Ecologically relevant stressors modify long-term memory formation in a model system

Behavioural Brain Research

Volumn 214, Issue 1, 2010, Pages 18-24

  Lukowiak, Ken ^a   Orr, Mike ^a   de Caigny, Pascaline ^a   Lukowiak, Kai S ^a   Rosenegger, David ^a   Han, Jae Il ^a   Dalesman, Sarah ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Long term memory; Lymnaea; Model system; Neuronal plasticity; Stress

Indexed keywords

CALCIUM ION; CALCIUM;

ADAPTIVE BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BREATHING; COGNITION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROWDING; ENVIRONMENTAL FACTOR; ENVIRONMENTAL STRESS; HERITABILITY; LEARNING; LONG TERM MEMORY; LYMNAEA; MEMORY CONSOLIDATION; NONHUMAN; PREDATOR PREY INTERACTION; PRIORITY JOURNAL; RECALL; STRAIN DIFFERENCE; ANIMAL; ANIMAL MODEL; CROWDING (AREA); DRUG EFFECTS; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; INSTRUMENTAL CONDITIONING; MEMORY; MENTAL STRESS; ODOR; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PSYCHOLOGY; SPECIES DIFFERENCE;

ANIMALS; CALCIUM; CONDITIONING, OPERANT; CROWDING; ECOLOGICAL AND ENVIRONMENTAL PHENOMENA; LYMNAEA; MEMORY; MODELS, ANIMAL; RESPIRATION; SMELL; SPECIES SPECIFICITY; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 77955055321     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.05.011     Document Type: Article

References (62)

