First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or ‘mothering’ alone

Pawluski, Jodi L.; Vanderbyl, Brandy L.; Ragan, Kelsey; Galea, Liisa A.M.

doi:10.1016/j.bbr.2006.08.017

Cited by 114 publications

(95 citation statements)

References 30 publications

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“…Among other the rodent species the onset of parental behavior is known to be associated with changes in cell morphology [22,43] and neurogenesis [42,52] within the hippocampus. Furthermore, parity is associated with marked changes in hippocampal dependent memory and spatial tasks [21,24,31,45]. In light of these previous findings, the patterns of cellular proliferation and neurogenesis within the DG demonstrated in the present study are particularly interesting.…”

Section: Discussionsupporting

confidence: 68%

Pup exposure elicits hippocampal cell proliferation in the prairie vole

Ruscio

Sweeny

Hazelton

et al. 2008

Behavioural Brain Research

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The onset of parental behavior has profound and enduring effects on behavior and neurobiology across a variety of species. In some cases, mere exposure to a foster neonate (and a subsequent parental response) can have similar effects. In the present experiment we exposed adult male and female prairie voles (Microtus ochrogaster) to two foster pups for twenty minutes and quantified cell proliferation in the dentate gyrus of the hippocampus (DG), medial amygdala (MeA) and cortical amygdala (CorA). Prairie voles are highly social rodents that typically display biparental care and spontaneous parental care when exposed to foster pups. Comparisons were made between the animals that responded parentally or non-parentally towards the pups, as well as control conditions. Cell proliferation was assessed using injections of 5-bromo-2'-deoxyuridine (BrdU) and immunocytochemical localization of this marker. The phenotype of the cells was determined using double label immufluoresence for BrdU and TuJ1 (a neuronal marker). An increase in cell proliferation in the DG was seen in animals exposed to pups. However, animals that responded nonparentally had a greater number of BrdU labeled cells in the DG compared to those that responded parentally. The majority of BrdU labeled cells co-expressed TuJ1 across all groups. These results demonstrate that exposure to a foster pup, and the behavioral reaction to it (parental or non-parental) is associated with site-specific changes in cell proliferation.

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Section: Discussionsupporting

confidence: 68%

Pup exposure elicits hippocampal cell proliferation in the prairie vole

Ruscio

Sweeny

Hazelton

et al. 2008

Behavioural Brain Research

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“…A similar pattern of behavior in the elevated plus maze and forced swim test was revealed in multiparous young (3-6 months old) and mid-aged (10-12 months old) rats; however, an interesting question that was not addressed in the present study was whether differences would have been observed in primiparous vs. multiparous rats over the lifespan. Indeed, other studies have shown that, when comparing these groups for cognitive performance and hippocampal morphology, a distinctive pattern emerges in primiparous rats [18,19,37]. Although investigating effects of primiparous vs. multiparous rats would be important, this was beyond the scope of the current experiment.…”

Section: Discussionmentioning

confidence: 74%

“…Following parturition, responsiveness to pups and maternal aggression toward intruders is enhanced with parity in rats and mice [15,16]. Spatial, reference, and working memory are improved in multiparous compared to nulliparous rats [17][18][19]. Following restraint stress, rats with reproductive experience demonstrate more rearing, less freezing, and more total and central entries in an open field as well as decreased c-fos expression in limbic regions (i.e.…”

Section: Introductionmentioning

confidence: 93%

Parity and estrogen-administration alter affective behavior of ovariectomized rats

Walf

Frye

2008

Physiology & Behavior

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Evidence from clinical and basic research studies demonstrates that estradiol (E 2 ) reduces anxiety and/or depressive behavior; however, this effect is not observed in all studies. One factor that may mitigate differential responses to E 2 may be previous E 2 experience, i.e. parity. To investigate this, performance in tasks that are utilized to assess whether compounds, such as E 2 , can alter anxietylike behavior (elevated plus maze) and have anti-depressant-like effects (forced swim test) were determined. Performance of ovariectomized (ovx), young (3-6 months old) rats that had never had a litter (nulliparous) was compared to that of those that had several litters in their lifetime (multiparous) following 48 h of oil vehicle or E 2 (10 µg) administration. We predicted that E 2 would decrease anxiety-like behavior and increase anti-depressant-like effects of ovx rats and that this pattern may be influenced by parity. Multiparous rats, irrespective of E 2 -priming, had increased open arm time compared to nulliparous rats. Administration of E 2 to ovx, nulliparous or multiparous rats decreased immobility in the forced swim test compared to vehicle-administration. Together, these data suggest that E 2 can alter affective behavior and rats with greater reproductive experience have decreased anxiety-like behavior in the elevated plus maze, irrespective of E 2 -priming.

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“…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). Thus, while parity reliably enhances spatial memory, whether multiple reproductive experiences further benefits memory warrants further investigation.…”

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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First reproductive experience persistently affects spatial reference and working memory in the mother and these effects are not due to pregnancy or ‘mothering’ alone

Cited by 114 publications

References 30 publications

Pup exposure elicits hippocampal cell proliferation in the prairie vole

Pup exposure elicits hippocampal cell proliferation in the prairie vole

Parity and estrogen-administration alter affective behavior of ovariectomized rats

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

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