Using local anaesthetics to block neuronal activity and map specific learning tasks to the mushroom bodies of an insect brain

European Journal of Neuroscience

Volumn 26, Issue 11, 2007, Pages 3193-3206

  Devaud, Jean Marc ^a   Blunk, Aline ^b   Podufall, Jasmin ^b   Giurfa, Martin ^a   Grünewald, Bernd ^b  

^a CNRS   (France)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Anaesthetic mechanisms; Insects; Olfactory learning; Patch clamp

Indexed keywords

LIDOCAINE; PROCAINE; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ANESTHESIA INDUCTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; HONEYBEE; LEARNING; MUSHROOM BODY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; TASK PERFORMANCE; WHOLE CELL;

ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; BEES; BEHAVIOR, ANIMAL; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; LEARNING; LIDOCAINE; MEMBRANE POTENTIALS; MUSHROOM BODIES; NEURONS; PATCH-CLAMP TECHNIQUES; PROCAINE; TIME FACTORS;

EID: 36249027513     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05904.x     Document Type: Article

References (78)

1. Anwyl, R. (1977) The effect of foreign cations, pH and pharmacological agents on the ionic permeability of an excitatory glutamate synapse. J. Physiol., 273, 389 404.
2. Bast, T., Zhang, W.N. Feldon, J. (2003) Dorsal hippocampus and classical fear conditioning to tone and context in rats: effects of local NMDA-receptor blockade and stimulation. Hippocampus, 13, 657 675.
3. deBelle, J.S. Heisenberg, M. (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science, 263, 692 695.
4. Bischoff, U., Brau, M.E., Vogel, W., Hempelmann, G. Olschewski, A. (2003) Local anaesthetics block hyperpolarization-activated inward current in rat small dorsal root ganglion neurones. Br. J. Pharmacol., 139, 1273 1280.
5. Bitterman, M.E., Menzel, R., Fietz, A. Schäfer, S. (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psych., 97, 107 119.
6. Bohbot, V., Otahal, P., Liu, Z., Nadel, L. Bures, J. (1996) Electroconvulsive shock and lidocaine reveal rapid consolidation of spatial working memory in the water maze. Proc. Natl Acad. Sci. USA, 93, 4016 4019.
7. + channels in peripheral nerve. Anesth. Analg., 87, 885 889.
8. Cano-Lozano, V., Bonnard, E., Gauthier, M. Richard, D. (1996) Mecamylamine-induced impairment of acquisition and retrieval of olfactory conditioning in the honeybee. Behav. Brain Res., 81, 215 222.
9. Cano-Lozano, V., Armengaud, C. Gauthier, M. (2001) Memory impairment induced by cholinergic antagonists injected into the mushroom bodies of the honeybee. J. Comp. Physiol. [A], 187, 249 254.
10. Corcoran, K.A. Maren, S. (2001) Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J. Neurosci., 21, 1720 1726.
11. Corcoran, K.A. Maren, S. (2004) Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction. Learn. Mem., 11, 598 603.
12. Cuevas, J. Adams, D.J. (1994) Local anaesthetic blockade of neuronal nicotinic ACh receptor-channels in rat parasympathetic ganglion cells. Br. J. Pharmacol., 111, 663 672.
13. Daumas, S., Halley, H., Frances, B. Lassalle, J.M. (2005) Encoding, consolidation, and retrieval of contextual memory: differential involvement of dorsal CA3 and CAI hippocampal subregions. Learn. Mem., 2, 375 382.
14. Dubnau, J., Grady, L., Kitamoto, K. Tully, T. (2001) Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory. Nature, 411, 476 480.
15. Erber, J., Masuhr, T. Menzel, R. (1980) Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol. Entomol., 5, 343 358.
16. Faber, T. Menzel, R. (2001) Visualizing mushroom body response to a conditioned odor in honeybees. Naturwissenschaften, 88, 472 476.
17. Fatt, P. Katz, B. (1953) The electrical properties of crustacean muscle fibres. J. Physiol., 28, 171 204.
18. Franks, C.J., Pemberton, D., Vinogradova, I., Cook, A., Walker, R.J. Holden-Dye, L. (2002) Ionic basis of the resting membrane potential and action potential in the pharyngeal muscle of Caenorhabditis elegans. J. Neurophysiol., 87, 954 961.
19. Giurfa, M. (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr. Opin. Neurobiol., 13, 1 10.
20. Giurfa, M. (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A, 193, 801 824.
21. Griffin, A.L. Berry, S.D. (2004) Inactivation of the anterior cingulate cortex impairs extinction of rabbit jaw movement conditioning and prevents extinction-related inhibition of hippocampal activity. Learn. Mem., 11, 604 610.
22. 2+ currents in neurons of the honeybee olfactory pathway. J. Exp. Biol., 206, 117 129.
