Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats

Physiology and Behavior

Volumn 84, Issue 5, 2005, Pages 799-806

  Lambert, K G ^a   Berry, A E ^a   Griffin, G ^b   Amory Meyers, E ^b   Madonia Lomas, L ^b   Love, Gennifer ^a   Kinsley, C H ^b  

^a RANDOLPH MACON COLLEGE   (United States)

^b UNIVERSITY OF RICHMOND   (United States)

Author keywords

Enrichment; Foraging; Pregnancy; Pup exposure; Spatial learning

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CHILDBIRTH; CONTROLLED STUDY; FEMALE; FORAGING BEHAVIOR; HABITUATION; LACTATION; LEARNING; MATERNAL BEHAVIOR; MAZE TEST; NEWBORN; NONHUMAN; NULLIPARA; PREGNANCY; PRIMIGRAVIDA; PRIORITY JOURNAL; PROGENY; RAT;

EID: 18844427516     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2005.03.012     Document Type: Article

References (42)

1. M. Numan Medial preoptic area and maternal behavior in the female rat J Comp Physiol Psychol 87 1974 746 759
2. M. Numan Neural control of maternal behavior N.A. Krasnegor R.S. Bridges Mammalian parenting 1990 Oxford New York City 231 259
3. E.A. Gould, C.S. Woolley, M. Frankfurt, and B.S. McEwen Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood J Neurosci 10 1990 1286 1291
4. C.S. Woolley, E. Gould, M. Frankfurt, and B.S. McEwen Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons Neurosci 10 1990 4035 4039
5. C.S. Woolley, and B.S. McEwen Estradiol mediates fluctuation in hippocampal synapse density during the estrus cycle in the adult rat J Neurosci 12 1992 2549 2554
6. C.S. Woolley, H.J. Wenzel, and P.A. Schwartzkroin Estradiol increases the frequency of multiple synapse boutonin proestrus rats Brain Res 703 1996 26 30
7. H.E. Scharfman, T.C. Mercurio, J.H. Goodman, M.A. Wilson, and N. MacLusky Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor J Neurosci 23 2003 11641 11652
8. C.S. Woolley, N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density J Neurosci 17 1997 1848 1859
9. S.G. Warren, A.G. Humphreys, J.M. Juraska, and W.T. Greenough LTP varies across the estrous cycle: enhanced synaptic plasticity in the hippocampal CA1 region of the adult female rat J Comp Neurol 373 1995 108 117
10. V. Znamensky, K.T. Akama, B.S. McEwen, and T.A. Milner Estrogen levels regulate the subcellular distribution of phosphorylated Akt in hippocampal CA1 dendrites J Neurosci 23 2003 2340 2347
11. P. Tanapat, N. Hastings, A.J. Reeves, and E. Gould Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat J Neurosci 19 1999 5792 5801
12. J.M. Daniel, A.J. Fader, A.L. Spencer, and G.P. Dohanich Estrogen enhances performance of female rats during acquisition of a radial arm maze Horm Behav 32 1997 217 225
13. V.N. Luine, S.T. Richards, V.Y. Wu, and K.D. Beck Estradiol enhances learning and memory in a spatial memory task and some effects levels of a monoaminergic neurotransmitters Horm Behav 34 1998 149 162
14. B. Berry, R. McMahon, and N. Gallagher Spatial learning and memory at defined points of the estrus cycle: effects on performance of a hippocampal-dependent task Behav Neurosci 111 1997 267 274
15. S.G. Warren, and J.M. Juraska Spatial and nonspatial learning across the rat estrous cycle Behav Neurosci 111 1997 259 266
16. L.A.M. Galea, M. Kavaliers, K.P. Ossenkopp, and E. Hampson Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus Horm Behav 29 1995 106 125
17. M.J. Rubinow, L.M. Arseneau, J.L. Beverly, and J.M. Juraska Effect of the estrous cycle on water maze acquisition depends on the temperature of the water Behav Neurosci 118 2004 863 868
18. D.L. Korol, E.L. Malin, K.A. Borden, R.A. Busby, and J. Couper-Leo Shifts in preferred learning strategy across the estrous cycle in female rats Horm Behav 45 2004 330 338
19. C.S. Woolley Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus Horm Behav 334 1998 140 148
20. N.L. Desmond, and W.B. Levy Ovarian steroidal control of connecting in the female hippocampus: an overview of recent experimental findings and speculations on its functional consequences Hippocampus 7 1997 239 245
