Associative learning during early adulthood enhances later memory retention in honeybees

PLoS ONE

Volumn 4, Issue 12, 2009, Pages

  Arenas, Andrés ^a   Fernández, Vanesa M ^a   Farina, Walter M ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

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;

EID: 77949532629     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008046     Document Type: Article

References (40)

1. Lorenz K (1935) Der Kumpan in der Umwelt des Vogels. Zeitschrift für Ornithologie 83: 137-213, 289-413.
2. Oitzl MS, Workel JO, Fluttert M, Frosch F, De Kloet ER (2000) Maternal deprivation affects behaviour from youth to senescence: Amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur J Neurosci 12(10): 3771-3780.
3. Iso H, Simoda S, Matsuyama T (2007) Environmental change during postnatal development alters behaviour, cognitions and neurogenesis of mice. Behav Brain Res 179: 90-98. (DOI 10.1016/j.bbr.2007.01.025).
4. Neal WR (1972) The effect of environmental deprivation on speech and language development: Implications for child care workers. Child Care Quarterly 1: 157-172.
5. Bialystok E (2001) Bilingualism in development: language, literacy, and cognition. Cambridge University Press.
6. Ichikawa N, Sasaki M (2003) Importance of social stimuli for the development of learning capability in honeybee. Appl Entomol Zool 38: 203-209.
7. Wilson EO (1971) The Insect Societies. Belknap Press of Harvard University Press, Cambridge.
8. Hölldobler B, Michener CD (1980) Mechanisms of identification and discrimination in social Hymenoptera. In: Evolution of Social Behavior: Hypothesis and Empirical Tests (H. Markl, Ed), Verlag Chemie, Weinheim. pp 35-58.
9. Caubet Y, Jaisson P (1991) A post-eclosion early learning involved in host recognition by Dinarmus basalis rondani (Hymenoptera: Pteromalidae) Anim Behav 42: 977-980.
10. Arenas A, Farina WM (2008) Age and rearing environment interact in the retention of early olfactory memories in honeybees. J Comp Physiol A 194: 629-640. (DOI 10.1007/s00359-008-0337-z).
11. Sandoz JC, Laloi D, Odoux JF, Pham-Delègue MH (2000) Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure. Anim Behav 59: 1025-1034. (DOI 10.1006/anbe.2000.1395).
12. Fernández VM, Arenas A, Farina WM (2009) Volatile exposure within the honeybee hive and its effect on olfactory discrimination. J Comp Physiol A 195: 759-768. (DOI 10.1007/s00359-009-0453-4).
13. Behrends A, Scheiner R (2009) Evidence for associative learning in newly emerged honey bees (Apis mellifera). Anim Cogn 12: 249-255.
14. Robinson GE (1992) Regulation of division of labor in insect societies. Ann Rev Entomol 37: 637-665.
15. Rösch GA (1925) Untersuchungen über die Arbeitsteilung im Bienenstaat. Z vergl Physiol 2: 571-631.
16. Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z vergl Physiol 34: 299-345.
17. Seeley TD (1982) Adaptive significance of the age polytheism schedule in honeybee colonies. Behavl Ecol Sociobiol 11(4): 287-293.
18. Garelick MG, Storm DR (2005) The relationship between memory retrieval and memory extinction. Proc Natl Acad Sci USA 102(26): 9091-9092.
19. Takeda K (1961) Classical conditioned response in the honey bee. J Insect Physiol 6: 168-179.
20. Bitterman ME, Menzel R, Fietz A, Schaefer S (1983) Classical conditioning of proboscis extension in honeybees. J Comp Physiol A 97: 107-119.
21. Masson C, Pham-Delègue MH, Fonta C, Gascuel J, Arnold G, et al. (1993) Recent advances in the concept of adaptation to natural odour signals in the honeybee Apis mellifera L. Apidologie 24: 169-194.
22. Winnington A, Napper RM, Mercer AR (1996) Structural plasticity of identified glomeruli in the antennal lobes of the adult worker honey bee. J Comp Neurol 365: 479-490.
23. Farris SM, Robinson GE, Fahrbach SE (2001) Experience- and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21(16): 6395-6404.
24. Chandra SBC, Hosler JS, Smith BH (2000) Heritable variation for latent inhibition and its correlation to reversal learning in the honey bee, Apis mellifera. J Comp Physiol A 114: 86-97. (DOI 10.1037//0735-7036.114.1.86).
25. Ferguson H, Cobey S, Smith BH (2001) Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera. Anim Behav 61: 527-534. (DOI 10.1006/anbe.2000.1635).
26. Lunney GH (1970) Using analysis of variance with a dichotomous dependent variable: an empirical study. J Educat Meas 7: 263-269.
27. Faber T, Joerges J, Menzel R (1999) Associative learning modifies neural representations of odors in the insect brain. Nat Neurosci 2: 74-78.
28. Daly KC, Christensen TA, Lei H, Smith BH, Hildebrand JG (2004) Learning modulates the ensemble representations for odors in primary olfactory networks. PNAS 101: 10476-10481.
29. Arenas A, Giurfa M, Farina WM, Sandoz JC (2009) Early olfactory experience modifies neural activity in the antennal lobe of a social insect at the adult stage. Eur J Neurosci 30: 1498-1508. (DOI 10.1111/j.1460-9568.2009.06940.x).
30. Vergoz V, Roussel E, Sandoz JC, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS ONE 2(3): e288. (DOI 10.1371/journal.pone.0000288).
31. Arenas A, Fernández VM, Farina WM (2008) Floral scents experienced within the colony affect long-term foraging preferences in honeybees. Apidologie 39: 714-722. (DOI 10.1051/apido: 2008053).
32. Daly KC, Durtschi ML, Smith BH (2001) Olfactory-based discrimination in the moth, Manduca sexta. J Insect Physiol 47: 375-384.
33. Laloi D, Pham-Delègue MH (2004) Bumble Bees show asymmetrical discrimination between two odors in a classical conditioning procedure, J Insect Behav 3(17): 385-396.
34. Maleszka R, Helliwell P (2001) Effect of juvenile hormone on short-term olfactory memory in young honeybees (Apis mellifera) Hormones and Behav 40: 403-408. (DOI 10.1006/hbeh.2001.1705).
35. Farina WM, Grüter C, Acosta LE, McCabe S (2007) Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94: 55-60.
36. Farina WM, Grüter C, Diaz PC (2005) Social learning of floral odours within the honeybee hive. Proc R Soc B 272: 1923-1928.
37. Gil M, De Marco RJ (2005) Olfactory learning by means of trophallaxis in Apis mellifera. J Exp Biol 208: 671-680.
38. Free JB (1969) Influence of the odour of a honeybee colony's food stores on the behaviour of its foragers. Nature 222: 778.
39. Sahakian BJ, Robbins TW, Morgan MJ, Iversen SD (1975) The effects of psychomotor stimulants on stereotypy and locomotor activity in socially deprived and control rats. Brain Res 84: 195.
40. Lodge DJ, Lawrence AJ (2003) The effect of isolation rearing on volitional ethanol consumption and central CCK/dopamine systems in Fawn-Hooded rats. Behav Brain Res 141: 113-122.