Long-term effects of infant learning on adult conditioned odor aversion are determined by the last preweaning experience

Developmental Psychobiology

Volumn 51, Issue 5, 2009, Pages 389-398

  Sevelinges, Yannick ^a   Mouly, Anne Marie ^b   Lévy, Frédéric ^a   Ferreira, Guillaume ^a  

^a UNIVERSITÉ DE TOURS   (France)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

Associative learning; Early olfactory learning; Food memory; Interference; Rat; Rattus norvegicus

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AVERSION; CHILD BEHAVIOR; CONDITIONING; CONTROLLED STUDY; FEMALE; LACTATION; LEARNING; MALE; NONHUMAN; PERINATAL PERIOD; RAT; SMELLING; SUCKLING; WEANING;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ASSOCIATION LEARNING; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); FEEDING BEHAVIOR; MEMORY; NIPPLES; ODORS; RATS; TIME FACTORS; WEANING;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 70349389293     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20378     Document Type: Article

References (45)

1. Armstrong, C. M., DeVito, L. M., & Cleland, T. A. (2006). Onetrial associative odor learning in neonatal mice. Chemical Senses, 31, 343-349.
2. Batsell, W. R, Jr., & Best, M. R. (1993). One bottle too many? Method of testing determines the detection of overshadowing and retention of taste aversions. Animal Learning and Behavior, 2, 154-158.
3. Blais, I., Terkel, J., & Goldblatt, A. (2006). Long-term impact of early olfactory experience on later olfactory conditioning. Developmental Psychobiology, 48, 501-507.
4. Bouslama, M., Durand, E., Chauviere, L., Van den Bergh, O., & Gallego, J. (2005). Olfactory classical conditioning in newborn mice. Behavioural Brain Research, 161, 102-106.
5. Brake, S. C. (1981). Suckling infant rats learn a preference for a novel olfactory stimulus paired with milk delivery. Science, 211, 506-508.
6. Campbell, B. A., & Campbell, E. H. (1962). Retention and extinction of learned fear in infant and adult rats. Journal of Comparative Physiology and Psychology, 55, 1-8.
7. Campbell, B. A., & Spear, N. E. (1972). Ontogeny of memory. Psychology Review, 79, 215-236.
8. Chapuis, J., Messaoudi, B., Ferreira, G., & Ravel, N. (2007). Importance of retronasal and orthonasal olfaction for odor aversion memory in rats. Behavioral Neuroscience, 121, 1383-1392.
9. Cheslock, S. J., Sanders, S. K., & Spear, N. E. (2004). Learning during the newborn's first meal: Special resistance to retroactive interference. Developmental Science, 7, 581-598.
10. Cheslock, S. J., Varlinskaya, E. I., Petrov, E. S., & Spear, N. E. (2000). Rapid and robust olfactory conditioning with milk before suckling experience: Promotion of nipple attachment in the newborn rat. Behavioral Neuroscience, 114, 484-495.
11. Coureaud, G., Schaal, B., Hudson, R., Orgeur, P., & Coudert, P. (2002). Transnatal olfactory continuity in the rabbit: Behavioral evidence and short-term consequence of its disruption. Developmental Psychobiology, 40, 372-390.
12. Delaunay-El Allam, M., Marlier, L., & Schaal, B. (2006). Learning at the breast: Preference formation for an artificial scent and its attraction against the odor of maternal milk. Infant Behavior and Development, 29, 308-321.
13. Escobar, M., Arcediano, F., Platt, T. L., & Miller, R. R. (2004). Interference and time: A brief review and an integration. Review in Neuroscience, 15, 415-438.
14. Fillion, T. J., & Blass, E. M. (1986). Infantile experience with suckling odors determines adult sexual behavior in male rats. Science, 231, 729-731.
15. Gruest, N., Richer, P., & Hars, B. (2004). Emergence of long-term memory for conditioned aversion in the rat fetus. Developmental Psychobiology, 44, 189-198.
16. Hepper, P. G., & Wells, D. L. (2006). Perinatal olfactory learning in the domestic dog. Chemical Senses, 31, 207-212.
17. Hofer, M. A., & Sullivan, R. M. (2001). Towards a neurobiology of attachment. In: C. A. Nelson & M. Luciana (Eds.), Developmental cognitive neuroscience (pp. 599-616). Cambridge, MA: MIT Press.
18. Ito, A., Kikusui, T., Takeuchi, Y., & Mori, Y. (2006). Effects of early weaning on anxiety and autonomic responses to stress in rats. Behavioural Brain Research, 171, 87-93.
19. Kanari, K., Kikusui, T., Takeuchi, Y., & Mori, Y. (2005). Multidimensional structure of anxiety-related behavior in early-weaned rats. Behavioural Brain Research, 156, 45-52.
20. Kim, J. H., McNally, G. P., & Richardson, R. (2006). Recovery of fear memories in rats: Role of gamma-amino butyric acid (GABA) in infantile amnesia. Behavioral Neuroscience, 120, 40-48.
21. Kim, J. H., & Richardson, R. (2007). Immediate post-reminder injection of gamma-amino butyric acid (GABA) agonist midazolam attenuates reactivation of forgotten fear in the infant rat. Behavioral Neuroscience, 121, 1328-1332.
