Odor memories regulate olfactory receptor expression in the sensory periphery

European Journal of Neuroscience

Volumn 39, Issue 10, 2014, Pages 1642-1654

  Claudianos, Charles ^a   Lim, Julianne ^a,b   Young, Melanie ^a   Yan, Shanzhi ^a   Cristino, Alexandre S ^a   Newcomb, Richard D ^c,d   Gunasekaran, Nivetha ^a   Reinhard, Judith ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c THE NEW ZEALAND INSTITUTE FOR PLANT AND FOOD RESEARCH LIMITED   (New Zealand)

^d UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Honeybee; Learning; Olfaction; Plasticity

Indexed keywords

OR109 PROTEIN; OR11 PROTEIN; OR150 PROTEIN; OR151 PROTEIN; OR152 PROTEIN; OR63 PROTEIN; OR81 PROTEIN; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; CALCIUM; INSECT PROTEIN; OLFACTORY RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA (ORGAN); APIS MELLIFERA; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BEE; CONDITIONING; FLUORESCENCE IMAGING; IMMUNOHISTOCHEMISTRY; LONG TERM MEMORY; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SMELLING; STIMULATION; WESTERN BLOTTING;

ANIMALS; ARTHROPOD ANTENNAE; BEES; BLOTTING, WESTERN; CALCIUM; CONDITIONING (PSYCHOLOGY); IMMUNOHISTOCHEMISTRY; INSECT PROTEINS; MEMORY, LONG-TERM; NEURONAL PLASTICITY; ODORS; OLFACTORY PERCEPTION; OLFACTORY RECEPTOR NEURONS; OPTICAL IMAGING; PHYSICAL STIMULATION; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ODORANT;

EID: 84900789509     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12539     Document Type: Article

References (64)

