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Background: Cognitive experiences during the early stages of life play an important role in shaping the future behavior in mammals but also in insects, in which precocious learning can directly modify behaviors later in life depending on both the timing and the rearing environment. However, whether olfactory associative learning acquired early in the adult stage of insects affect memorizing of new learning events has not been studied yet. Methodology: Groups of adult honeybee workers that experienced an odor paired with a sucrose solution 5 to 8 days or 9 to 12 days after emergence were previously exposed to (i) a rewarded experience through the offering of scented food, or (ii) a non-rewarded experience with a pure volatile compound in the rearing environment. Principal Findings: Early rewarded experiences (either at 1-4 or 5-8 days of adult age) enhanced retention performance in 9-12-day-conditioned bees when they were tested at 17 days of age. The highest retention levels at this age, which could not be improved with prior rewarded experiences, were found for memories established at 5-8 days of adult age. Associative memories acquired at 9-12 days of age showed a weak effect on retention for some pure pre-exposed volatile compounds; whereas the sole exposure of an odor at any younger age did not promote long-term effects on learning performance. Conclusions: The associative learning events that occurred a few days after adult emergence improved memorizing in middle-aged bees. In addition, both the timing and the nature of early sensory inputs interact to enhance retention of new learning events acquired later in life, an important matter in the social life of honeybees. © 2009 Arenas et al.


Documento: Artículo
Título:Associative learning during early adulthood enhances later memory retention in honeybees
Autor:Arenas, A.; Fernández, V.M.; Farina, W.M.
Filiación:Grupo de Estudio de Insectos Sociales, IFIBYNE-CONICET, Departamento de Biodiversidad y Biologia Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II, Ciudad Universitaria, Buenos Aires, Argentina
Palabras clave:sucrose; volatile agent; carbohydrate; animal behavior; article; behavioral science; controlled study; honeybee; memory consolidation; nonhuman; reward; sensory stimulation; social behavior; state dependent learning; task performance; aging; animal; bee; conditioning; drug effect; environment; feeding behavior; learning; long term memory; longevity; odor; physiology; smelling; solution and solubility; volatilization; Apis mellifera; Apoidea; Hexapoda; Mammalia; Aging; Animals; Association Learning; Bees; Behavior, Animal; Carbohydrates; Conditioning (Psychology); Environment; Feeding Behavior; Longevity; Odors; Olfactory Perception; Retention (Psychology); Solutions; Volatilization
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
CAS:sucrose, 122880-25-5, 57-50-1; Carbohydrates; Solutions


