Low environmental calcium blocks long-term memory formation in a freshwater pulmonate snail

Neurobiology of Learning and Memory

Volumn 95, Issue 4, 2011, Pages 393-403

  Dalesman, Sarah ^a   Braun, Marvin H ^a   Lukowiak, Ken ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Environmental calcium; Learning; Long term memory; Lymnaea stagnalis; Pulmonate snail

Indexed keywords

ARTICLE; BREATHING; CALCIUM METABOLISM; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENVIRONMENTAL IMPACT; FRESHWATER ENVIRONMENT; GASTROPOD; INSTRUMENTAL CONDITIONING; INTERMEDIATE TERM MEMORY; LEARNING; LOCOMOTION; LONG TERM MEMORY; LYMNAEA STAGNALIS; MEMORY; MICROELECTRODE; NONHUMAN; PROTEIN SYNTHESIS; REARING; SNAIL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BEHAVIOR, ANIMAL; CALCIUM; CONDITIONING, OPERANT; ENVIRONMENT; MEMORY, LONG-TERM; NEURAL CONDUCTION; NEURONS; OXYGEN CONSUMPTION; RETENTION (PSYCHOLOGY); SNAILS; STRESS, PHYSIOLOGICAL;

EID: 79955468140     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2010.11.017     Document Type: Article

References (64)