22. Mainardi, D., Marsan, M., & Pasquali, A. (1965). Causation of sexual preferences in the house mouse. The behavior of mice reared by parents whose odor was artificially altered. Atti della Societá Italiana di Scienze Naturali, 104, 325-338.
23. Marr, J. N., & Gardner, L. E. (1965). Early olfactory experience and later social behavior in the rat: Preference, sexual responsiveness, and care of young. Journal of genetic Psychology, 107, 167-174.
24. McLean, J. H., Darby-King, A., & Hodge, E. (1996). 5-HT2 receptor involvement in conditioned olfactory learning in the neonate rat pup. Behavioral Neuroscience, 110, 1426-1434.
25. Moriceau, S., & Sullivan, R. M. (2004). Unique neural circuitry for neonatal olfactory learning. Journal of Neuroscience, 24, 1182-1189.
26. Moriceau, S., & Sullivan, R. M. (2005). Neurobiology of infant attachment. Developmental Psychobiology, 47, 230-242.
27. Ono, M., Kikusui, T., Sasaki, N., Ichikawa, M., Mori, Y., & Murakami-Murofushi, K. (2008). Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice. Neuroscience, 156, 1103-1110.
28. Porter, R. H., Winberg, J., & Varendi, H. (2005). Prenatal preparation for early olfactory learning. In: B. Hopkins & S. P. Johnson (Eds.), Prenatal development of postnatal functions (pp 103-129). Westport, CT: Praeger Publishers/Greenwood Publishing Group, Inc.
29. Rescorla, R. A. (1988). Behavioral studies of Pavlovian conditioning. Annual Review of Neuroscience, 11, 329-352.
30. Rudy, J. W. (1993). Contextual conditioning and auditory cue conditioning dissociate during development. Behavioral Neuroscience, 107, 887-891.
31. Rudy, J. W., & Morledge, P. (1994). Ontogeny of contextual fear conditioning in rats: Implications for consolidation, infantile amnesia, and hippocampal system function. Behavioral Neuroscience, 108, 227-234.
32. Saint-Dizier, H., Levy, F., & Ferreira, G. (2007). Influence of the mother in the development of flavored-food preference in lambs. Developmental Psychobiology, 49, 98-106.
33. Sevelinges, Y., Levy, F., Mouly, A. M., & Ferreira, G. (2009). Rearing with artificially scented mothers attenuates conditioned odor aversion in adulthood but not its amygdala dependency. Behavioural Brain Research, 198(2), 313-320.
34. Sevelinges, Y., Moriceau, S., Holman, P., Miner, C., Muzny, K., Gervais, R., et al. (2007). Enduring effects of infant memories: Infant odor-shock conditioning attenuates amygdala activity and adult fear conditioning. Biological Psychiatry, 62, 1070-1079.
35. Sevelinges, Y., Sullivan, R. M., Messaoudi, B., & Mouly, A. M. (2008). Neonatal odor-shock conditioning alters the neural network involved in odor fear learning at adulthood. Learning & Memory, 15, 649-656.
36. Shah, A., Oxley, G., Lovic, V., & Fleming, A. S. (2002). Effects of preweaning exposure to novel maternal odors on maternal responsiveness and selectivity in adulthood. Developmental Psychobiology, 41, 187-196.
37. Slotnick, B. M., Westbrook, F., & Darling, F. M. C. (1997). What the rat's nose tells the rat's mouth: Long delay aversion conditioning with aqueous odors and potentiation of taste by odors. Animal Learning and Behavior, 25, 357-369.
38. Smotherman, W. P. (1982). In utero chemosensory experience alters taste preferences and corticosterone responsiveness. Behavioral and Neural Biology, 36, 61-68.
39. Sullivan, R. M., Taborsky-Barba, S., Mendoza, R., Itano, A., Leon, M., Cotman, C. W., et al. (1991). Olfactory classical conditioning in neonates. Pediatrics, 87, 511-518.
40. Sullivan, R. M., Wilson, D. A., Lemon, C., & Gerhardt, G. A. (1994). Bilateral 6-OHDA lesions of the locus coeruleus impair associative olfactory learning in newborn rats. Brain Research, 643, 306-309.
41. Sullivan, R. M., Wilson, D. A., & Leon, M. (1989). Norepinephrine and learning-induced plasticity in infant rat olfactory system. Journal of Neuroscience, 9(11), 3998-4006.
42. Sullivan, R. M., Zyzak, D. R., Skierkowski, P., & Wilson, D. A. (1992). The role of olfactory bulb norepinephrine in early olfactory learning. Brain Research and Developmental Brain Research, 70, 279-282.
43. Val-Laillet, D., & Nowak, R. (2008). Early discrimination of the mother by rabbit pups. Applied Animal Behavioural Science, 111, 173-182.
44. Weber, M., McNally, G. P., & Richardson, R. (2006). Opioid receptors regulate retrieval of infant fear memories: Effects of naloxone on infantile amnesia. Behavioral Neuroscience, 120, 702-709.
45. Wilson, D. A., Sullivan, R. M., & Leon, M. (1987). Single-unit analysis of postnatal olfactory learning: Modified olfactory bulb output response patterns to learned attractive odors. Journal of Neuroscience, 7, 3154-3162.