperman J., Lukowiak K., and Syed NI. In vitro synaptogenesis between the somata of identified Lymnaea neurons requires protein synthesis but not extrinsic growth factors or substrate adhesion molecules. The Journal of Neuroscience 17 (1997) 7839-7849
9. Frenkel L., Maldonado H., and Delorenzi A. Retrieval improvement is induced by water shortage through angiotensin II. Neurobiology of Learning and Memory 83 (2005) 173-177
10. Fulton D., Kemenes I., Andrew RJ., and Benjamin PR. A single time-window for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning. The European Journal of Neuroscience 21 (2005) 1347-1358
11. Gisquet-Verrier P., Botreau F., Venero C., and Sandi C. Exposure to retrieval cues improves retention performance and induces changes in ACTH and corticosterone release. Psychoneuroendocrinology 29 (2004) 529-556
12. Gordon WC., and Spear NE. Effect of reactivation of a previously acquired memory on the interaction between memories in the rat. Journal of Experimental Psychology 99 (1973) 349-355
13. Gulpinar MA., and Yegen BC. The physiology of learning and memory: role of peptides and stress. Current Protein & Peptide Science 5 (2004) 457-473
14. Haney J., and Lukowiak K. Context learning and the effect of context on memory retrieval in Lymnaea. Learning & Memory 8 (2001) 35-43
15. Hazzalin C.A., Panse R.L., Cano E., and Mahadevan L.C. Anisomycin selectively desensitizes signalling components involved in stress kinase activation and fos and jun induction. Molecular and Cellular Biology 18 (1998) 1844-1854
16. Het S., Ramlow G., and Wolf OT. A meta-analytic review of the effects of acute cortisol administration on human memory. Psychoneuroendocrinology 30 (2005) 771-784
17. Izquierdo I., Dalmaz C., Dias RD., and Godoy MG. Memory facilitation by post-training and pretest ACTH, epinephrine, and vasopressin administration: two separate effects. Behavioral Neuroscience 102 (1988) 803-806
18. Izquierdo LA., Barros DM., Medina JH., and Izquierdo I. Stress hormones enhance retrieval of fear conditioning acquired either one day or many months before. Behavioural Pharmacology 13 (2002) 203-213
19. Kemenes G., and Benjamin PR. Appetitive learning in snails shows characteristics of conditioning in vertebrates. Brain Research 489 (1989) 163-166
20. Kim JJ., and Diamond DM. The stressed hippocampus, synaptic plasticity and lost memories. Nature Reviews. Neuroscience 3 (2002) 453-462
21. Kim JJ., Koo JW., Lee HJ., and Han JS. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. The Journal of Neuroscience 25 (2005) 1532-1539
22. Kojima S., Hosono T., Fujito Y., and Ito E. Optical detection of neuromodulatory effects of conditioned taste aversion in the pond snail Lymnaea stagnalis. Journal of Neurobiology 49 (2001) 118-128
23. Kojima S., Nanakamura H., Nagayama S., Fujito Y., and Ito E. Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning. Neuroscience Letters 230 (1997) 179-182
24. Kojima S., Kobayashi S., Yamanaka M., Sadamoto H., Nakamura H., Fujito Y., et al. Sensory preconditioning for feeding response in the pond snail, Lymnaea stagnalis. Brain Research 808 (1998) 113-115
25. Kotani S., Hasegawa J., Meng H., Suzuki T., Sato K., Sakakibara M., et al. Hyperpolarizing shift by quinine in the steady-state inactivation curve of delayed rectifier-type potassium current in bullfrog sympathetic neurons. Neuroscience Letters 300 (2001) 87-90
26. Kuhlmann S., Piel M., and Wolf OT. Impaired memory retrieval after psychosocial stress in healthy young men. The Journal of Neuroscience 25 (2005) 2977-2982
27. Kuhlmann S., Kirschbaum C., and Wolf OT. Effects of oral cortisol treatment in healthy young women on memory retrieval of negative and neutral words. Neurobiology of Learning and Memory 83 (2005) 158-162
28. LaBar KS., and Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews. Neuroscience 7 (2006) 54-64
29. Lacoste A., Malham SK., Cueff A., Jalabert F., Gelebart F., and Poulet SA. Evidence for a form of adrenergic response to stress in the mollusc Crassostrea gigas. Journal of Experimental Biology 204 (2001) 1247-1255
30. Lin X., Chen S., and Tee D. Effects of quinine on the excitability and voltage-dependent currents of isolated spiral ganglion neurons in culture. Journal of Neurophysiology 79 (1998) 2503-2512