1. Anfora, G., Frasnelli, E., Maccagnani, B., Rogers, L.J. & Vallortigara, G. (2010) Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav. Brain Res., 206, 236-239.
2. Arenas, A., Giurfa, M., Sandoz, J.C., Hourcade, B., Devaud, J.M. & Farina, W.M. (2012) Early olfactory experience induces structural changes in the primary olfactory center of an insect brain. Eur. J. Neurosci., 35, 682-690.
3. Bhagavan, S. & Smith, B.H. (1997) Olfactory conditioning in the honey bee, Apis mellifera: effects of odor intensity. Physiol. Behav., 61, 107-117.
4. Biswas, S., Russell, R.J., Jackson, C.J., Vidovic, M., Ganeshina, O., Oakeshott, J.G. & Claudianos, C. (2008) Bridging the synaptic gap: neuroligins and neurexin I in Apis mellifera. PLoS ONE, 3, e3542.
5. Biswas, S., Reinhard, J., Oakeshott, J., Russell, R., Srinivasan, M.V. & Claudianos, C. (2010) Sensory regulation of neuroligins and neurexin I in the honeybee brain. PLoS ONE, 5, e9133.
6. Brockmann, A. & Bruckner, B. (1995) Projection pattern of poreplate sensory neurones in honey bee worker, Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morphol., 24, 405-411.
7. Carcaud, J., Hill, T., Giurfa, M. & Sandoz, J.C. (2012) Differential coding by two olfactory subsystems in the honeybee brain. J. Neurophysiol., 108, 1106-1121.
8. Chen, X., Yu, X., Cai, Y., Zheng, H., Yu, D., Liu, G., Zhou, Q., Hu, S. & Hu, F. (2010) Next-generation small RNA sequencing for microRNAs profiling in the honey bee Apis mellifera. Insect Mol. Biol., 19, 799-805.
9. Collins, A.M., Williams, V. & Evans, J.D. (2004) Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Insect Mol. Biol., 13, 141-146.
10. Danty, E., Briand, L., Michard-Vanhee, C., Perez, V., Arnold, G., Gaudemer, O., Huet, D., Huet, J.C., Ouali, C., Masson, C. & Pernollet, J.C. (1999) Cloning and expression of a queen pheromone-binding protein in the honeybee: an olfactory-specific, developmentally regulated protein. J. Neurosci., 19, 7468-7475.
11. De Groof, G., Gwinner, H., Steiger, S., Kempenaers, B. & Van der Linden, A. (2010) Neural correlates of behavioural olfactory sensitivity changes seasonally in European starlings. PLoS ONE, 5, e14337.
12. De Jong, R. & Pham-Delegue, M.H. (1991) Electroantennogram responses related to olfactory conditioning in the honey bee (Apis mellifera ligustica). J. Insect Physiol., 37, 319-324.
13. Deisig, N., Giurfa, M. & Sandoz, J.C. (2010) Antennal lobe processing increases separability of odor mixture representations in the honeybee. J. Neurophysiol., 103, 2185-2194.
14. Denker, M., Finke, R., Schaupp, F., Grun, S. & Menzel, R. (2010) Neural correlates of odor learning in the honeybee antennal lobe. Eur. J. Neurosci., 31, 119-133.
15. Eisenhardt, D. (2012) Extinction learning in honey bees. In Galizia, C.G., Eisenhardt, D. & Giurfa, M. (Eds), Honeybee Neurobiology and Behavior. Springer, New York, pp. 423-438.
16. Eisenhardt, D. & Menzel, R. (2007) Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiol. Learn. Mem., 87, 167-173.
17. Faber, T. & Menzel, R. (2001) Visualizing mushroom body response to a conditioned odor in honeybees. Naturwissenschaften, 88, 472-476.
18. Faber, T., Joerges, J. & Menzel, R. (1999) Associative learning modifies neural representations of odors in the insect brain. Nat. Neurosci., 2, 74-78.
19. Farris, S.M., Robinson, G.E. & Fahrbach, S.E. (2001) Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J. Neurosci., 21, 6395-6404.
20. Fernandez, P.C., Locatelli, F.F., Person-Rennell, N., Deleo, G. & Smith, B.H. (2009) Associative conditioning tunes transient dynamics of early olfactory processing. J. Neurosci., 29, 10191-10202.
21. Galizia, C.G. & Rossler, W. (2010) Parallel olfactory systems in insects: anatomy and function. Annu. Rev. Entomol., 55, 399-420.
22. 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.
23. Hallem, E.A. & Carlson, J.R. (2006) Coding of odors by a receptor repertoire. Cell, 125, 143-160.
24. Hallem, E.A., Ho, M.G. & Carlson, J.R. (2004) The molecular basis of odor coding in the Drosophila antenna. Cell, 117, 965-979.
25. Hourcade, B., Perisse, E., Devaud, J.M. & Sandoz, J.C. (2009) Long-term memory shapes the primary olfactory center of an insect brain. Learn. Memory, 16, 607-615.
26. Hourcade, B., Muenz, T.S., Sandoz, J.C., Rossler, W. & Devaud, J.M. (2010) Long-term memory leads to synaptic reorganization in the mushroom bodies: a memory trace in the insect brain? J. Neurosci., 30, 6461-6465.
27. Hu, A., Zhang, W. & Wang, Z. (2010) Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway. Proc. Natl. Acad. Sci. USA, 107, 10262-10267.
28. Joerges, J., Kuettner, A., Galizia, G. & Menzel, R. (1997) Representations of odours and odour mixtures visualized in the honeybee brain. Nature, 387, 285-288.
29. Kiely, A., Authier, A., Kralicek, A.V., Warr, C.G. & Newcomb, R.D. (2007) Functional analysis of a Drosophila melanogaster olfactory receptor expressed in Sf9 cells. J. Neurosci. Meth., 159, 189-194.
30. Kirschner, S., Kleineidam, C.J., Zube, C., Rybak, J., Grunewald, B. & Rossler, W. (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J. Comp. Neurol., 499, 933-952.
31. Knudsen, J., Eriksson, R., Gershenzon, J. & Stahl, B. (2006) Diversity and distribution of floral scent. Bot. Rev., 72, 1-120.
