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Abstract:

Cognitive experiences during the early stages of life play an important role in shaping future behavior. Behavioral and neural long-term changes after early sensory and associative experiences have been recently reported in the honeybee. This invertebrate is an excellent model for assessing the role of precocious experiences on later behavior due to its extraordinarily tuned division of labor based on age polyethism. These studies are mainly focused on the role and importance of experiences occurred during the first days of the adult lifespan, their impact on foraging decisions, and their contribution to coordinate food gathering. Odor-rewarded experiences during the first days of honeybee adulthood alter the responsiveness to sucrose, making young hive bees more sensitive to assess gustatory features about the nectar brought back to the hive and affecting the dynamic of the food transfers and the propagation of food-related information within the colony. Early olfactory experiences lead to stable and long-term associative memories that can be successfully recalled after many days, even at foraging ages. Also they improve memorizing of new associative learning events later in life. The establishment of early memories promotes stable reorganization of the olfactory circuits inducing structural and functional changes in the antennal lobe (AL). Early rewarded experiences have relevant consequences at the social level too, biasing dance and trophallaxis partner choice and affecting recruitment. Here, we revised recent results in bees' physiology, behavior, and sociobiology to depict how the early experiences affect their cognition abilities and neural-related circuits. © 2013 Arenas, Ramírez, Balbuena and Farina.

Registro:

Documento: Artículo
Título:Behavioral and neural plasticity caused by early social experiences: The case of the honeybee
Autor:Arenas, A.; Ramírez, G.P.; Balbuena, M.S.; Farina, W.M.
Filiación:Grupo de Estudio de Insectos Sociales, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, IFIBYNE-CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Department of Behavioral Physiology and Sociobiology, Bioze ntrum, University of Würzburg, Würzburg, 97074, Germany
Palabras clave:Associative learning; Behavior; Early experiences; Honeybee; Olfaction; Plasticity; article; associative memory; cognition; experience; foraging behavior; honeybee; long term memory; memory consolidation; nerve cell plasticity; nonhuman; odor; olfactory memory; recall; reinforcement; reward; smelling; social life; state dependent learning; taste
Año:2013
Volumen:4 AUG
DOI: http://dx.doi.org/10.3389/fphys.2013.00041
Título revista:Frontiers in Physiology
Título revista abreviado:Front. Physiol.
ISSN:1664042X
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_1664042X_v4AUG_n_p_Arenas.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_1664042X_v4AUG_n_p_Arenas

Referencias:

  • Arenas, A., Farina, W.M., Age and rearing environment interact in the retention of early olfactory memories in honeybees (2008) J. Comp. Physiol, A194, 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., Fernández, V.M., Farina, W.M., Associative learning during early adulthood enhances later memory retention in honeybees (2009) PLoS ONE, 4, pp. e8046. , doi: 10.1371/journal.pone.0008046
  • 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., 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 (2012) Eur. J. Neurosci., 35, pp. 682-690
  • Balbuena, M.S., Arenas, A., Farina, W.M., Floral scents learned inside the honeybee hive have a long-lasting effect on recruitment (2012) Anim. Behav., 84, pp. 77-83
  • Behrends, A., Scheiner, R., Evidence for associative learning in newly emerged honey bees (Apis mellifera) (2009) Anim. Cogn., 12, pp. 249-255
  • Biesmejer, J.C., Seeley, T.D., The use of waggle dance information by honey bees throughout their foraging careers (2005) Behav. Ecol. Sociobiol., 59, pp. 133-142
  • Bitterman, M.E., Menzel, R., Fietz, A., Schäfer, S., Classical conditioning of proboscis extension in honeybees (Apis mellifera) (1983) J. Comp. Psychol., 97, pp. 107-119
  • Brown, S.M., Napper, R.M., Mercer, A.R., Foraging experience, glomerulus volume, and synapse number: a stereological study of the honey bee antennal lobe (2004) J. Neurobiol., 60, pp. 40-50
  • Carlsson, M.A., Galizia, C.G., Hansson, B.S., Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae) (2002) Chem. Senses, 27, pp. 231-244
  • Cornwell-Jones, C.A., Velasquez, P., Wright, E.L., McGaugh, J.L., Early experience influences adult retention of aversively motivated tasks in normal, but not DSP4-treated rats (1988) Dev. Psychobiol., 21, pp. 177-185
  • Cramer, C.P., Pfister, J.P., Haig, K.A., Experience during suckling alters later spatial learning (1988) Dev. Psychobiol., 21, pp. 1-24
  • Díaz, P.C., Grüter, C., Farina, W.M., Floral scents affect the distribution of hive bees around dancers (2007) Behav. Ecol. Sociobiol., 61, pp. 1589-1597
  • Dukas, R., Evolutionary biology of insect learning (2008) Annu. Rev. Entomol., 53, pp. 145-160
  • Dyer, F.C., The biology of the dance language (2002) Annu. Rev. Entomol., 47, pp. 917-949
  • Faber, T., Joerges, J., Menzel, R., Associative learning modifies neural representations of odors in the insect brain (1999) Nat. Neurosci., 2, pp. 74-78
  • Fahrbach, S.E., Structure of the mushroom bodies of the insect brain (2006) Annu. Rev. Entomol., 51, pp. 209-232
  • Farina, W.M., Grüter, C., Arenas, A., Olfactory information transfer during recruitment in honey bees," (2012) Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel, pp. 89-102. , eds C. G. Galizia, D. Eisenhardt, and M Giurfa (Dordrecht; Heidelberg; London; New York: Springer)
  • Farina, W.M., Grüter, C., Díaz, P.C., Social learning of floral odours inside the honeybee hive (2005) Proc. Biol. Sci., 272, pp. 1923-1928
  • Farris, S.M., Robinson, G.E., Fahrbach, S.E., Experience -and age- related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee (2001) J. Neurosci., 21, pp. 6395-6404
  • Friedrich, R.W., Korsching, S.I., Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging (1997) Neuron, 18, pp. 737-752
  • Galizia, C.G., Franke, T., Menzel, R., Sandoz, J.C., Optical imaging of concealed brain activity using a gold mirror in honeybees (2012) J. Insect Physiol., 55, pp. 743-749
  • Galizia, C.G., Nägler, K., Hölldobler, B., Menzel, R., Odour coding is bilaterally symmetrical in the AL of honeybees (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 honeybee Apis mellifera (1999) Nat. Neurosci., 2, pp. 473-478
  • Garelick, M.G., Storm, D.R., The relationship between memory retrieval and memory extinction (2005) Proc. Natl. Acad. Sci., 102, pp. 9091-9092. , U. S. A
  • Gerber, B., Geberzahn, N., Hellstern, F., Klein, J., Kowalksy, O., Wüstenberg, D., Honey bees transfer olfactory memories established during flower visits to a proboscis extension paradigm in the laboratory (1996) Anim. Behav., 52, pp. 1079-1085
  • 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., Sandoz, Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees (2012) Learn. Mem., 19, pp. 54-66
  • Gerber, B., Geberzahn, N., Hellstern, F., Klein, J., Kowalksy, O., Wustenberg, D., Honey bees transfer olfactory memories established during flower visits to a proboscis extension paradigm in the laboratory (1996) Anim. Behav., 52, pp. 1079-1085
