Maternal Experience Produces Long-Lasting Behavioral Modifications in the Rat.

Love, Gennifer; Torrey, Nicole; McNamara, Ilan; Morgan, Melissa; Banks, Margaret; Hester, Naomi W.; Glasper, Erica R.; DeVries, A. Courtney; Kinsley, Craig Howard; Lambert, Kelly G.

doi:10.1037/0735-7044.119.4.1084

Cited by 126 publications

(109 citation statements)

References 53 publications

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“…Dams having had at least one litter typically outperform virgins on tasks of cognitive performance (Kinsley et al 1999, Love et al 2005, Bodensteiner et al 2006, Pawluski et al 2006a, Macbeth et al 2008. Primiparous or multiparous dams are found to have a greater spinal density on hippocampal dendrites compared with nulliparous dams (Pawluski & Galea 2006).…”

Section: Discussionmentioning

confidence: 99%

“…The present study supports these findings, demonstrating a greater cognitive performance in multiparous, compared with nulliparous, dams. It cannot be ignored, however, that many studies to date have either found no cognitive and/or morphological differences between primiparous and multiparous dams, or have found differences that favor primiparous over multiparous dams (Wartella et al 2003, Love et al 2005, Pawluski & Galea 2006, Pawluski et al 2006a. One explanation may be that the beneficial effects of multiple pregnancies do not summate in a long-term manner.…”

mentioning

confidence: 88%

“…For instance, rats that have had one or more litters outperform virgin rats in either probe or competitive trials of a dry land maze (Love et al 2005) and make fewer errors in a radial arm maze than do virgins (Kinsley et al 1999, Pawluski et al 2006a. These data are of particular interest because they suggest that a prolonged exposure to steroids can have long-lasting (even life-long) effects on cognition.…”

Section: Introductionmentioning

confidence: 94%

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Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks

Paris¹,

Frye²

2008

Reproduction

114

105

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Ovarian hormone elevations are associated with enhanced learning/memory. During behavioral estrus or pregnancy, progestins, such as progesterone (P 4 ) and its metabolite 5a-pregnan-3a-ol-20-one (3a,5a-THP), are elevated due, in part, to corpora luteal and placental secretion. During 'pseudopregnancy', the induction of corpora luteal functioning results in a hormonal milieu analogous to pregnancy, which ceases after about 12 days, due to the lack of placental formation. Multiparity is also associated with enhanced learning/memory, perhaps due to prior steroid exposure during pregnancy. Given evidence that progestins and/or parity may influence cognition, we investigated how natural alterations in the progestin milieu influence cognitive performance. In Experiment 1, virgin rats (nulliparous) or rats with two prior pregnancies (multiparous) were assessed on the object placement and recognition tasks, when in high-estrogen/P 4 (behavioral estrus) or low-estrogen/P 4 (diestrus) phases of the estrous cycle. In Experiment 2, primiparous or multiparous rats were tested in the object placement and recognition tasks when not pregnant, pseudopregnant, or pregnant (between gestational days (GDs) 6 and 12). In Experiment 3, pregnant primiparous or multiparous rats were assessed daily in the object placement or recognition tasks. Females in natural states associated with higher endogenous progestins (behavioral estrus, pregnancy, multiparity) outperformed rats in low progestin states (diestrus, non-pregnancy, nulliparity) on the object placement and recognition tasks. In earlier pregnancy, multiparous, compared with primiparous, rats had a lower corticosterone, but higher estrogen levels, concomitant with better object placement performance. From GD 13 until post partum, primiparous rats had higher 3a,5a-THP levels and improved object placement performance compared with multiparous rats.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 88%