32. Lacher, V. (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren fuer Geruch, Kohlendioxid, Luftfeuchtigkeit und Temperatur auf den Antennen der Arbeitsbiene und der Drohne. Z. vergl. Physiol., 48, 587-623.
33. Letzkus, P., Ribi, W.A., Wood, J.T., Zhu, H., Zhang, S.W. & Srinivasan, M.V. (2006) Lateralization of olfaction in the honeybee Apis mellifera. Curr. Biol., 16, 1471-1476.
34. Lise, M.F. & El-Husseini, A. (2006) The neuroligin and neurexin families: from structure to function at the synapse. Cell. Mol. Life Sci., 63, 1833-1849.
35. Liu, F., Peng, W., Li, Z., Li, W., Li, L., Pan, J., Zhang, S., Miao, Y., Chen, S. & Su, S. (2012) Next-generation small RNA sequencing for microRNAs profiling in Apis mellifera: comparison between nurses and foragers. Insect Mol. Biol., 21, 297-303.
36. Lyko, F., Foret, S., Kucharski, R., Wolf, S., Falckenhayn, C. & Maleszka, R. (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol., 8, e1000506.
37. Menzel, R. (1999) Memory dynamics in the honeybee. J. Comp. Physiol. A., 185, 323-340.
38. Menzel, R. (2001) Searching for the memory trace in a mini-brain, the honeybee. Learn. Memory, 8, 53-62.
39. Menzel, R. (2012) The honeybee as a model for understanding the basis of cognition. Nat. Rev. Neurosci., 13, 758-768.
40. Menzel, R. & Muller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci., 19, 379-404.
41. Mercer, T.R., Dinger, M.E., Mariani, J., Kosik, K.S., Mehler, M.F. & Mattick, J.S. (2008) Noncoding RNAs in Long-Term Memory Formation. Neuroscientist, 14, 434-445.
42. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, e45.
43. Rath, L., Giovanni Galizia, C. & Szyszka, P. (2011) Multiple memory traces after associative learning in the honey bee antennal lobe. Eur. J. Neurosci., 34, 352-360.
44. Reinhard, J. & Claudianos, C. (2012) Molecular insights into honeybee brain plasticity. In Galizia, C.G., Eisenhardt, D. & Giurfa, M. (Eds), Honeybee Neurobiology and Behavior. Springer, New York, pp. 359-372.
45. Reinhard, J., Srinivasan, M.V., Guez, D. & Zhang, S.W. (2004a) Floral scents induce recall of navigational and visual memories in honeybees. J. Exp. Biol., 207, 4371-4381.
46. Reinhard, J., Srinivasan, M.V. & Zhang, S. (2004b) Olfaction: scent-triggered navigation in honeybees. Nature, 427, 411.
47. Reinhard, J., Srinivasan, M.V. & Zhang, S. (2006) Complex memories in honeybees: can there be more than two? J. Comp. Physiol. A., 192, 409-416.
48. Reinhard, J., Sinclair, M., Srinivasan, M.V. & Claudianos, C. (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS ONE, 5, e9110.
49. Rinker, D.C., Pitts, R.J., Zhou, X., Suh, E., Rokas, A. & Zwiebel, L.J. (2013) Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae. Proc. Natl. Acad. Sci. USA, 110, 8260-8265.
50. Robertson, H.M. & Wanner, K.W. (2006) The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res., 16, 1395-1403.
51. Rybak, J. & Menzel, R. (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J. Comp. Neurol., 334, 444-465.
52. Sachse, S. & Galizia, C.G. (2003) The coding of odour-intensity in the honeybee antennal lobe: local computation optimizes odour representation. Eur. J. Neurosci., 18, 2119-2132.
53. Sandoz, J.C. (2012) Olfactory plasticity. In Binder, M.D., Hirokawa, N. & Windhorst, U. (Eds), Encyclopedia of Neuroscience. Springer Verlag, Berlin, pp. 1-5.
54. Sandoz, J.C., Pham-Delegue, M.H., Renou, M. & Wadhams, L.J. (2001) Asymmetrical generalisation between pheromonal and floral odours in appetitive olfactory conditioning of the honey bee (Apis mellifera L.). J. Comp. Physiol. A., 187, 559-568.
55. Schneider, D. & Steinbrecht, R. (1968) Checklist of insect olfactory sensilla. Sym. Zool. S., 23, 279-297.
56. Sigg, D., Thompson, C.M. & Mercer, A.R. (1997) Activity-dependent changes to the brain and behavior of the honey bee, Apis mellifera (L.). J. Neurosci., 17, 7148-7156.
57. Stollhoff, N., Menzel, R. & Eisenhardt, D. (2008) One retrieval trial induces reconsolidation in an appetitive learning paradigm in honeybees (Apis mellifera). Neurobiol. Learn. Mem., 89, 419-425.
58. Szyszka, P., Demmler, C., Oemisch, M., Sommer, L., Biergans, S., Birnbach, B., Silbering, A.F. & Galizia, C.G. (2011) Mind the gap: olfactory trace conditioning in honeybees. J. Neurosci., 31, 7229-7239.
59. Wadhams, L.J., Blight, M.M., Kerguelen, V., Le Metayer, M., Marion-Poll, F., Masson, C., Pham-Delegue, M.H. & Woodcock, C.M. (1994) Discrimination of oilseed rape volatiles by honey bee: novel combined gas chromatographic-electrophysiological behavioral assay. J. Chem. Ecol., 20, 3221-3231.
60. Wanner, K.W., Nichols, A.S., Walden, K.K., Brockmann, A., Luetje, C.W. & Robertson, H.M. (2007) A honey bee odorant receptor for the queen substance 9-oxo-2-decenoic acid. Proc. Natl. Acad. Sci. USA, 104, 14383-14388.
61. Wilson, D.A., Best, A.R. & Sullivan, R.M. (2004) Plasticity in the olfactory system: lessons for the neurobiology of memory. Neuroscientist, 10, 513-524.
62. Winston, M.L. (1987) The Biology of the Honey Bee. Harvard University Press, Harvard.
63. Withers, G.S., Fahrbach, S.E. & Robinson, G.E. (1993) Selective neuroanatomical plasticity and division of labour in the honeybee. Nature, 364, 238-240.
64. Zhou, S., Stone, E.A., Mackay, T.F. & Anholt, R.R. (2009) Plasticity of the chemoreceptor repertoire in Drosophila melanogaster. PLoS Genet., 5, e1000681.