Neonatal infection modulates behavioral flexibility and hippocampal activation on a Morris Water Maze task

Physiology and Behavior

Volumn 129, Issue , 2014, Pages 152-159

  Williamson, Lauren L ^a   Bilbo, Staci D ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Arc; Immediate early gene; Reversal learning; Spatial learning

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; ACTIVITY REGULATED CYTOSKELETAL-ASSOCIATED PROTEIN; CYTOSKELETON PROTEIN; NERVE PROTEIN;

ADULT; ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DENTATE GYRUS; ESCHERICHIA COLI; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS POTENTIAL; MALE; MORRIS WATER MAZE TEST; NEUROMODULATION; NEWBORN INFECTION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL LEARNING; ANIMAL; COMPLICATION; ESCHERICHIA COLI INFECTION; EXECUTIVE FUNCTION; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; MAZE TEST; MEMORY DISORDERS; METABOLISM; NEWBORN; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TASK PERFORMANCE; TIME;

ANIMALS; ANIMALS, NEWBORN; CYTOSKELETAL PROTEINS; DENTATE GYRUS; ESCHERICHIA COLI INFECTIONS; EXECUTIVE FUNCTION; IMMUNOHISTOCHEMISTRY; MALE; MAZE LEARNING; MEMORY DISORDERS; NERVE TISSUE PROTEINS; RATS, SPRAGUE-DAWLEY; TASK PERFORMANCE AND ANALYSIS; TIME FACTORS;

EID: 84896040262     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.02.033     Document Type: Article

References (53)