23. Hamill, O.P., Neher, E., Marty, A., Sakman, B. Sigworth, F.J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. Eur. J. Physiol., 391, 85 100.
24. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature, 366, 59 63.
25. Hammer, M. Menzel, R. (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem., 5, 146 156.
26. Heisenberg, M. (2003) Mushroom body memoir: from maps to models. Nat. Rev. Neurosci., 4, 266 275.
27. Heisenberg, M., Borst, A., Wagner, S. Byers, D. (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet., 2, 1 30.
28. Hille, B. (1966) Common mode of action of three agents that decrease the transient change in sodium permeability in nerves. Nature, 210, 1220 1222.
29. Hille, B. (2001) Classical mechanisms of block. Ion Channels of Excitable Membranes. Sinauer Associate, Sunderland, MA, pp. 503 536.
30. Keller, M., Perrin, G., Meurisse, M., Ferreira, G. Levy, F. (2004) Cortical and medial amygdala are both involved in the formation of olfactory offspring memory in sheep. Eur. J. Neurosci., 20, 3433 3441.
31. Kirschfeld, K. (1987) The action of volatile anesthetics on the resting and receptor potential in insect photoreceptors. Naturwissen, 74, 29.
32. Kirschfeld, K. (1988) The influence of general-anesthetics on neurons sensitive to motion in the visual-system of the fly. Naturwissen, 75, 468 470.
33. Kirschfeld, K. Baierrogowski, V. (1987) The neuronal basis of the anesthetic state - a comparative physiological approach. 1. The influence of anesthetics on the behavior of insects. Biol. Cybern., 55, 345 354.
34. Komai, H. McDowell, T.S. (2001) Local anesthetic inhibition of voltage-activated potassium currents in rat dorsal root ganglion neurons. Anesthesiology, 94, 1089 1095.
35. Komischke, B., Giurfa, M., Lachnit, H. Malun, D. (2002) Successive olfactory reversal learning in honeybees. Learn. Mem., 9, 122 129.
36. Komischke, B., Sandoz, J.-C., Lachnit, H. Giurfa, M. (2003) Non-elemental processing in olfactory discrimination tasks need bilateral input in honeybees. Behav. Brain Res., 145, 135 143.
37. Komischke, B., Sandoz, J.-C., Malun, D. Giurfa, M. (2005) Partial unilateral lesions of the mushroom bodies affect olfactory learning in honeybees Apis mellifera L. Eur. J. Neurosci., 21, 477 485.
38. Kreissl, S. Bicker, G. (1992) Dissociated neurons of the pupal honeybee brain in cell culture. J. Neurocytol., 21, 545 556.
39. Kuwabara, M. (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool., 13, 458 464.
40. Lachnit, H., Giurfa, M. Menzel, R. (2004) Odor processing in honeybees: is the whole equal to, more than, or different from the sum of its parts ? Adv. Study Behav., 34, 241 264.
41. Lapied, B., Grolleau, F. Sattelle, D.B. (2001) Indoxacarb, an oxadiazine insecticide, blocks insect neuronal sodium channels. Br. J. Pharmacol., 132, 587 595.
42. Leuwer, M., Haeseler, G., Hecker, H., Bufler, J., Dengler, R. Aronson, J.K. (2004) An improved model for the binding of lidocaine and structurally related local anaesthetics to fast-inactivated voltage-operated sodium channels, showing evidence of cooperativity. Br. J. Pharmacol., 141, 47 54.
43. Locatelli, F., Bundrock, G. Müller, U. (2005) Focal and temporal release of glutamate in the mushroom bodies improves olfactory memory in Apis mellifera. J. Neurosci., 25, 11614 11648.
44. Lunney, G.H. (1970) Using analysis of variance with a dichotomous dependent variable: an empirical study. J. Educat. Meas., 7, 263 269.
45. Malin, E.L. McGaugh, J.L. (2006) Differential involvement of the hippocampus, anterior cingulate cortex, and basolateral amygdala in memory for context and footshock. Proc. Natl Acad. Sci. USA, 103, 1959 1963.
46. Malun, D., Plath, N., Giurfa, M., Moseleit, A.D. Müller, U. (2002a) Hydroxyurea-induced partial mushroom body ablation in the honeybee Apis mellifera: volumetric analysis and quantitative protein determination. J. Neurobiol., 50, 31 44.
47. Malun, D., Giurfa, M., Galizia, C.G., Plath, N., Brandt, R., Gerber, B. Eisermann, B. (2002b) Hydroxyurea-induced partial mushroom body ablation does not affect acquisition and retention of olfactory differential conditioning in honeybees. J. Neurobiol., 53, 343 360.
48. Martin, C., Gervais, R., Messaoudi, B. Ravel, N. (2006) Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur. J. Neurosci., 23, 1801 1810.
49. Menzel, R. (1999) Memory dynamics in the honeybee. J. Comp. Physiol., 185, 323 340.
50. Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn. Mem., 8, 53 62.
