Early-life nutritional stress affects associative learning and spatial memory but not performance on a novel object test

Behaviour

Volumn 152, Issue 2, 2015, Pages 195-218

  Kriengwatana, Buddhamas ^a,b   Farrell, Tara M ^a   Aitken, Sean D T ^a   Garcia, Laura ^a   MacDougall Shackleton, Scott A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

behavioural flexibility; cognition; development; developmental stress; juvenile stress; personality

Indexed keywords

AVES; PASSERI; TAENIOPYGIA GUTTATA;

EID: 84924019487     PISSN: 00057959     EISSN: 1568539X     Source Type: Journal    
DOI: 10.1163/1568539X-00003239     Document Type: Article

References (52)

1. Adret, P. (1993). Operant conditioning, song learning and imprinting to taped song in the zebra finch. - Anim. Behav. 46: 149-159.
2. Amy, M., van Oers, K. & Naguib, M. (2012). Worms under cover: relationships between performance in learning tasks and personality in great tits (Parus major). - Anim. Cog. 15: 763-770.
3. Arnold, K.E., Ramsay, S.L., Donaldson, C. & Adam, A. (2007). Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring. - Proc. Roy. Soc. Lond. B: Biol. Sci. 274: 2563-2569.
4. Bailey, D.J., Wade, J. & Saldanha, C.J. (2009). Hippocampal lesions impair spatial memory performance, but not song-A developmental study of independent memory systems in the zebra finch. - Dev. Neurobiol. 69: 491-504.
5. Bonaparte, K.M., Riffle-Yokoi, C. & Burley, N.T. (2011). Getting a head start: diet, sub-adult growth, and associative learning in a seed-eating passerine. - PLoS ONE 6: e23775.
6. Boogert, N.J., Giraldeau, L.-A. & Lefebvre, L. (2008). Song complexity correlates with learning ability in zebra finch males. - Anim. Behav. 76: 1735-1741.
7. Boogert, N.J., Fawcett, T.W. & Lefebvre, L. (2011). Mate choice for cognitive traits: a review of the evidence in nonhuman vertebrates. - Behav. Ecol. 22: 447-459.
8. Boogert, N.J., Zimmer, C. & Spencer, K.A. (2013). Pre- and post-natal stress have opposing effects on social information use. - Biol. Lett. 9: 2021088.
9. Brumm, H., Zollinger, S.A. & Slater, P.J.B. (2009). Developmental stress affects song learning but not song complexity and vocal amplitude in zebra finches. - Behav. Ecol. Socio-biol. 63: 1387-1395.
10. Brust, V., Wuerz, Y. & Krüger, O. (2013). Behavioural flexibility and personality in zebra finches. - Ethology 119: 559-569.
11. Brust, V., Krüger, O., Naguib, M. & Krause, E.T. (2014). Lifelong consequences of early nutritional conditions on learning performance in zebra finches (Taeniopygia guttata). - Behav. Process. 103: 320-326.
12. Buchanan, K.L., Leitner, S., Spencer, K.A., Goldsmith, A.R. & Catchpole, C.K. (2004). Developmental stress selectively affects the song control nucleus HVC in the zebra finch. - Proc. Roy. Soc. Lond. B: Biol. Sci. 271: 2381-2386.
13. Carere, C., Drent, P.J., Groothuis, T.G.G. & Koolhaas, J.M. (2005). Epigenetic effects on personality traits: early food provisioning and sibling competition. - Behaviour 142: 1329-1355.
14. Carere, C. & Locurto, C. (2011). Interaction between animal personality and animal cognition. - Curr. Zool. 57: 491-498.
15. Crino, O.L., Driscoll, S.C. & Breuner, C.W. (2014). Corticosterone exposure during development has sustained but not lifelong effects on body size and total and free corticosterone responses in the zebra finch. - Gen. Comp. Endocrinol. 196: 123-129.
16. Criscuolo, F., Monaghan, P., Nasir, L. & Metcalfe, N.B. (2008). Early nutrition and pheno-typic development: 'catch-up' growth leads to elevated metabolic rate in adulthood. - Proc. Roy. Soc. Lond. B: Biol. Sci. 275: 1565-1570.
17. Dingemanse, N.J. & Réale, D. (2005). Natural selection and animal personality. - Behaviour 142: 1165-1190.
18. Farrell, T.M., Weaver, K., An, Y. & MacDougall-Shackleton, S.A. (2012). Song bout length is indicative of spatial learning in European starlings. - Behav. Ecol. 23: 101-111.
19. Fisher, M.O., Nager, R.G. & Monaghan, P. (2006). Compensatory growth impairs adult cognitive performance. - PLOS Biol. 4: 1462-1466.
20. Floresco, S.B., Magyar, O., Ghods-Sharifi, S., Vexelman, C. & Tse, M.T.L. (2006). Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. - Neuropsychopharmacology 31: 297-309.
21. Forstmeier, W. & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse. - Behav. Ecol. Sociobiol. 65: 47-55.
22. Galea, L.A.M., Wide, J.K., Paine, T.A., Holmes, M.M., Ormerod, B.K. & Floresco, S.B. (2001). High levels of estradiol disrupt conditioned place preference learning, stimulus response learning and reference memory but have limited effects on working memory. - Behav. Brain Res. 126: 115-126.
23. Goerlich, V.C., Nätt, D., Elfwing, M., Macdonald, B. & Jensen, P. (2012). Transgenerational effects of early experience on behavioral, hormonal and gene expression responses to acute stress in the precocial chicken. - Horm. Behav. 61: 711-718.
24. Guillette, L.M., Reddon, A.R., Hoeschele, M. & Sturdy, C.B. (2011). Sometimes slower is better: slow-exploring birds are more sensitive to changes in a vocal discrimination task. - Proc. Roy. Soc. Lond. B: Biol. Sci. 278: 767-773.