1. Bilbo S.D., Schwarz J.M. The immune system and developmental programming of brain and behavior. Front Neuroendocrinol 2012, 33:267-286.
2. Spencer S.J., Heida J.G., Pittman Q.J. Early life immune challenge-effects on behavioural indices of adult rat fear and anxiety. Behav Brain Res 2005, 164:231-238.
3. Amaral D., Lavenex P. Hippocampal neuroanatomy. The hippocampus book 2007, Oxford University Press, New York. P. Andersen, R.G. Morris, D. Amaral, T.V. Bliss, J. O'Keefe (Eds.).
4. Schwarz J.M. The immune system and the developing brain 2012, Morgan & Claypool Life Sciences, San Rafael, Calif.
5. Meyer U., Nyffeler M., Yee B.K., Knuesel I., Feldon J. Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice. Brain Behav Immun 2008, 22:469-486.
6. Bilbo S.D., Smith S.H., Schwarz J.M. A lifespan approach to neuroinflammatory and cognitive disorders: a critical role for glia. J Neuroimmune Pharmacol 2012, 7:24-41.
7. Han X., Li N., Meng Q., Shao F., Wang W. Maternal immune activation impairs reversal learning and increases serum tumor necrosis factor-alpha in offspring. Neuropsychobiology 2011, 64:9-14.
8. Cronise K., Kelly S.J. Maternal urinary tract infection alters water maze performance in the offspring. Neurotoxicol Teratol 2001, 23:373-379.
9. Samuelsson A.M., Jennische E., Hansson H.A., Holmang A. Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1345-R1356.
10. Chlodzinska N., Gajerska M., Bartkowska K., Turlejski K., Djavadian R.L. Lipopolysaccharide injected to pregnant mice affects behavior of their offspring in adulthood. Acta Neurobiol Exp (Wars) 2011, 71:519-527.
11. Fitting S., Booze R.M., Mactutus C.F. Neonatal intrahippocampal injection of the HIV-1 proteins gp120 and Tat: differential effects on behavior and the relationship to stereological hippocampal measures. Brain Res 2008, 1232:139-154.
12. Wallace K.L., Lopez J., Shaffery J.P., Wells A., Paul I.A., Bennett W.A. Interleukin-10/Ceftriaxone prevents E. coli-induced delays in sensorimotor task learning and spatial memory in neonatal and adult Sprague-Dawley rats. Brain Res Bull 2010, 81:141-148.
13. Bilbo S.D., Biedenkapp J.C., Der-Avakian A., Watkins L.R., Rudy J.W., Maier S.F. Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci 2005, 25:8000-8009.
14. 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.
15. Bilbo S.D., Newsum N.J., Sprunger D.B., Watkins L.R., Rudy J.W., Maier S.F. Differential effects of neonatal handling on early life infection-induced alterations in cognition in adulthood. Brain Behav Immun 2007, 21:332-342.
16. 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.
17. Williamson L.L., Sholar P.W., Mistry R.S., Smith S.H., Bilbo S.D. Microglia and memory: modulation by early-life infection. J Neurosci 2011, 31:15511-15521.
18. Bilbo S.D. Early-life infection is a vulnerability factor for aging-related glial alterations and cognitive decline. Neurobiol Learn Mem 2010, 94:57-64.
19. Bland S.T., Beckley J.T., Young S., Tsang V., Watkins L.R., Maier S.F., et al. Enduring consequences of early-life infection on glial and neural cell genesis within cognitive regions of the brain. Brain Behav Immun 2010, 24:329-338.
20. Kelly M.P., Deadwyler S.A. Acquisition of a novel behavior induces higher levels of Arc mRNA than does overtrained performance. Neuroscience 2002, 110:617-626.
21. Guzowski J.F., McNaughton B.L., Barnes C.A., Worley P.F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 1999, 2:1120-1124.
22. Pinaud R., Penner M.R., Robertson H.A., Currie R.W. Upregulation of the immediate early gene arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Brain Res Mol Brain Res 2001, 91:50-56.
23. Nedivi E. Molecular analysis of developmental plasticity in neocortex. J Neurobiol 1999, 41:135-147.
24. Worley P.F., Christy B.A., Nakabeppu Y., Bhat R.V., Cole A.J., Baraban J.M. Constitutive expression of zif268 in neocortex is regulated by synaptic activity. Proc Natl Acad Sci U S A 1991, 88:5106-5110.
25. Yamada Y., Hada Y., Imamura K., Mataga N., Watanabe Y., Yamamoto M. Differential expression of immediate-early genes, c-fos and zif268, in the visual cortex of young rats: effects of a noradrenergic neurotoxin on their expression. Neuroscience 1999, 92:473-484.
26. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14:433-445.
27. Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., et al. Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci U S A 1995, 92:5734-5738.
28. Steward O., Worley P. Local synthesis of proteins at synaptic sites on dendrites: role in synaptic plasticity and memory consolidation?. Neurobiol Learn Mem 2002, 78:508-527.
29. Steward O., Worley P.F. A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc Natl Acad Sci U S A 2001, 98:7062-7068.
30. Guzowski J.F., Lyford G.L., Stevenson G.D., Houston F.P., McGaugh J.L., Worley P.F., et al. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 2000, 20:3993-4001.
31. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2007, Academic Press.
32. Guzowski J.F., Knierim J.J., Moser E.I. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 2004, 44:581-584.
33. Guzowski J.F., Miyashita T., Chawla M.K., Sanderson J., Maes L.I., Houston F.P., et al. Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc Natl Acad Sci U S A 2006, 103:1077-1082.
34. Guzowski J.F., Worley P.F. Cellular compartment analysis of temporal activity by fluorescence in situ hybridization (catFISH). Curr Protoc Neurosci Ch 1 Unit 1.8 2001, 1.8.1-1.8.16.
35. Miyashita T., Kubik S., Haghighi N., Steward O., Guzowski J. Rapid activation of plasticity-associated gene transcription in hippocampal neurons provides a mechanism for encoding of one-trial experience. J Neurosci 2009, 29:898-906.
36. Ramirez-Amaya V., Vazdarjanova A., Mikhael D., Rosi S., Worley P.F., Barnes C.A. Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 2005, 25:1761-1768.
37. Vazdarjanova A., Guzowski J.F. Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 2004, 24:6489-6496.
38. Snyder J.S., Ferrante S.C., Cameron H.A. Late maturation of adult-born neurons in the temporal dentate gyrus. PLoS One 2012, 7:e48757.
39. Snyder J.S., Glover L.R., Sanzone K.M., Kamhi J.F., Cameron H.A. The effects of exercise and stress on the survival and maturation of adult-generated granule cells. Hippocampus 2009, 19:898-906.
40. Ramirez-Amaya V., Angulo-Perkins A., Chawla M.K., Barnes C.A., Rosi S. Sustained transcription of the immediate early gene Arc in the dentate gyrus after spatial exploration. J Neurosci 2013, 33:1631-1639.
41. Burghardt N.S., Park E.H., Hen R., Fenton A.A. Adult-born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 2012, 22:1795-1808.
42. Bilbo S.D., Barrientos R.M., Eads A.S., Northcutt A., Watkins L.R., Rudy J.W., et al. Early-life infection leads to altered BDNF and IL-1beta mRNA expression in rat hippocampus following learning in adulthood. Brain Behav Immun 2008, 22:451-455.
43. Sandi C., Loscertales M., Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci 1997, 9:637-642.
44. Bilbo S.D., Yirmiya R., Amat J., Paul E.D., Watkins L.R., Maier S.F. Bacterial infection early in life protects against stressor-induced depressive-like symptoms in adult rats. Psychoneuroendocrinology 2008, 33:261-269.
45. Ghods-Sharifi S., Haluk D.M., Floresco S.B. Differential effects of inactivation of the orbitofrontal cortex on strategy set-shifting and reversal learning. Neurobiol Learn Mem 2008, 89:567-573.
46. Chudasama Y., Bussey T.J., Muir J.L. Effects of selective thalamic and prelimbic cortex lesions on two types of visual discrimination and reversal learning. Eur J Neurosci 2001, 14:1009-1020.
47. McAlonan K., Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 2003, 146:97-103.
48. de Bruin J.P., Sanchez-Santed F., Heinsbroek R.P., Donker A., Postmes P. A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Res 1994, 652:323-333.
49. Furtado J.C., Mazurek M.F. Behavioral characterization of quinolinate-induced lesions of the medial striatum: relevance for Huntington's disease. Exp Neurol 1996, 138:158-168.
50. Gilmore J.H., Fredrik Jarskog L., Vadlamudi S., Lauder J.M. Prenatal infection and risk for schizophrenia: IL-1beta, IL-6, and TNFalpha inhibit cortical neuron dendrite development. Neuropsychopharmacology 2004, 29:1221-1229.
51. Weissenbock H., Hornig M., Hickey W.F., Lipkin W.I. Microglial activation and neuronal apoptosis in Bornavirus infected neonatal Lewis rats. Brain Pathol 2000, 10:260-272.
52. Iida R., Yamada K., Mamiya T., Saito K., Seishima M., Nabeshima T. Characterization of learning and memory deficits in C57BL/6 mice infected with LP-BM5, a murine model of AIDS. J Neuroimmunol 1999, 95:65-72.
53. Williamson L.L., Bilbo S.D. Chemokines and the hippocampus: a new perspective on hippocampal plasticity and vulnerability. Brain Behav Immun 2013, 30:186-194.