  • 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
  • Grüter, C., Acosta, L.E., Farina, W.M., Propagation of olfactory information within the honeybee hive (2006) Behav. Ecol. Sociobiol., 60, pp. 707-715
  • Grüter, C., Balbuena, M.S., Farina, W.M., Informational conflicts created by the waggle dance (2008) Proc. Biol. Sci., 275, pp. 1321-1327
  • Grüter, C., Balbuena, M.S., Farina, W.M., Retention of long-term memories in different age groups of honeybee (Apis mellifera) workers (2009) Ins. Soc., 56, pp. 385-387
  • Grüter, C., Farina, W.M., The honeybee waggle dance: can we follow the steps (2009) Trends Ecol Evol, 24, pp. 242-247
  • Gschanes, A., Eggenreich, U., Windisch, M., Crailsheim, K., Early postnatal stimulation influences passive avoidance behaviour of adult rats. Behav (1998) Brain Res, 93, pp. 91-98
  • 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
  • Ichikawa, N., Sasaki, M., Importance of social stimuli for the development of learning capability in honeybee (2003) Appl. Entomol. Zool., 38, pp. 203-209
  • Joerges, J., Küttner, A., Galizia, C.G., Menzel, R., Representations of odors and odor mixtures visualized in the honeybee brain (1997) Nature, 387, pp. 285-287
  • Kearns, C.A., Inouye, D.W., Techniques for Pollination Biologists (1993), Boulder, CO: University Press of Colorado; Kuwabara, M., Bildung Des Bedingten Reflexes Von Pavlovs Typus Bei Der Honigbiene (1957) Apis Mellifera. Fukuoka: Biologisches Institut, Naturwissenschaftliche Fakultät, Universität Kyushu.
  • Lindauer, M., Ein Beitrag zur Frage der Arbeitsteinlung im Bienenstaat (1952) Z vergl Physiol, 34, pp. 299-345
  • Lorenz, K., Der Kumpan in der Umwelt des Vogels. Zeitschrift für Ornithologie 83 (1935) 137-213, pp. 289-413
  • Maleszka, R., Helliwell, P., Effect of juvenile hormone on short-term olfactory memory in young honeybees (Apis mellifera) Horm (2001) Behav, 40, pp. 403-408
  • Martinez, A., Farina, W.M., Honeybees modify gustatory responsiveness after receiving nectar from foragers within the hive (2008) Behav. Ecol. Sociobiol., 62, pp. 529-535
  • 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 honeybee, Apis mellifera (1987) Neurobiology and Behavior of Honeybee, pp. 280-295. , eds R. Menzel and A. Mercer (Berlin Heidelberg: Springer Verlag)
  • Masson, C., Pham-Delègue, M.H., Fonta, C., Gascuel, J., Arnold, G., Nicolas, G., Recent advances in the concept of adaptation to natural odour signals in the honeybee Apis mellifera L (1993) Apidologie, 24, pp. 169-194
  • Matthews, K., Robbins, T.W., Early experience as a determinant of adult behavioral responses to reward: the effects of repeated maternal separation in the rat (2003) Neurosci. Biobehav. Rev., 27, pp. 45-55
  • Menzel, R., Memory dynamics in the honeybee (1999) J. Comp. Physiol. A, 185, pp. 323-340
  • Menzel, R., The honeybee as a model for understanding the basis of cognition (2012) Nature, 13, pp. 758-768
  • Michener, C.D., (1974) The Social Behavior of Bees: A Comparative Study, , Cambridge: Harvard University Press
  • Morgan, S.M., Butz Huryn, V.M., Downes, S.R., Mercer, A.R., The effects of queenlessness on the maturation of the honey bee olfactory system. Behav (1998) Brain Res, 91, pp. 115-126
  • Müller, U., Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees (2000) Neuron, 27, pp. 159-168
  • Neal, W.R., The effect of environmental deprivation on speech and language development: Implications for child care workers (1972) Child Care Q, 1, pp. 157-172
  • Page, R.E., Erber, J., Fondrk, M.K., The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L (1998) J. Comp. Physiol., A 182, pp. 489-500
  • Pankiw, T., Page Jr, R.E., The effect of genotype, age, sex, and caste on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L (1999) J. Comp. Physiol., A 185, pp. 207-213
  • Pankiw, T., Nelson, M., Page, R.E., Fondrk, M.K., The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality (2004) Behav. Ecol. Sociobiol., 55, pp. 286-292
  • Pankiw, T., Waddington, K.D., Pager Jr, R.E., Modulation of sucrose response thresholds in honey bees (Apis mellifera L.): influence of genotype, feeding, and foraging experience (2001) J. Comp. Physiol., A 187, pp. 293-301
  • Pryce, C.R., Feldon, J., Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms (2003) Neurosci. Biobehav. Rev., 27, pp. 57-71