1. Alkon D.L., Sakakibara M. Calcium activates and inactivates a photoreceptor soma potassium current. Biophysical Journal 1985, 48:983-995.
2. + currents mediates retention of a learned association. Behavioral and Neural Biology 1985, 44:278-300.
3. Benjamin P.R., Staras K., Kemenes G. A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learning & Memory 2000, 7:124-131.
4. Boycott A.E. The habitats of fresh-water Mollusca in Britain. Journal of Animal Ecology 1936, 5:116-186.
5. Brembs B. Operant conditioning in invertebrates. Current Opinions in Neurobiology 2003, 13:710-717.
6. Dalesman S., Lukowiak K. Effect of acute exposure to low environmental calcium alters respiration and locomotion of Lymnaea stagnalis (L.). Journal of Experimental Biology 2010, 213:1471-1476.
7. Dalesman S., Rundle S.D. Cohabitation enhances the avoidance response to heterospecific alarm cues in a freshwater snail. Animal Behaviour 2010, 79:173-177.
8. Dalesman S., Rundle S.D., Bilton D.T., Cotton P.A. Phylogenetic relatedness and ecological interactions determine anti-predator behaviour. Ecology 2007, 88:2462-2467.
9. Dalesman S., Rundle S.D., Coleman R.A., Cotton P.A. Cue association and antipredator behaviour in a pulmonate snail, Lymnaea stagnalis. Animal Behaviour 2006, 71:789-797.
10. Dalesman S., Rundle S.D., Cotton P.A. Predator regime influences innate anti-predator behaviour in the freshwater gastropod Lymnaea stagnalis. Freshwater Biology 2007, 52:2134-2140.
11. Dalesman S., Rundle S.D., Cotton P.A. Developmental plasticity compensates for selected low levels of behavioural avoidance in a freshwater snail. Animal Behaviour 2009, 78:987-991.
12. De Caigny P., Lukowiak K. Crowding, an environmental stressor, blocks long-term memory formation in Lymnaea. Journal of Experimental Biology 2008, 211:2678-2688.
13. Dewith N.D. Evidence for independent regulation of specific ions in hemolymph of Lymnaea stagnalis (L). Proceedings of the Koninklijke Nederlandse Akademie Van Wetenschappen Series C-Biological and Medical Sciences 1977, 80:144-157.
14. - uptake in the pulmonate freshwater snail Lymnaea stagnalis. Comparative Biochemistry and Physiology A - Physiology 1987, 87:671-675.
15. Frost W. Memory traces: Snails reveal a novel storage mechanism. Current Biology 2006, 16:R640-R641.
16. Glass N., Darby P. The effect of calcium and pH on Florida apple snail, Pomacea paludosa (Gastropoda: Ampullariidae), shell growth and crush weight. Aquatic Ecology 2009, 43:1085-1093.
17. Greenaway P. Calcium regulation in the freshwater mollusc, Limnaea stagnalis (L.) (Gastropoda: Pulmonata): 1. The effect of internal and external calcium concentration. Journal of Experimental Biology 1971, 54:199-214.
18. Grosell M., Brix K.V. High net calcium uptake explains the hypersensitivity of the freshwater pulmonate snail, Lymnaea stagnalis, to chronic lead exposure. Aquatic Toxicology 2009, 91:302-311.
19. Il-Han J., Janes T., Lukowiak K. The role of serotonin in the enhancement of long-term memory resulting from predator detection in Lymnaea. Journal of Experimental Biology 2010, 213:3603-3614.
20. 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.
21. Kandel E.R. The molecular biology of memory storage: A dialogue between genes and synapses. Science 2001, 294:1030-1038.
22. Keller W.B. Limnology in northeastern Ontario: From acidification to multiple stressors. Canadian Journal of Fisheries and Aquatic Sciences 2009, 66:1189-1198.
23. Lewis D.B., Magnuson J.J. Intraspecific gastopod shell strength variation among north temperate lakes. Canadian Journal of Fisheries and Aquatic Sciences 1999, 56:1687-1695.
24. Lukowiak K., Adatia N., Krygier D., Syed N. Operant conditioning in Lymnaea: Evidence for intermediate- and long-term memory. Learning & Memory 2000, 7:140-150.
25. Lukowiak K., Cotter R., Westly J., Ringseis E., Spencer G., Syed N. Long-term memory of an operantly conditioned respiratory behaviour pattern in Lymnaea stagnalis. Journal of Experimental Biology 1998, 201:877-882.
26. Lukowiak K., Martens K., Rosenegger D., Browning K., de Caigny P., Orr M. The perception of stress alters adaptive behaviours in Lymnaea stagnalis. Journal of Experimental Biology 2008, 211:1747-1756.
27. Lukowiak K., Orr M., de Caigny P., Lukowiak K.S., Rosenegger D., Han J.I., et al. Ecologically relevant stressors modify long-term memory formation in a model system. Behavioural Brain Research 2010, 214:18-24.
28. Lukowiak K., Ringseis E., Spencer G., Wildering W., Syed N. Operant conditioning of aerial respiratory behaviour in Lymnaea stagnalis. Journal of Experimental Biology 1996, 199:683-691.
29. 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?. Journal of Experimental Biology 2003, 206:2097-2103.
30. Macan T.T. Ecology of fresh-water Mollusca in the English Lake District. Journal of Animal Ecology 1950, 19:124-146.
31. Madsen H. Effect of calcium concentration on growth and egg laying of Helisoma duryi, Bulinus africanus and Bulinus truncatus (Gastropoda: Planorbidae). Journal of Applied Ecology 1987, 24:823-836.
32. Magee J.C., Johnston D. Plasticity of dendritic function. Current Opinion in Neurobiology 2005, 15:334-342.
33. Marder E., Abbott L.â.F., Turrigiano G.G., Liu Z., Golowasch J. Memory from the dynamics of intrinsic membrane currents. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:13481-13486.