25. Holveck, M.-J., Vieira De Castro, A.C., Lachlan, R.F., ten Cate, C. & Riebel, K. (2008). Accuracy of song syntax learning and singing consistency signal early condition in zebra finches. - Behav. Ecol. 19: 1267-1281.
26. Holveck, M.-J. & Riebel, K. (2010). Low-quality females prefer low-quality males when choosing a mate. - Proc. Roy. Soc. Lond. B: Biol. Sci. 277: 153-160.
27. Honarmand, M., Goymann, W. & Naguib, M. (2010). Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in zebra finch nestlings and fledglings. - PloS ONE 5: e12930.
28. Korol, D.L. (2004). Role of estrogen in balancing contributions from multiple memory systems. - Neurobiol. Learning. Mem. 82: 309-323.
29. Krause, E.T. & Naguib, M. (2011). Compensatory growth affects exploratory behaviour in zebra finches, Taeniopygia guttata. - Anim. Behav. 81: 1295-1300.
30. Krause, E.T., Honarmand, M., Wetzel, J. & Naguib, M. (2009). Early fasting is long lasting: differences in early nutritional conditions reappear under stressful conditions in adult female zebra finches. - PLOS ONE 4: e5015.
31. Kriengwatana, B., Wada, H., MacMillan, A. & MacDougall-Shackleton, S.A. (2013). Juvenile nutritional stress affects growth rate, adult organ mass, and innate immune function in zebra finches (Taeniopygia guttata). - Physiol. Biochem. Zool. 86: 769-781.
32. Kriengwatana, B., Wada, H., Schmidt, K.L., Taves, M.D., Soma, K.K. & Macdougall-Shackleton, S.A. (2014). Effects of nutritional stress during different developmental periods on song and the hypothalamic-pituitary-adrenal axis in zebra finches. - Horm. Behav. 65: 285-293.
33. Lemon, W.C. (1991). Fitness consequences of foraging behaviour in the zebra finch. - Nature 352: 153-155.
34. Lemon, W.C. & Barth, R.H. (1992). The effects of feeding rate on reproductive success in the zebra finch, Taeniopygia guttata. - Anim. Behav. 44: 851-857.
35. Lindström, J. (1999). Early development and fitness in birds and mammals. - Trends Ecol. Evol. 14: 343-348.
36. Martins, T.L.F., Roberts, M.L., Giblin, I., Huxham, R. & Evans, M.R. (2007). Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches. - Horm. Behav. 52: 445-453.
37. Metcalfe, N.B. & Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? - Trends Ecol. Evol. 16: 254-260.
38. Monaghan, P. (2008). Early growth conditions, phenotypic development and environmental change. - Phil. Trans. Roy. Soc. B 363: 1635-1645.
39. Naguib, M. & Nemitz, A. (2007). Living with the past: nutritional stress in juvenile males has immediate effects on their plumage ornaments and on adult attractiveness in zebra finches. - PLoS ONE 2: e901.
40. Naguib, M., Flörcke, C. & van Oers, K. (2011). Effects of social conditions during early development on stress response and personality traits in great tits (Parus major). - Dev. Psychobiol. 53: 592-600.
41. Nowicki, S., Peters, S. & Podos, J. (1998). Song learning, early nutrition and sexual selection in songbirds. - Integr. Comp. Biol. 38: 179-190.
42. Nowicki, S., Searcy, W.A. & Peters, S. (2002). Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis". - J. Comp. Physiol. A 188: 1003-1014.
43. Pravosudov, V.V., Lavenex, P. & an Omanska, A. (2005). Nutritional deficits during early development affect hippocampal structure and spatial memory later in life. - Behav. Neurosci. 119: 1368-1374.
44. Ragozzino, M.E. (2002). The effects of dopamine D1 receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. - Learn. Mem. 9: 18-28.
45. Spencer, K.A. & MacDougall-Shackleton, S.A. (2011). Indicators of development as sexually selected traits: the developmental stress hypothesis in context. - Behav. Ecol. 22: 1-9.
46. Spencer, K.A. & Verhulst, S. (2007). Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata). - Horm. Behav. 51: 273-280.
47. Spencer, K.A., Buchanan, K.L., Goldsmith, A.R. & Catchpole, C.K. (2003). Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). - Horm. Behav. 44: 132-139.
48. Stamps, J.A. & Groothuis, T.G.G. (2010). Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. - Phil. Trans. Roy. Soc. Lond. B 365: 4029-4041.
49. Titulaer, M., van Oers, K. & Naguib, M. (2012). Personality affects learning performance in difficult tasks in a sex-dependent way. - Anim. Behav. 83: 723-730.
50. Tschirren, B., Rutstein, A.N., Potsma, E., Marriette, M. & Griffith, S.C. (2009). Short- and long-term consequences of early developmental conditions: a case study on wild and domesticated zebra finches. - J. Evol. Biol. 22: 387-395.
51. van Oers, K., Drent, P.J., de Jong, G. & van Noordwijk, A.J. (2004). Additive and nonadditive genetic variation in avian personality traits. - Heredity 93: 496-503.
52. Wada, H., Salvante, K.G., Stables, C., Wagner, E., Williams, T.D. & Breuner, C.W. (2008). Adrenocortical responses in zebra finches (Taeniopygia guttata): individual variation, repeatability, and relationship to phenotypic quality. - Horm. Behav. 53: 472-480.