  • Ramírez, G.P., Martínez, A.S., Fernández, V.M., Corti Bielsa, G., Farina, W.M., The influence of gustatory and olfactory experiences on responsiveness to reward in the honeybee (2010) PLoS ONE, 5, pp. e13498. , doi: 10.1371/journal.pone.0013498
  • 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
  • Ray, S., Ferneyhough, B., The effects of age on olfactory learning and memory in the honey bee Apis mellifera (1997) Learn. Mem., 8, pp. 789-793
  • Riley, J.R., Greggers, U., Smith, A.D., Reynolds, D.R., Menzel, R., The flight paths of honeybees recruited by the waggle dance (2005) Nature, 435, pp. 205-207
  • Robinson, G., Regulation of division of labor in insect societies (1992) Annu. Rev. Entomol., 37, pp. 637-665
  • Rösch, G.A., Untersuchungen uber die Arbeitsteilung im Bienenstaat 1. Teil: Die Tatigkeiten im normalen Bienenstaate und ihre Beziehungen zum Alter der Arbeitsbienen (1925) Z vergl Physiol, 2, pp. 571-631
  • Rubin, B.D., Katz, L.C., Optical imaging of odorant representations in the mammalian olfactory bulb (1999) Neuron, 23, pp. 499-511
  • Sachse, S., Galizia, C.G., 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 honeybees: steps towards the olfactory code (1999) Eur. J. Neurosci., 11, pp. 3970-3982
  • 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 honeybee antenal lobe (2003) Neuroscience, 120, pp. 1137-1148
  • Sandoz, J.C., Laloi, D., Odoux, J.F., Pham-Delegué, M.H., Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure (2000) Anim. Behav., 59, pp. 1025-1034
  • 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
  • Scheiner, R., Erber, J., Page Jr, R.E., Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L (1999) J. Comp. Physiol., A 185, pp. 1-10
  • Scheiner, R., Page Jr, R.E., Erber, J., The effects of genotype, foraging Role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L (2001) Neurobiol. Learn. Mem., 76, pp. 138-150
  • Seeley, T.D., Adaptive significance of the age polyethism schedule in honeybee colonies (1982) Behav. Ecol. Sociobiol., 11, pp. 287-293
  • Seeley, T.D., Social foraging in honeybees: how nectar foragers assess their colony's nutritional status (1989) Behav. Ecol. Sociobiol., 24, pp. 181-199
  • Sigg, D., Thompson, C.M., Mercer, A.R., Activity-dependent changes to the brain and behavior of the honey bee Apis mellifera (L. ). (1997) J. Neurosci., 17, pp. 7148-7156
  • Takeda, K., Classical conditioned response in the honey bee (1961) J. Insect Physiol., 6, pp. 168-179
  • Uchida, N., Takahashi, Y.K., Tanifuji, M., Mori, K., Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features (2000) Nat. Neurosci., 3, pp. 1035-1043
  • Von Frisch, K., (1967) The Dance Language and Orientation of Bees, , Cambridge, MA: Harvard University Press
  • Wang, W.S., Zhang, S., Sato, K., Srinivasan, M.V., Maturation of odor representation in the honeybee antennal lobe (2005) J. Insect Physiol., 51, pp. 1244-1254
  • Willmer, P.G., Stone, G.N., Behavioral, ecological, and physiological determinants of the activity patterns of bees (2004) Adv. Stud. Behav., 34, pp. 347-466
  • Wilson, E.O., (1971) The Insect Societies, , Cambridge, MA: Harvard University Press
  • Winnington, A.P., 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
  • Winston, M.L., (1987) Biology of the Honey Bee, , Cambridge: Harvard University Press

Citas:

---------- APA ----------
Arenas, A., Ramírez, G.P., Balbuena, M.S. & Farina, W.M. (2013) . Behavioral and neural plasticity caused by early social experiences: The case of the honeybee. Frontiers in Physiology, 4 AUG.
http://dx.doi.org/10.3389/fphys.2013.00041
---------- CHICAGO ----------
Arenas, A., Ramírez, G.P., Balbuena, M.S., Farina, W.M. "Behavioral and neural plasticity caused by early social experiences: The case of the honeybee" . Frontiers in Physiology 4 AUG (2013).
http://dx.doi.org/10.3389/fphys.2013.00041
---------- MLA ----------
Arenas, A., Ramírez, G.P., Balbuena, M.S., Farina, W.M. "Behavioral and neural plasticity caused by early social experiences: The case of the honeybee" . Frontiers in Physiology, vol. 4 AUG, 2013.
http://dx.doi.org/10.3389/fphys.2013.00041
---------- VANCOUVER ----------
Arenas, A., Ramírez, G.P., Balbuena, M.S., Farina, W.M. Behavioral and neural plasticity caused by early social experiences: The case of the honeybee. Front. Physiol. 2013;4 AUG.
http://dx.doi.org/10.3389/fphys.2013.00041