Maternal and developmental immune challenges alter behavior and learning ability of offspring

Hormones and Behavior

Volumn 62, Issue 3, 2012, Pages 337-344

  Grindstaff, Jennifer L ^a   Hunsaker, Veronica R ^a,b   Cox, Shelby N ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b UTAH STATE UNIVERSITY   (United States)

Author keywords

Bird; Developmental stress; Growth; Learning; Maternal antibodies; Maternal effects; Maternal immune challenge; Neonatal immune challenge; Neophobia; Zebra finch

Indexed keywords

KEYHOLE LIMPET HEMOCYANIN; LIPOPOLYSACCHARIDE; MATERNAL ANTIBODY;

ANIMAL BEHAVIOR; ARTICLE; BEHAVIOR CHANGE; CATABOLISM; CONTROLLED STUDY; EGG LAYING; FEMALE; FORAGING BEHAVIOR; GROWTH INHIBITION; GROWTH RATE; LEARNING; MALE; MATERNAL STRESS; NEONATAL STRESS; NEOPHOBIA; NEWBORN; NONHUMAN; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROGENY; PROVOCATION TEST; SEX DIFFERENCE; TAENIOPYGIA GUTTATA;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; FINCHES; HEMOCYANIN; IMMUNE SYSTEM; LEARNING; LIPOPOLYSACCHARIDES; MALE; SEX CHARACTERISTICS;

EID: 84866770804     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2012.04.005     Document Type: Article

References (53)