Section: Introductionmentioning

confidence: 94%

See 1 more Smart Citation

Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks

Paris¹,

Frye²

2008

Reproduction

114

105

View full text Add to dashboard Cite

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“…Parous females also have decreased anxiety-like behavior as measured in the open field (Wartella et al, 2003) and on the elevated plus maze (Neumann, 2001;Lonstein, 2005). Furthermore, recent work indicates that multiparity continues to decrease anxiety as measured on the elevated plus maze up to 18 months after last weaning (Love et al, 2005), indicating effects on behavior throughout the female's lifespan.…”

mentioning

confidence: 92%

“…Interestingly, parous females (primiparous and multiparous) continue to outperform nulliparous females on a dryland version of the Morris water maze at 6, 12, 18 and 24 months of age (Gatewood et al, 2005), and are significantly faster than NP females to find a baited food well at 13 months of age (Love et al, 2005), long past their last reproductive experience. However, one recent study indicated that, compared to NP females, primiparous but not multiparous females have significantly better spatial memory on the radial arm maze (Pawluski et al, 2006b).…”

mentioning

confidence: 99%

Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF)

Macbeth

Scharfman

MacLusky

et al. 2008

Hormones and Behavior

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Recognition memory and anxiety were examined in nulliparous (NP: 0 litters) and multiparous (MP: 5-6 litters) middle-aged female rats (12 months old) to assess possible enduring effects of multiparity at least 3 months after last litter was weaned. MP females performed significantly better than NP females on the non-spatial memory task, object recognition, and the spatial memory task, object placement. Anxiety as measured on the elevated plus maze did not differ between groups. Monoaminergic activity and levels were measured in prefrontal cortex, CA1 hippocampus, CA3 hippocampus, and olfactory bulb (OB). NP and MP females differed in monoamine concentrations in the OB only, with MP females having significantly greater concentrations of dopamine and metabolite DOPAC, norepinephrine and metabolite MHPG, and the serotonin metabolite 5-HIAA, as compared to NP females. These results indicate a long-term change in OB neurochemistry as a result of multiparity. Brain-derived neurotrophic factor (BDNF) was also measured in hippocampus (CA1, CA3, dentate gyrus), and septum. MP females had higher BDNF levels in both CA1 and septum; as these regions are implicated in memory performance, elevated BDNF may underlie the observed memory task differences. Thus, MP females (experiencing multiple bouts of pregnancy, birth, and pup rearing during the first year of life) displayed enhanced memory task performance, but equal anxiety responses, as compared to NP females. These results are consistent with previous studies showing long-term changes in behavioral function in MP, as compared to NP, rats, and suggest that alterations in monoamines and a neurotrophin, BDNF, may contribute to the observed behavioral changes.

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Paternal experience suppresses adult neurogenesis without altering hippocampal function in Peromyscus californicus

Glasper

Kozorovitskiy

Pavlic

et al. 2011

J of Comparative Neurology

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Paternal care is rare among mammals, occurring in ≈6% of species. California mice (Peromyscus californicus) are unusual; fathers participate extensively in raising their young and display the same components of parental care as mothers, with the exception of nursing. Parenting is a complex experience, having stressful and enriching aspects. The hippocampus is sensitive to experience and responds to both stress and environmental enrichment with changes in structure and function. In rats, where females care exclusively for offspring, parenting is associated with suppressed hippocampal adult neurogenesis. Since this effect has been causally linked to lactation, it is unlikely that fathers would show a similar change. To investigate this issue, we examined adult neurogenesis in the hippocampus of California mouse fathers compared to males without pups and observed reduced adult neurogenesis. Similar effects were found in California mouse mothers. Next, we investigated whether behaviors linked to the hippocampus, namely, object recognition and novelty-suppressed feeding, were altered in fathers, and observed no substantial changes. During caregiving, suppressed adult neurogenesis does not appear to be related to changes in behaviors associated with the hippocampus, although it is possible that there are other effects on hippocampal function.

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Maternal Experience Produces Long-Lasting Behavioral Modifications in the Rat.

Cited by 126 publications

References 53 publications

Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks

Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks

Effects of multiparity on recognition memory, monoaminergic neurotransmitters, and brain-derived neurotrophic factor (BDNF)

Paternal experience suppresses adult neurogenesis without altering hippocampal function in Peromyscus californicus

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