1. Bacon F. The new organon 1620, Bobbs-Merrill, New York, [1620/1960]. F.H. Anderson (Ed.).
2. Yerkes R.M., Dodson J.D. The relation of strength of stimulus to rapidity of habit-formation. J Comp Neurol Psychol 1908, 18:459-482.
3. Shors T.J. Learning during stressful times. Learn Mem 2004, 11:137-144.
4. Selye H. The evolution of the stress concept. Am Sci 1973, 61:692-699.
5. McEwen B., Sapolsky R. Stress and cognitive function. Curr Opin Neurobiol 1996, 5:205-216.
6. Lukowiak K., Martens K., Rosenegger D., Browning K., de Caigny P., Orr M. The perception of stress alters adaptive behavious in Lymnaea stagnalis. J Exp Biol 2008, 211:1747-1756.
7. de Quervain D.J.F., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
8. Bowman R.E., Beck K.D., Luine V.N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 2003, 43:48-59.
9. Cahill L., Gorski L., Le K. Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding. Learn Mem 2003, 10:270-274.
10. Joels M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cogn Sci 2006, 10:152-158.
11. Hebb D.O. The Organization of Behavior 1949, Wiley, New York.
12. Lewis D.J. Psychobiology of active and inactive memory. Psychol Bull 1979, 86:1054-1083.
13. Kim J., Diamond D. The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 2002, 3:453-463.
14. Lukowiak K., Fras M., Smyth K., Wong C., Hittel K. Reconsolidation and memory infidelity in Lymnaea. Neurobiol Learn Mem 2007, 87:547-560.
15. Yehuda R., LeDoux J. Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 2007, 56:19-32.
16. Benjamin P.R., Staras K., Kemenes G. A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn Mem 2000, 7:124-131.
17. Parvez K., Rosenegger D., Martens K., Orr M., Lukowiak K. Learning at a snail's pace. Can J Neurol Sci 2006, 33:347-356.
18. Lukowiak K., Ringseis E., Spencer G., Wildering W., Syed N. Operant conditioning of aerial respiratory behaviour in Lymnaea stagnalis. J Exp Biol 1996, 199:683-691.
19. Syed N.I., Bulloch A.G., Lukowiak K. In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 1990, 250:282-285.
20. Syed N.I., Ridgway R.L., Lukowiak K., Bulloch A.G.M. Transplantation and functional integration of an identified respiratory interneuron in Lymnaea stagnalis. Neuron 1992, 8:767-774.
21. Lukowiak K., Cotter R., Westly J., Ringseis E., Spencer G. Long-term memory of an operantly conditioned respiratory behaviour pattern in Lymnaea stagnalis. J Exp Biol 1998, 201:877-882.
22. Lukowiak K., Haque Z., Spencer G., Varshney N., Sangha S., Syed N. Long-term memory survives nerve injury and subsequent regeneration process. Learn Mem 2003, 10:44-54.
23. Lukowiak K., Sangha S., McComb C., Varshney N., Rosenegger D., Sadamoto H., et al. Associative learning and memory in Lymnaea stagnalis: how well do they remember?. J Exp Biol 2003, 206:2097-2103.
24. Lukowiak K., Adatia A., Krygier D., Syed N. Operant conditioning in Lymnaea: evidence for intermediate and long-term memory. Learn Mem 2000, 7:140-150.
25. Sangha S., Scheibenstock A., McComb C., Lukowiak K. Intermediate and long-term memories of associative learning are differentially affected by transcription vs translation blockers in Lymnaea. J Exp Biol 2003, 206:1605-1613.
26. Sangha S., Morrow R., Smyth K., Cooke R., Lukowiak K. Cooling blocks ITM and LTM formation and preserves memory. Neurobiol Learn Mem 2003, 80:130-139.
27. Scheibenstock A., Krygier D., Haque Z., Syed S., Lukowiak K. The soma of RPeD1 must be present for LTM formation of associative learning in Lymnaea. J Neurophysiol 2002, 88:1584-1591.
28. Sangha S., Scheibenstock A., Lukowiak K. Reconsolidation of a long- term memory in Lymnaea requires new protein and RNA synthesis and the soma of RPeD1. J Neurosci 2003, 23:8034-8040.
29. Sangha S., Scheibenstock A., Morrow R., Lukowiak K. Extinction requires new RNA and protein synthesis and the soma of the cell RPeD1 in Lymnaea stagnalis. J Neurosci 2003, 23:9842-9851.
30. Sangha S., Scheibenstock A., Martens K., Varshney N., Cooke R., Lukowiak K. Impairing forgetting by preventing new learning and memory. Behav Neurosci 2005, 119:787-796.
31. McComb C., Rosenegger D., Varshney N., Kwok H.-Y., Lukowiak K. Operant conditioning of an in vitro CNS-pneumostome preparation of Lymnaea. Neurobiol Learn Mem 2005, 84:9-24.
32. Lattal K.M., Radulovic J., Lukowiak K. Extinction: does it or doesn't it? The requirement of altered gene activity and new protein synthesis. Biol Psychiatry 2006, 60:344-351.