21. J.A. Russell, A.J. Douglas, and C.D. Ingram Brain preparations for maternity-adaptive changes in behavioral and neuroendocrine systems during pregnancy and lactation. An overview Prog Brain Res 133 2001 1 38
22. M.C. Diamond, R.E. Johnson, and C. Ingraham Brain plasticity induced by environment and pregnancy Int J Neurosci 2 1971 171 178
23. C.H. Kinsley, L. Madonia, G. Gifford, K. Tureski, G. Griffin, and C. Lowry Motherhood improves learning and memory: neural activity in rats is enhanced by pregnancy and the demands of rearing offspring Nature 402 1999 137 138
24. A.S. Fleming, C. Kuchera, A. Lee, and G. Winocur Olfactory-based social learning varies as a function of parity in female rats Psychobiology 22 1994 37 43
25. L.A.M. Galea, B.K. Ormerod, S. Sampath, X. Kostaras, D.M. Wilkie, and M.T. Phelps Spatial working memory and hippocampal size across pregnancy in rats Horm Behav 37 2000 86 95
26. K. Matthieu, M. Meurisse, P. Poindron, R. Nowak, G. Ferreira, and M. Shayit Maternal experience influences the establishment of visual/auditory, but not olfactory, recognition of the newborn lamb by ewes at parturition Dev Psychobiol 43 2003 167 176
27. C.S. Woolley, E. Gould, and B.S. McEwen Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons Brain Res 531 1990 225 231
28. Y. Watanabe, E. Gould, and B.S. McEwen Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons Brain Res 588 1992 341 345
29. B.S. McEwen, E.A. Gould, and R.R. Sakai The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress Br J Psychiatr, Suppl 15 1992 18 23
30. R.S. Sapolsky, L.C. Krey, and B.S. McEwen Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging J Neurol 5 1985 1222 1227
31. K.G. Lambert, S.K. Buckelew, G. Stafisso-Sandoz, S. Gaffga, W. Carpenter, and J. Fisher Activity stress induces atrophy of apical dendrites of hippocampal pyramidal neurons in male rats Physiol Behav 65 1998 43 49
32. R.P. Kesner, M. Dakis, and B.L. Bolland Phencyclidine disrupts long- but not short-term memory within a spatial learning task Psychopharmacology 111 1993 85 90
33. T. Fremouw, P. Jackson-Smith, and R.P. Kesner Impaired place learning and unimpaired cue learning in hippocampal-lesioned pigeons Behav Neurosci 111 1997 963 975
34. K. Tomizawa, N. Iga, Y.F. Lu, A. Moriwaki, M. Matsushita, and S.T. Li Oxytocin imporoves long-lasting spatial memory during motherhood through MAP kinase cascade Nat Neurosci 6 2003 327 390
35. I.D. Neumann Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient, and lactating rats Prog Brain Res 133 2001 143 152
36. R.J. Windle, S. Wood, N. Shanks, P. Perks, G.L. Conde, and A.P.C. deCosta Endocrine and behavioral responses to noise stress: comparison of virgin and lactating female rats during non-disrupted maternal activity J Neuroendocrinol 9 1997 407 414
37. J. Wartella, E. Amory, A.H. MacBeth, I. McNamara, L. Stevens, and K.G. Lambert Single or multiple reproductive experiences attenuate neurobehavioral stress and fear responses in the female rat Physiol Behav 79 2003 373 381
38. K. Uvnas-Moberg Oxytocin linked anti-stress effects-the relaxation and growth response Acta Physiol Scand, Suppl 640 1997 38 42
39. B.S. McEwen, J.M. Weiss, and L.S. Schwartz Selective retention of corticosterone by limbic structures in rat brain Nature 220 1968 911 912
40. A.P.C. Da Costa, R.J. Kampa, R.J. Windle, C.D. Ingram, and S.L. Lightman Region-specific immediate-early gene expression following the administration of corticotropin releasing hormone in virgin and lactating rats Brain Res 770 1997 151 162
41. I.D. Neumann, L. Torner, and A. Wigger Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behavior in virgin, pregnant and lactating rats Neuroscience 95 1999 567 575
42. A.R. Genzanni, G. Petraglia, F. Bernardi, E. Casarosa, C. Salvestroni, and A. Tonetti Circulating levels of allopregnanolone in humans: gender, age, and endocrine influences J Clin Endocrinol Metab 83 1998 2099 2103