51. Menzel, R., Erber, J. Masuhr, T. (1974) Learning and memory in the honeybee. In Barton Browne, L. (Ed.), Experimental Analysis of Insect Behaviour. Springer, Berlin, pp. 195 217.
52. Menzel, R. Giurfa, M. (2001) Cognitive architecture of a mini-brain: the honeybee. Trends Cogn. Sci., 5, 62 71.
53. Mobbs, P.G. (1982) The brain of the honeybee Apis mellifera I. The connections and spatial organization of the mushroom bodies. Philos. Trans. R. Soc. Lond. B Biol. Sci., 298, 309 354.
54. Müller, D., Staffeldt, D., Fiala, A. Menzel, R. (2003) Procaine impairs learning and memory consolidation in the honeybee. Brain Res., 977, 124 127.
55. Myers, K.M. Davis, M. (2002) Behavioral and neural analysis of extinction. Neuron, 14, 567 584.
56. Nishizawa, N., Shirasaki, T., Nakao, S., Matsuda, H. Shingu, K. (2002) The inhibition of the N-methyl-D-aspartate receptor channel by local anesthetics in mouse CA1 pyramidal neurons. Anesth. Analg., 94, 325 330.
57. +, and simulation. J. Neurophysiol., 81, 1749 1759.
58. Rajaram, S. Nash, H.A. (2004) A specific alteration in the electroretinogram of Drosophila melanogaster is induced by halothane and other volatile general anesthetics. Anesth. Analg., 98, 1705 1711.
59. Sandoz, J.-C. Menzel, R. (2001) Side-specificity of olfactory learning in the honeybee: generalization between odors and sides. Learn. Mem., 8, 286 294.
60. Schäfer, S., Rosenboom, H. Menzel, R. (1994) Ionic currents of Kenyon cells from the mushroom body of the honeybee. J. Neurosci., 14, 4600 4612.
61. Scholz, A. (2002) Mechanisms of (local) anaesthetics on voltage-gated sodium and other ion channels. Br. J. Anaesth., 89, 52 61.
62. Schwaerzel, M., Heisenberg, M. Zars, T. (2002) Extinction antagonizes olfactory memory at the subcellular level. Neuron, 35, 951 960.
63. Schwaerzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S. Heisenberg, M. (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci., 23, 10495 10502.
64. Scotto-Lomassesse, S., Strambi, C., Strambi, A., Aouane, A., Augier, R., Rougon, G. Cayre, M. (2003) Suppression of adult neurogenesis impairs olfactory learning and memory in an insect. J. Neurosci., 23, 9289 9296.
65. Sheets, M.F. Hanck, D.A. (2003) Molecular action of lidocaine on the voltage sensors of sodium channels. J. Gen. Physiol., 121, 163 175.
66. Stollhoff, N., Menzel, R. Eisenhardt, D. (2005) Spontaneous recovery from extinction depends on the reconsolidation of the acquisition memory in an appetitive learning paradigm in the honeybee (Apis mellifera). J. Neurosci., 25, 4485 4492.
67. Strausfeld, N.J., Hansen, L., Li, Y., Gomez, R.S. Ito, K. (1998) Evolution, discovery and interpretations of arthropod mushroom bodies. Learn. Mem., 5, 11 37.
68. Sugiyama, K. Muteki, T. (1994) Local anesthetics depress the calcium current of rat sensory neurons in culture. Anesthesiology, 80, 1369 1378.
69. van Swinderen, B. (2006) A succession of anesthetic endpoints in the Drosophila brain. J. Neurobiol., 66, 1195 1211.
70. Taylor, R.E. (1959) Effect of procaine on electrical properties of squid axon membrane. Am. J. Physiol., 196, 1071 1078.
71. Teixeira, C.M., Pomedli, S.R., Maei, H.R., Kee, N. Frankland, P.W. (2006) Involvement of the anterior cingulate cortex in the expression of remote spatial memory. J. Neurosci., 26, 7555 7564.
72. Theander, S., Fåhraeus, C.& Grampp, W. (1996) Analysis of leak current properties in the lobster stretch receptor neurone. Acta Physiol. Scand., 157, 493 509.
73. Uusitalo, R.O., Juusola, M. Weckstrom, M. (1995) Graded responses and spiking properties of identified first-order visual interneurons of the fly compound eye. J. Neurophysiol., 73, 1782 1792.
74. Washio, H. (1972) The ionic requirements for the initiation of action potentials in insect muscle fibers. J. Gen. Physiol., 59, 121 134.
75. Winters, B.D. Bussey, T.J. (2005) Transient inactivation of perirhinal cortex disrupts encoding, retrieval, and consolidation of object recognition memory. J. Neurosci., 25, 52 61.
76. Wolbarsht, M.L. Hanson, F.E. (1965) Electrical activity in the chemoreceptors of the blowfly. 3. Dendritic action potentials. J. Gen. Physiol., 48, 673 683.
77. Wüstenberg, D., Boytcheva, M., Grünewald, B., Byrne, J.H., Menzel, R. Baxter, D.A. (2004) Current- and voltage-clamp recordings and computer simulations of kenyon cells in honeybee. J. Neurophysiol., 92, 2589 2603.
78. Zar, J.H. (1999) Biostatistical Analysis, 4th Edn. Prentice Hall, Upper Saddle River, New Jersey, USA.