33. Orr M., El-Bekai M., Lui M., Watson K., Lukowiak K. Predator detection in Lymnaea. J Exp Biol 2007, 210:4150-4158.
34. Boranic M., Poljak-Blazi M. Effect of the crowding stress on hemopoietic colony formation in mice. Exp Hematol 1983, 11:873-877.
35. Holt S. Staying alive in adversity: transcriptome dynamics in the stress-resistant dauer larva. Funct Integr Genom 2006, 6:285-299.
36. Colton H. Some effects of environment on the growth of Lymnaea columella (Say). Proc Natl Acad Sci USA 1908, 60:410-448.
37. Crabb E. Growth of a pond snail. Lymnaea stagnalis appressa, as indicated by increase in shell-size. Biol Bull 1929, 56:41-63.
38. Forbes G., Crampton H. The effects of population density upon growth and size in Lymnaea palustris. Biol Bull 1942, 83:283-289.
39. Noland L., Carriker M. Observations on the biology of the snail Lymnaea stagnalis appressa during twenty generations in laboratory culture. Am Midl Nat 1946, 36:467-493.
40. Orr M., Lukowiak K. Electrophysiological and behavioural evidence demonstrating that predator detection alters adaptive behaviours in the snail Lymnaea. J Neurosci 2008, 28:2726-2734.
41. Orr M., Hittel K., Lukowiak K. Comparing memory-forming capabilities between laboratory-reared and wild Lymnaea. J Exp Biol 2008, 211:2807-2816.
42. Orr M., Hittel K., Lukowiak K. 'Different strokes for different folks': geographically isolated strains of Lymnaea stagnalis only respond to sympatric predators and have different memory forming capabilities. J Exp Biol 2009, 212:2237-2247.
43. Orr M., Hittel K., Lukowiak K.S., Han J., Lukowiak K. Differences in LTM-forming capability between geographically different strains of Alberta Lymnaea stagnalis are maintained whether they are trained in the lab or in the wild. J Exp Biol 2009, 212:3911-3918.
44. Haney J., Lukowiak K. Context learning and the effect of context on memory retrieval in Lymnaea. Learn Mem 2001, 8:35-43.
45. McGaugh J. Memory-a century of consolidation. Science 2000, 287(14):248-251.
46. Diamond D., Fleshner M., Ingersoll N., Rose G. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 1996, 110:661-672.
47. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 2002, 78:578-595.
48. Woodson J., Macintosh D., Fleshner M., Diamond D. Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learn Mem 2003, 10:326-336.
49. Voronezhskaya E., Khabarova M., Nezlin L. Apical sensory neurons mediate developmental retardation induced by conspecific environmental stimuli in freshwater pulmonate snails. Development 2004, 131:3671-3680.
50. deCaigny P., Lukowiak K. Crowding, an environmental stressor, blocks long-term memory formation in Lymnaea. J Exp Biol 2008, 211:2678-2688.
51. deCaigny P., Lukowiak K. A clash of stressors and LTM formation. Commun Integr Biol 2009, 2:1-3.
52. Boycott A.E. The habitats of fresh-water Mollusca in Britain. J Anim Ecol 1936, 5:116-186.
53. Rundle S.D., Spicer J.I., Coleman R.A., Vosper J., Soane J. Environmental calcium modifies induced defences in snails. Proc R Soc B 2004, 271:S67-S70.
54. Jeziorski A., Yan N.D., Paterson A.M., DeSellas A.M., Turner M.A., Jeffries D.S., et al. The widespread threat of calcium decline in fresh waters. Science 2008, 322:1374-1377.
55. Dalesman S., Lukowiak K. Effect of acute exposure to low environmental calcium on respiration and locomotion in Lymnaea stagnalis (L.). J Exp Biol 2010, 213:1470-1471.
56. Macan T.T. Ecology of fresh-water Mollusca in the English Lake District. J Anim Ecol 1950, 19:124-146.
57. Greenaway P. Calcium regulation in the freshwater mollusc. Limnaea stagnalis (L.) (Gastropoda: Pulmonata): 1. The effect of internal and external calcium concentration. J Exp Biol 1971, 54:199-214.
58. - uptake in the pulmonate freshwater snail Lymnaea stagnalis. Comp Biochem Phys A 1987, 87:671-675.
59. Grosell M., Brix K.V. High net calcium uptake explains the hypersensitivity of the freshwater pulmonate snail. Lymnaea stagnalis, to chronic lead exposure. Aquat Toxicol 2009, 91:302-311.
60. Dewith N.D. Evidence for independent regulation of specific ions in hemolymph of Lymnaea stagnalis (L). Proc Kon Ned Akad Wet C 1977, 80:144-157.
61. Piggott H., Dussart G. Egg-laying and associated behavioural responses of Lymnaea peregra (Müller) and Lymnaea stagnalis (L.) to calcium in their environment. Malacologia 1995, 37:13-21.
62. Mery F., Kawecki T.J. An operating cost of learning in Drosophila melanogaster. Anim Behav 2004, 68:589-598.