31. Lukowiak K., Adatia N., Krygier D., and Syed N. Operant conditioning in Lymnaea: evidence for intermediate- and long-term memory. Learning & Memory 7 (2000) 140-150
32. Lukowiak K., Ringseis E., Spencer G., Wildering W., and Syed N. Operant conditioning of aerial respiratory behaviour in Lymnaea stagnalis. The Journal of Experimental Biology 199 (1996) 683-691
33. Lukowiak K., Cotter R., Westly J., Ringseis E., and Spencer G. Long-term memory of an operantly conditioned respiratory behaviour pattern in Lymnaea stagnalis. The Journal of Experimental Biology 201 Pt 6 (1998) 877-882
34. McComb C., Sangha S., Qadry S., Yue J., Scheibenstock A., and Lukowiak K. Context extinction and associative learning in Lymnaea. Neurobiology of Learning and Memory 78 (2002) 23-34
35. Nikitin VP., and Kozyrev SA. Long-term synaptic facilitation in defensive behaviour command neurons in the snail during acquisition of sensitization depends on RNA synthesis. Neuroscience and Behavioral Physiology 35 (2005) 355-362
36. Parvez K., Stewart O., Sangha S., and Lukowiak K. Boosting intermediate-term into long-term memory. Journal of Experimental Biology 208 (2005) 1525-1536
37. Rodriguez Manzanares PA., Isoardi NA., Carrer HF., and Molina VA. Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. The Journal of Neuroscience 25 (2005) 8725-8734
38. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory 78 (2002) 578-595
39. Sangha S., Scheibenstock A., and Lukowiak K. Reconsolidation of a long-term memory in Lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. The Journal of Neuroscience 23 (2003) 8034-8040
40. Sangha S., Scheibenstock A., McComb C., and Lukowiak K. Intermediate and long-term memories of associative learning are differentially affected by transcription versus translation blockers in Lymnaea. Journal of Experimental Biology 206 (2003) 1605-1613
41. Sangha S., Scheibenstock A., Morrow R., and Lukowiak K. Extinction requires new RNA and protein synthesis and the soma of the cell right pedal dorsal 1 in Lymnaea stagnalis. The Journal of Neuroscience 23 (2003) 9842-9851
42. Sangha S., Scheibenstock A., Martens K., Varshney N., Cooke R., and Lukowiak K. Impairing forgetting by preventing new learning and memory. Behavioral Neuroscience 119 (2005) 787-796
43. Sangha S., Varshney N., Fras M., Smyth K., Rosenegger D., Parvez K., et al. Memory, reconsolidation and extinction in Lymnaea require the soma of RPeD1. Advances in Experimental Medicine and Biology 551 (2004) 311-318
44. Sara SJ. Retrieval and reconsolidation: toward a neurobiology of remembering. Learning & Memory 7 (2000) 73-84
45. Scheibenstock A., Krygier D., Haque Z., Syed N., and Lukowiak K. The Soma of RPeD1 must be present for long-term memory formation of associative learning in Lymnaea. Journal of Neurophysiology 88 (2002) 1584-1591
46. Shors TJ. Learning during stressful times. Learning & Memory 11 (2004) 137-144
47. Sonetti D., Peruzzi E., and Stefano GB. Endogenous morphine and ACTH association in neural tissues. Medical Science Monitor 11 (2005) MS22-MS30
48. Sugai R., Shiga H., Azami S., Watanabe T., Sadamoto H., Fujito Y., et al. Taste discrimination in conditioned taste aversion of the pond snail Lymnaea stagnalis. Journal of Experimental Biology 209 (2006) 826-833
49. Syed NI., Bulloch AG., and Lukowiak K. In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250 (1990) 282-285
50. Syed NI., Bulloch AG., and Lukowiak K. The respiratory central pattern generator (CPG) of Lymnaea reconstructed in vitro. Acta Biologica Hungarica 43 (1992) 409-419
51. Taylor BE., and Lukowiak K. The respiratory central pattern generator of Lymnaea: a model, measured and malleable. Respiration Physiology 122 (2000) 197-207
52. Thompson EA., and de Wied D. The relationship between the antidiuretic activity of rat eye plexus blood and passive avoidance behaviour. Physiology & Behavior 11 (1973) 377-380
53. Torocsik B., and Szeberenyi J. Anisomycin uses multiple mechanisms to stimulate mitogen-activated protein kinases and gene expression and to inhibit neuronal differentiation in PC12 phaeochromocytoma cells. The European Journal of Neuroscience 12 (2000) 527-532
54. Woodson JC., Macintosh D., Fleshner M., and Diamond DM. Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learning & Memory 10 (2003) 326-336