Artículo

La versión final de este artículo es de uso interno de la institución.
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The antennal lobe (AL) is the first olfactory center of the insect brain and is constituted of different functional units, the glomeruli. In the AL, odors are coded as spatiotemporal patterns of glomerular activity. In honeybees, olfactory learning during early adulthood modifies neural activity in the AL on a long-term scale and also enhances later memory retention. By means of behavioral experiments, we first verified that olfactory learning between the fifth and eighth day of adulthood induces better retention performances at a late adult stage than the same experience acquired before or after this period. We checked that the specificity of memory for the odorants used was improved. We then studied whether such early olfactory learning also induces long-term structural changes in the AL consistent with the formation of long-term olfactory memories. We also measured the volume of 15 identified glomeruli in the ALs of 17-day-old honeybees that either experienced an odor associated with sucrose solution between the fifth and eighth day of adulthood or were left untreated. We found that early olfactory experience induces glomerulus-selective increases in volume that were specific to the learned odor. By comparing our volumetric measures with calcium-imaging recordings from a previous study, performed in 17-day-old bees subjected to the same treatment and experimental conditions, we found that glomeruli that showed structural changes after early learning were those that exhibited a significant increase in neural activity. Our results make evident a correlation between structural and functional changes in the AL following early olfactory learning. © 2012 The Authors. European Journal of Neuroscience © 2012 Federation of European Neuroscience Societies and Blackwell Publishing Ltd.

Registro:

Documento: Artículo
Título:Early olfactory experience induces structural changes in the primary olfactory center of an insect brain
Autor:Arenas, A.; Giurfa, M.; Sandoz, J.C.; Hourcade, B.; Devaud, J.M.; Farina, W.M.
Filiación:Departamento de Biodiversidad y Biología Experimental, Grupo de Estudio de Insectos Sociales, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria (C1428EHA), Buenos Aires, Argentina
IFIBYNE, CONICET,3 Grupo de Estudio de Insectos Sociales, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria (C1428EHA), Buenos Aires, Argentina
UPS, Centre de Recherches sur la Cognition Animale, Université de Toulouse, s118 route de Narbonne, F-31062 Toulouse Cedex 9, France
CNRS, Centre de Recherches sur la Cognition Animale, 118 route de Narbonne, F-31062 Toulouse Cedex 9, France
CNRS, Laboratoire Evolution Génomes Spéciation, 1 avenue de la Terrasse, F-91198 Gif-sur-Yvette, France
Palabras clave:Antennal lobe; Associative learning; Early experiences; Honeybee; Memory retrieval; Olfaction; animal behavior; animal experiment; animal tissue; antenna (organ); article; controlled study; electroencephalogram; experiential learning; experimental animal; glomerular structure; honeybee; long term memory; memory consolidation; nonhuman; olfactory cortex; olfactory memory; olfactory nervous system; priority journal; volumetry; Animals; Animals, Newborn; Arthropod Antennae; Bees; Brain; Insects; Learning; Odors; Olfactory Pathways; Olfactory Perception
Año:2012
Volumen:35
Número:5
Página de inicio:682
Página de fin:690
DOI: http://dx.doi.org/10.1111/j.1460-9568.2012.07999.x
Título revista:European Journal of Neuroscience
Título revista abreviado:Eur. J. Neurosci.
ISSN:0953816X
CODEN:EJONE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0953816X_v35_n5_p682_Arenas

Referencias:

  • Arenas, A., Farina, W.F., Age and rearing environment interact in the retention of early olfactory memories in honey bees (2008) J. Comp. Physiol. A., 194, pp. 629-640
  • Arenas, A., Fernández, V.M., Farina, W.M., Floral odor learning within the hive affects honeybees' foraging decisions (2007) Naturwissenschaften, 94, pp. 218-222
  • Arenas, A., Fernández, V.M., Farina, W.M., Floral scents experienced within the colony affect long-term foraging preferences in honeybees (2008) Apidologie, 39, pp. 714-722
  • Arenas, A., Giurfa, M., Farina, W.M., Sandoz, J.C., Early olfactory experience modifies neural activity in the antennal lobe of a social insect at the adult stage (2009) Eur. J. Neurosci., 30, pp. 1498-1508
  • Arenas, A., Fernández, V.M., Farina, W.M., Associative learning during early adulthood enhances later memory retention in honey bees (2009) PLoS ONE, 4, pp. e8046
  • Ashraf, S.I., McLoon, A.L., Sclarsic, S.M., Kunes, S., Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila (2006) Cell, 124, pp. 191-205
  • Barth, M., Heisenberg, M., Vision affects mushroom bodies and central complex in Drosophila melanogaster (1997) Learn. Mem., 4, pp. 219-229
  • Bitterman, M.E., Menzel, R., Fietz, A., Schaefer, S., Classical conditioning of proboscis extension in honey bees (1983) J. Comp. Psychol., 97, p. 107
  • Carman, H.M., Booze, R.M., Mactutus, C.F., Long-term retention of spatial navigation by preweanling rats (2002) Dev. Psychol., 40, pp. 68-77
  • Cummings, D.M., Brunjes, P.C., The effects of variable periods of functional deprivation on olfactory bulb development in rats (1997) Exp. Neurol., 148, pp. 360-366
  • Deisig, N., Giurfa, M., Lachnit, H., Sandoz, J.C., Neural representation of olfactory mixtures in the honey bee antennal lobe (2006) Eur. J. Neurosci., 24, pp. 1161-1174
  • Deisig, N., Giurfa, M., Sandoz, J.C., Antennal lobe processing increases separability of odor mixture representations in the honey bee (2010) J. Neurophysiol., 103, pp. 2185-2194
  • Devaud, J.M., Acebes, A., Ferrús, A., Odor exposure causes central adaptation and morphological changes in selected olfactory glomeruli in Drosophila (2001) J. Neurosci., 21, pp. 6274-6282
  • Devaud, J.M., Acebes, A., Ramaswami, M., Ferrús, A., Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age (2003) J. Neurobiol., 56, pp. 13-23
  • Faber, T., Joerges, J., Menzel, R., Associative learning modifies neural representations of odors in the insect brain (1999) Nat. Neurosci., 2, pp. 74-78
  • Farbman, A.I., Brunjes, P.C., Rentfro, L., Michas, J., Ritz, S., The effect of unilateral naris occlusion on cell dynamics in the developing rat olfactory epithelium (1988) J. Neurosci., 8, pp. 3290-3295
  • Galizia, C.G., Nägler, K., Hölldobler, B., Menzel, R., Odour coding is bilaterally symmetrical in the AL of honey bees (Apis mellifera) (1998) Eur. J. Neurosci., 10, pp. 2964-2974
  • Galizia, C.G., Sachse, S., Rappert, A., Menzel, R., The glomerular code for odor representation is species specific in the honey bee Apis mellifera (1999) Nat. Neurosci., 2, pp. 473-478
  • Gascuel, J., Masson, C., Influence of olfactory deprivation on synapse frequency in developing antennal lobe of the honeybee Apis mellifera (1987) Neurosci. Res. Commun., 1, pp. 173-180
  • Giurfa, M., Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well (2007) J. Comp. Physiol. A., 193, pp. 801-824
  • Giurfa, M., Núñez, J., Chittka, L., Menzel, R., Colour preferences of flower-naive honeybees (1995) J. Comp. Physiol. A., 177, pp. 247-259
  • Grünbaum, L., Müller, U., Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee (1998) J. Neurosci., 18, pp. 4384-4392
  • Heisenberg, M., Heusipp, M., Wanke, C., Structural plasticity in the Drosophila brain (1995) J. Neurosci., 15, pp. 1951-1960
  • Hourcade, B., Perisse, E., Devaud, J.M., Sandoz, J.C., Long-term memory shapes the primary olfactory center of an insect brain (2009) Learn. Mem., 16, pp. 607-615
  • Hubel, D.H., Wiesel, T.N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex (1962) J. Physiol., 160, pp. 106-154
  • Joerges, J., Küttner, A., Galizia, C.G., Menzel, R., Representations of odours and odour mixtures visualized in the honey bee brain (1997) Nature, 387, pp. 285-288
  • Keuroghlian, A.S., Knudsen, E.I., Adaptive auditory plasticity in developing and adult animals (2007) Prog. Neurobiol., 82, pp. 109-121
  • Lindauer, M., Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat (1952) Z. Vgl. Physiol., 34, pp. 299-345
  • Lorenz, K., Der Kumpan in der Umwelt des Vogels (1935) Zeitschrift für Ornithologie, 83, pp. 137-213
  • Manrique, T., Molero, A., Candido, A., Gallo, M., Early learning failure impairs adult learning in rats (2005) Dev. Psychobiol., 46, pp. 340-349
  • Masson, C., Arnold, G., Ontogeny, maturation and plasticity of the olfactory system in the worker bee (1984) J. Insect Physiol., 30, pp. 7-14
  • Masson, C., Arnold, G., Organization and plasticity of the olfactory system of the honey bee, Apis mellifera (1987) Neurobiology and Behavior of Honey Bee, p. 281. , In Menzel, R. & Mercer, A. (Eds), Springer Verlag, Berlin, Heidelberg
  • Menzel, R., Learning in honey bees in an ecological and behavioral context (1985) Experimental Behavioral Ecology and Sociobiology, pp. 55-74. , In Hölldobler, B. & Lindauer, M. (Eds), Gustav Fischer Verlag, New York
  • Menzel, R., Memory dynamics in the honeybee (1999) J. Comp. Physiol. A., 185, pp. 323-340
  • Müller, U., Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees (2000) Neuron, 27, pp. 159-168
  • Phan, M.L., Pytte, C.L., Vicario, D.S., Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 1088-1093
  • Quinn, G., Keough, M., (2002) Experimental Design and Data Analysis for Biologists, , Cambridge University Press, Cambridge
  • Rath, L., Galizia, G., Szsyszka, P., Multiple memory traces after associative learning in the honey bee antennal lobe (2011) Eur. J. Neurosci., 34, pp. 352-360
  • Rösch, G.A., Untersuchungen über die Arbeitsteilung im Bienenstaat (1925) Z. Vgl. Physiol., 2, pp. 571-631
  • Sachse, S., Galizia, C.G., The role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study (2002) J. Neurophysiol., 87, pp. 1106-1117
  • Sachse, S., Rappert, A., Galizia, C.G., The spatial representation of chemical structures in the AL of honey bees: steps towards the olfactory code (1999) Eur. J. Neurosci., 11, pp. 3970-3982
  • Sachse, S., Rueckert, E., Keller, A., Okada, R., Tanaka, N.K., Ito, K., Vosshall, L.B., Activity-dependent plasticity in an olfactory circuit (2007) Neuron, 56, pp. 838-850
  • Sandoz, J.C., Galizia, C.G., Menzel, R., Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honey bee antennal lobes (2003) Neuroscience, 120, pp. 1137-1148
  • Schäble, S., Poeggel, G., Braun, K., Gruss, M., Long-term consequences of early experience on adult avoidance learning in female rats: role of the dopaminergic system (2007) Neurobiol. Learn. Mem., 87, pp. 109-122
  • Schmidt, U., Eckert, M., The influence of early odour experience on the neural response of the olfactory bulb in laboratory mice (1988) J. Comp. Physiol. A., 163, pp. 771-776
  • Seeley, T.D., Adaptive significance of the age polytheism schedule in honey bee colonies (1982) Behav. Ecol. Sociobiol., 11, pp. 287-293
  • Sokal, R.R., Rohlf, F.J., (1995) Biometry: The Principles and Practice of Statistics in Biological Research, , 3rd Edn. W. H. Freeman and Co., New York 715
  • Stieb, S.M., Hellwig, A., Wehner, R., Rössler, W., Visual experience affects both behavioral and neuronal aspects in the individual life history of the desert ant Cataglyphis fortis (2011) Dev. Neurobiol, , [Epub ahead of print]
  • Strausfeld, N.J., Organization of the honey bee mushroom body: representation of the calyx within the vertical and g lobes (2002) J. Comp. Neurol., 450, pp. 4-33
  • Suh, G.S., Wong, A.M., Hergarden, A.C., Wang, J.W., Simon, A.F., Benzer, S., Axel, R., Anderson, D.J., A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila (2004) Nature, 431, pp. 854-859
  • Takeda, K., Classical conditioned response in the honey bee (1961) J. Insect Physiol., 6, pp. 168-179
  • Winnington, A., Napper, R.M., Mercer, A.R., Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee (1996) J. Comp. Neurol., 365, pp. 479-490
  • Yu, D., Ponomarev, A., Davis, R.L., Altered representation of the spatial code for odors after olfactory classical conditioning: memory trace formation by synaptic recruitment (2004) Neuron, 42, pp. 437-449