1. Addison B., Klasing K.C., Robinson W.D., Austin S.H., Ricklefs R.E. Ecological and life-history factors influencing the evolution of maternal antibody allocation: a phylogenetic comparison. Proc. R. Soc. Lond. B Biol. Sci. 2009, 276:3979-3987.
2. Andreano J.M., Cahill L. Sex influences on the neurobiology of learning and memory. Learn. Mem. 2009, 16:248-266.
3. Bangasser D.A., Shors T.J. Critical brain circuits at the intersection between stress and learning. Neurosci. Biobehav. Rev. 2010, 34:1223-1233.
4. Bilbo S.D., Schwarz J.M. Early-life programming of later-life brain and behavior: a critical role for the immune system. Front. Behav. Neurosci. 2009, 3:1-14.
5. Bilbo S.D., Levkoff L.H., Mahoney J.H., Watkins L.R., Rudy J.W., Maier S.F. Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav. Neurosci. 2005, 119:293-301.
6. Bilbo S.D., Rudy J.W., Watkins L.R., Maier S.F. A behavioural characterization of neonatal infection-facilitated memory impairment in adult rats. Behav. Brain Res. 2006, 169:39-47.
7. Boogert N.J., Giraldeau L.A., Lefebvre L. Song complexity correlates with learning ability in zebra finch males. Anim. Behav. 2008, 76:1735-1741.
8. Butler M.W., Toomey M.B., McGraw K.J., Rowe M. Ontogenetic immune challenges shape adult personality in mallard ducks. Proc. R. Soc. Lond. B Biol. Sci. 2012, 10.1098/rspb.2011.0842.
9. Davison F., Magor K.E., Kaspers B. The avian mucosal immune system. Avian Immunology 2008, 107-127. Elsevier, New York. F. Davison, B. Kaspers, K.A. Schat (Eds.).
10. de Kloet E.R., Grootendorst J., Karssen A.A., Oitzl M.S. Gene×environment interaction and cognitive performance: animal studies on the role of corticosterone. Neurobiol. Learn. Mem. 2002, 78:570-577.
11. Dixon F.J., Jacot-Guillarmod H., McConahey P.J. The antibody responses of rabbits and rats to hemocyanin. J. Immunol. 1966, 97:350-355.
12. Fumagalli F., Molteni R., Racagni G., Riva M.A. Stress during development: impact on neuroplasticity and relevance to psychopathology. Prog. Neurobiol. 2007, 81:197-217.
13. Grindstaff J.L. Maternal antibodies reduce costs of an immune response during development. J. Exp. Biol. 2008, 211:654-660.
14. Grindstaff J.L., Brodie E.D., Ketterson E.D. Immune function across generations: Integrating mechanism and evolutionary process in maternal antibody transmission. Proc. R. Soc. Lond. B Biol. Sci. 2003, 270:2309-2319.
15. Grindstaff J.L., Hasselquist D., Nilsson J.Å., Sandell M., Smith H.G., Stjernman M. Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc. R. Soc. Lond. B Biol. Sci. 2006, 273:2551-2557.
16. Harre E.M., Galic M.A., Mouihate A., Noorbakhsh F., Pittman Q.J. Neonatal inflammation produces selective behavioural deficits and alters n-methyl-d-aspartate receptor subunit mRNA in the adult rat brain. Eur. J. Neurosci. 2008, 27:644-653.
17. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 1988, 12:123-137.
18. Hasselquist D., Marsh J.A., Sherman P.W., Wingfield J.C. Is avian humoral immunocompetence suppressed by testosterone?. Behav. Ecol. Sociobiol. 1999, 45:167-175.
19. Heller E.D., Leitner G., Drabkin N., Melamed D. Passive immunization of chicks against Escherichia coli. Avian Pathol. 1990, 19:345-354.
20. Holveck M.J., Riebel K. Preferred songs predict preferred males: consistency and repeatability of zebra finch females across three contexts. Anim. Behav. 2007, 74:297-309.
21. Hsiao E.Y., Patterson P.H. Activation of the maternal immune system induces endocrine changes in the placenta via IL-6. Brain Behav. Immun. 2011, 25:604-615.
22. Jurincic-Winkler C., Klippel K.F., Beuth J., Markl J. Value of keyhole limpet hemocyanin in prevention of superficial bladder-cancer recurrence. Onkologie 1995, 18:41-50.
23. Karrow N.A. Activation of the hypothalamic-pituitary-adrenal axis and autonomic nervous system during inflammation and altered programming of the neuroendocrine-immune axis during fetal and neonatal development: lessons learned from the model inflammagen, lipopolysaccharide. Brain Behav. Immun. 2006, 20:144-158.
24. Kentner A.C., McLeod S.A., Field E.F., Pittman Q.J. Sex-dependent effects of neonatal inflammation on adult inflammatory markers and behavior. Endocrinology 2010, 151:2689-2699.
25. Kitraki E., Kremmyda O., Youlatos D., Alexis M., Kittas C. Spatial performance and corticosteroid receptor status in the 21-day restraint stress paradigm. Stress: Current neuroendocrine and genetic approaches 2004, 323-327.
26. Klasing K.C., Leshchinsky T.V. Functions, costs, and benefits of the immune system during development and growth. 22nd International Ornithological Congress 1999, 2817-2835. BirdLife South Africa, Durban, South Africa. N.J. Adams, R.H. Slotow (Eds.).
27. Kohman R.A., Tarr A.J., Sparkman N.L., Bogale T.M.H., Boehm G.W. Neonatal endotoxin exposure impairs avoidance learning and attenuates endotoxin-induced sickness behavior and central IL-1 beta gene transcription in adulthood. Behav. Brain Res. 2008, 194:25-31.
28. Kortet R., Hedrick A.V., Vainikka A. Parasitism, predation and the evolution of animal personalities. Ecol. Lett. 2010, 13:1449-1458.
29. Koutsos E.A., Klasing K.C. The acute phase response in Japanese quail (Coturnix coturnix japonica). Comp. Biochem. Physiol. 2001, 128:255-263.
30. Lee K.A. Linking immune defenses and life history at the levels of the individual and the species. Integr. Comp. Biol. 2006, 46:1000-1015.
31. Lemke H., Lange H. Is there a maternally induced immunological imprinting phase a la Konrad Lorenz?. Scand. J. Immunol. 1999, 50:348-354.
32. Littell R.C., Milliken G.A., Stroup W.W., Wolfinger R.D., Schabenberger O. SAS for Mixed Models 2006, SAS Institute Inc, Cary, NC.
33. Martins T.L.F., Roberts M.L., Giblin I., Huxham R., Evans M.R. Speed of exploration and risk-taking behavior are linked to corticosterone titres in zebra finches. Horm. Behav. 2007, 52:445-453.
34. Meyer U., Feldon J., Schedlowski M., Yee B.K. Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci. Biobehav. Rev. 2005, 29:913-947.
35. Meyer U., Feldon J., Fatemi S.H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 2009, 33:1061-1079.
36. Meyer U., Feldon J., Dammann O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation?. Pediatr. Res. 2011, 69:26R-33R.
37. Mueller B.R., Bale T.L. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 2008, 28:9055-9065.
38. Nii T., Sonoda Y., Isobe N., Yoshimura Y. Effects of lipopolysaccharide on the expression of proinflammatory cytokines and chemokines and the subsequent recruitment of immunocompetent cells in the oviduct of laying and molting hens. Poult. Sci. 2011, 90:2332-2341.
39. Nowicki S., Searcy W.A., Peters S. Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis". J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 2002, 188:1003-1014.
40. Owen-Ashley N.T., Turner M., Hahn T.P., Wingfield J.C. Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm. Behav. 2006, 49:15-29.
41. Pihlaja M., Siitari H., Alatalo R.V. Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival. J. Anim. Ecol. 2006, 75:1154-1164.
42. Romano A., Rubolini D., Caprioli M., Boncoraglio G., Ambrosini R., Saino N. Sex-related effects of an immune challenge on growth and begging behavior of barn swallow nestlings. PLoS One 2011, 6:e22805.
43. Schielzeth H., Forstmeier W. Conclusions beyond support: overconfident estimates in mixed models. Behav. Ecol. 2009, 20:416-420.
44. Schoech S.J., Rensel M.A., Heiss R.S. Short- and long-term effects of developmental corticosterone exposure on avian physiology, behavioral phenotype, cognition, and fitness: a review. Curr. Zool. 2011, 57:514-530.
45. Sol D. The cognitive-buffer hypothesis for the evolution of large brains. Cognitive Ecology II 2009, 111-134. The University of Chicago Press, Chicago. R. Dukas, J.M. Ratcliffe (Eds.).
46. Spencer K.A., Verhulst S. Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata). Horm. Behav. 2007, 51:273-280.
47. Spencer K.A., Wimpenny J.H., Buchanan K.L., Lovell P.G., Goldsmith A.R., Catchpole C.K. Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata). Behav. Ecol. Sociobiol. 2005, 58:423-428.
48. Spencer K.A., Evans N.P., Monaghan P. Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 2009, 150:1931-1934.
49. Stenzel-Poore M., Vale W.W., Rivier C. Relationship between antigen-induced immune stimulation and activation of the hypothalamic-pituitary-adrenal axis in the rat. Endocrinology 1993, 132:1313-1318.
50. Tobler M., Sandell M.I. Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata. Horm. Behav. 2007, 52:640-645.
51. Wynne O., Horvat J.C., Osei-Kumah A., Smith R., Hansbro P.M., Clifton V.L., Hodgson D.M. Early life infection alters adult BALB/c hippocampal gene expression in a sex specific manner. Stress Int. J. Biol. Stress 2011, 14:247-261.
52. Yirmiya R., Goshen I. Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun. 2011, 25:181-213.
53. Zann R.A. The Zebra Finch: A Synthesis of Field and Laboratory Studies 1996, Oxford University Press, New York.