  • Lorenz, K., Der Kumpan in der Umwelt des Vogels (1935) Zeitschrift Für Ornithologie, 83, pp. 137-213+289-413
  • Oitzl, M.S., Workel, J.O., Fluttert, M., Frosch, F., de Kloet, E.R., Maternal deprivation affects behaviour from youth to senescence: Amplification of individual differences in spatial learning and memory in senescent Brown Norway rats (2000) Eur J Neurosci, 12 (10), pp. 3771-3780
  • Iso, H., Simoda, S., Matsuyama, T., Environmental change during postnatal development alters behaviour, cognitions and neurogenesis of mice (2007) Behav Brain Res, 179, pp. 90-98. , (DOI 10.1016/j.bbr.2007.01.025)
  • Neal, W.R., The effect of environmental deprivation on speech and language development: Implications for child care workers (1972) Child Care Quarterly, 1, pp. 157-172
  • Bialystok, E., (2001) Bilingualism In Development: Language, Literacy, and Cognition, , Cambridge University Press
  • Ichikawa, N., Sasaki, M., Importance of social stimuli for the development of learning capability in honeybee (2003) Appl Entomol Zool, 38, pp. 203-209
  • Wilson, E.O., (1971) The Insect Societies, , Belknap Press of Harvard University Press, Cambridge
  • Hölldobler, B., Michener, C.D., Mechanisms of identification and discrimination in social Hymenoptera (1980) Evolution of Social Behavior: Hypothesis and Empirical Tests, pp. 35-58. , H. Markl, Ed), Verlag Chemie, Weinheim
  • Caubet, Y., Jaisson, P., A post-eclosion early learning involved in host recognition by Dinarmus basalis rondani (Hymenoptera: Pteromalidae) (1991) Anim Behav, 42, pp. 977-980
  • Arenas, A., Farina, W.M., Age and rearing environment interact in the retention of early olfactory memories in honeybees (2008) J Comp Physiol A, 194, pp. 629-640. , DOI 10.1007/s00359-008-0337-z
  • Sandoz, J.C., Laloi, D., Odoux, J.F., Pham-Delègue, M.H., Olfactory information transfer in the honeybee: Compared efficiency of classical conditioning and early exposure (2000) Anim Behav, 59, pp. 1025-1034. , DOI 10.1006/anbe.2000.1395
  • Fernández, V.M., Arenas, A., Farina, W.M., Volatile exposure within the honeybee hive and its effect on olfactory discrimination (2009) J Comp Physiol A, 195, pp. 759-768. , DOI 10.1007/s00359-009-0453-4
  • Behrends, A., Scheiner, R., Evidence for associative learning in newly emerged honey bees (Apis mellifera) (2009) Anim Cogn, 12, pp. 249-255
  • Robinson, G.E., Regulation of division of labor in insect societies (1992) Ann Rev Entomol, 37, pp. 637-665
  • Rösch, G.A., Untersuchungen über die Arbeitsteilung im Bienenstaat (1925) Z Vergl Physiol, 2, pp. 571-631
  • Lindauer, M., Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat (1952) Z Vergl Physiol, 34, pp. 299-345
  • Seeley, T.D., Adaptive significance of the age polytheism schedule in honeybee colonies (1982) Behavl Ecol Sociobiol, 11 (4), pp. 287-293
  • Garelick, M.G., Storm, D.R., The relationship between memory retrieval and memory extinction (2005) Proc Natl Acad Sci USA, 102 (26), pp. 9091-9092
  • Takeda, K., Classical conditioned response in the honey bee (1961) J Insect Physiol, 6, pp. 168-179
  • Bitterman, M.E., Menzel, R., Fietz, A., Schaefer, S., Classical conditioning of proboscis extension in honeybees (1983) J Comp Physiol A, 97, pp. 107-119
  • Masson, C., Pham-Delègue, M.H., Fonta, C., Gascuel, J., Arnold, G., Recent advances in the concept of adaptation to natural odour signals in the honeybee Apis mellifera L (1993) Apidologie, 24, pp. 169-194
  • 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
  • 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 (16), pp. 6395-6404
  • Chandra, S.B.C., Hosler, J.S., Smith, B.H., Heritable variation for latent inhibition and its correlation to reversal learning in the honey bee, Apis mellifera (2000) J Comp Physiol A, 114, pp. 86-97. , DOI 10.1037//0735-7036.114.1.86
  • Ferguson, H., Cobey, S., Smith, B.H., Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera (2001) Anim Behav, 61, pp. 527-534. , DOI 10.1006/anbe.2000.1635
  • Lunney, G.H., Using analysis of variance with a dichotomous dependent variable: An empirical study (1970) J Educat Meas, 7, pp. 263-269
  • Faber, T., Joerges, J., Menzel, R., Associative learning modifies neural representations of odors in the insect brain (1999) Nat Neurosci, 2, pp. 74-78
  • Daly, K.C., Christensen, T.A., Lei, H., Smith, B.H., Hildebrand, J.G., Learning modulates the ensemble representations for odors in primary olfactory networks (2004) PNAS, 101, pp. 10476-10481
  • 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. , DOI 10.1111/j.1460-9568.2009.06940.x
  • Vergoz, V., Roussel, E., Sandoz, J.C., Giurfa, M., Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex (2007) PLoS ONE, 2 (3), pp. e288. , DOI 10.1371/journal.pone.0000288
  • 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. , DOI 10.1051/apido: 2008053
  • Daly, K.C., Durtschi, M.L., Smith, B.H., Olfactory-based discrimination in the moth, Manduca sexta (2001) J Insect Physiol, 47, pp. 375-384
  • Laloi, D., Pham-Delègue, M.H., Bumble Bees show asymmetrical discrimination between two odors in a classical conditioning procedure (2004) J Insect Behav, 3 (17), pp. 385-396
  • Maleszka, R., Helliwell, P., Effect of juvenile hormone on short-term olfactory memory in young honeybees (Apis mellifera) (2001) Hormones and Behav, 40, pp. 403-408. , DOI 10.1006/hbeh.2001.1705
  • Farina, W.M., Grüter, C., Acosta, L.E., McCabe, S., Honeybees learn floral odors while receiving nectar from foragers within the hive (2007) Naturwissenschaften, 94, pp. 55-60
  • Farina, W.M., Grüter, C., Diaz, P.C., Social learning of floral odours within the honeybee hive (2005) Proc R Soc B, 272, pp. 1923-1928
  • Gil, M., de Marco, R.J., Olfactory learning by means of trophallaxis in Apis mellifera (2005) J Exp Biol, 208, pp. 671-680
  • Free, J.B., Influence of the odour of a honeybee colony's food stores on the behaviour of its foragers (1969) Nature, 222, p. 778
  • Sahakian, B.J., Robbins, T.W., Morgan, M.J., Iversen, S.D., The effects of psychomotor stimulants on stereotypy and locomotor activity in socially deprived and control rats (1975) Brain Res, 84, p. 195
  • Lodge, D.J., Lawrence, A.J., The effect of isolation rearing on volitional ethanol consumption and central CCK/dopamine systems in Fawn-Hooded rats (2003) Behav Brain Res, 141, pp. 113-122


---------- APA ----------
Arenas, A., Fernández, V.M. & Farina, W.M. (2009) . Associative learning during early adulthood enhances later memory retention in honeybees. PLoS ONE, 4(12).
---------- CHICAGO ----------
Arenas, A., Fernández, V.M., Farina, W.M. "Associative learning during early adulthood enhances later memory retention in honeybees" . PLoS ONE 4, no. 12 (2009).
---------- MLA ----------
Arenas, A., Fernández, V.M., Farina, W.M. "Associative learning during early adulthood enhances later memory retention in honeybees" . PLoS ONE, vol. 4, no. 12, 2009.
---------- VANCOUVER ----------
Arenas, A., Fernández, V.M., Farina, W.M. Associative learning during early adulthood enhances later memory retention in honeybees. PLoS ONE. 2009;4(12).