34. Martens K., Amarell M., Parvez K., Hittel K., De Caigny P., Ito E., et al. One-trial conditioning of aerial respiratory behaviour in Lymnaea stagnalis. Neurobiology of Learning and Memory 2007, 88:232-242.
35. McComb C., Meems R., Syed N., Lukowiak K. Electrophysiological differences in the CPG aerial respiratory behavior between juvenile and adult Lymnaea. Journal of Neurophysiology 2003, 90:983-992.
36. McComb C., Rosenegger D., Varshney N., Kwok H.Y., Lukowiak K. Operant conditioning of an in vitro CNS-pneumostome preparation of Lymnaea. Neurobiology of Learning and Memory 2005, 84:9-24.
37. McKillop W., Harrison A. Distribution of aquatic gastopods across the interface between the Canadian sheild and limestone formations. Canadian Journal of Zoology 1972, 50:1433-1445.
38. Milner B., Squire L.R., Kandel E.R. Cognitive neuroscience and the study of memory. Neuron 1998, 20:445-468.
39. Nikitin E.S., Kiss T., Staras K., O'Shea M., Benjamin P.R., Kemenes G. Persistent sodium current is a target for cAMP-induced neuronal plasticity in a state-setting modulatory interneuron. Journal of Neurophysiology 2006, 95:453-463.
40. Nikitin E.S., Vavoulis D.V., Kemenes I., Marra V., Pirger Z., Michel M., et al. Persistent sodium current is a nonsynaptic substrate for long-term associative memory. Current Biology 2008, 18:1221-1226.
41. Orr M.V., El-Bekai M., Lui M., Watson K., Lukowiak K. Predator detection in Lymnaea stagnalis. Journal of Experimental Biology 2007, 210:4150-4158.
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. Journal of Experimental Biology 2009, 212:2237-2247.
43. Orr M.V., Lukowiak K. Electrophysiological and behavioral evidence demonstrating that predator detection alters adaptive behaviors in the snail Lymnaea. Journal of Neuroscience 2008, 28:2726-2734.
44. Parvez K., Rosenegger D., Orr M., Martens K., Lukowiak K. Canadian association of neurosciences review: Learning at a snail's pace. Canadian Journal of Neurological Sciences 2006, 33:347-356.
45. Parvez K., Stewart O., Sangha S., Lukowiak K. Boosting intermediate-term into long-term memory. Journal of Experimental Biology 2005, 208:1525-1536.
46. 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.
47. Rosenegger D., Wright C., Lukowiak K. A quantitative proteomic analysis of long-term memory. Molecular Brain 2010, 3:9.
48. Rundle S.D., Spicer J.I., Coleman R.A., Vosper J., Soane J. Environmental calcium modifies induced defences in snails. Proceedings of the Royal Society of London Series B - Biological Sciences 2004, 271:S67-S70.
49. Sangha S., Morrow R., Smyth K., Cooke R., Lukowiak K. Cooling blocks ITM and LTM formation and preserves memory. Neurobiology of Learning and Memory 2003, 80:130-139.
50. Sangha S., Scheibenstock A., Lukowiak K. Reconsolidation of a long-term memory in Lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. Journal of Neuroscience 2003, 23:8034-8040.
51. Sangha S., Scheibenstock A., McComb C., Lukowiak K. Intermediate and long-term memories of associative learning are differentially affected by transcription versus translation blockers in Lymnaea. The Journal of Experimental Biology 2003, 206:1605-1613.
52. Scheibenstock A., Krygier D., Haque Z., Syed N., Lukowiak K. The soma of RPeD1 must be present for long-term memory formation of associative learning in Lymnaea. Journal of Neurophysiology 2002, 88:1584-1591.
53. Shors T.J. Learning during stressful times. Learning & Memory 2004, 11:137-144.
54. Spencer G.E., Kazmi M.H., Syed N.I., Lukowiak K. Changes in the activity of a CPG neuron after the reinforcement of an operantly conditioned behavior in Lymnaea. Journal of Neurophysiology 2002, 88:1915-1923.
55. Spencer G.E., Syed N.I., Lukowiak K. Neural changes after operant conditioning of the aerial respiratory behavior in Lymnaea stagnalis. Journal of Neuroscience 1999, 19:1836-1843.
56. Sunada H., Horikoshi T., Lukowiak K., Sakakibara M. Increase in excitability of RPeD11 results in memory enhancement of juvenile and adult Lymnaea stagnalis by predator-induced stress. Neurobiology of Learning and Memory 2010, 94:269-277.
57. Syed N.I., Bulloch A.G.M., Lukowiak K. Invitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 1990, 250:282-285.
58. Syed N.I., Bulloch A.G.M., Lukowiak K. The respiratory central pattern generator (CPG) of Lymnaea reconstructed invitro. Acta Biologica Hungarica 1992, 409:419.
59. 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.
60. Van Der Borght O., Van Puymbroek S. Calcium metabolism in a freshwater mollusc: Quantitative importance of water and food supply for calcium during growth. Nature 1966, 210:791-793.
61. Williams N.V. Studies on aquatic pulmonate snails in central Africa 1. Field distribution in relation to water chemistry. Malacologia 1970, 10:153-164.
62. Young J.O. A laboratory study, using 45Ca tracer, on the source of calcium during growth in two freshwater species of Gastropoda. Proceedings of the Malacoglogical Society of London 1975, 41:439-445.
63. Young J.O. Preliminary field and laboratory studies on the survival and spawning of several species of gastropoda in calcium-poor and calcium-rich waters. Proceedings of the Malacoglogical Society of London 1975, 41:429-437.
64. Zalizniak L., Kefford B.J., Nugegoda D. Effects of different ionic compositions on survival and growth of Physa acuta. Aquatic Ecology 2009, 43:145-156.