Citas:

---------- APA ----------
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. European Journal of Neuroscience, 35(5), 682-690.
http://dx.doi.org/10.1111/j.1460-9568.2012.07999.x
---------- CHICAGO ----------
Arenas, A., Giurfa, M., Sandoz, J.C., Hourcade, B., Devaud, J.M., Farina, W.M. "Early olfactory experience induces structural changes in the primary olfactory center of an insect brain" . European Journal of Neuroscience 35, no. 5 (2012) : 682-690.
http://dx.doi.org/10.1111/j.1460-9568.2012.07999.x
---------- MLA ----------
Arenas, A., Giurfa, M., Sandoz, J.C., Hourcade, B., Devaud, J.M., Farina, W.M. "Early olfactory experience induces structural changes in the primary olfactory center of an insect brain" . European Journal of Neuroscience, vol. 35, no. 5, 2012, pp. 682-690.
http://dx.doi.org/10.1111/j.1460-9568.2012.07999.x
---------- VANCOUVER ----------
Arenas, A., Giurfa, M., Sandoz, J.C., Hourcade, B., Devaud, J.M., Farina, W.M. Early olfactory experience induces structural changes in the primary olfactory center of an insect brain. Eur. J. Neurosci. 2012;35(5):682-690.
http://dx.doi.org/10.1111/j.1460-9568.2012.07999.x