Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life

Casolini, Paola; Cigliana, Giovanni; Alemà, G; Ruggieri, Valentina; Angelucci, L.; Catalani, A.

doi:10.1016/s0306-4522(96)00668-9

Cited by 89 publications

(65 citation statements)

References 40 publications

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“…However, chronic central blockade of MR in rats does impair spatial memory in the water maze (Yau et al 1999). Moreover, our data are consistent with the previously published studies, whereby hippocampal MR expression is increased and memory improved, following chronic antidepressant treatment (Casolini et al 1997) or CORT treatment during lactation (Yau et al 1995).…”

Section: Discussionsupporting

confidence: 92%

Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches ( Taeniopygia guttata ) selected for acute high corticosterone response to stress

et al. 2006

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In mammals, stress hormones have profound influences on spatial learning and memory. Here, we investigated whether glucocorticoids influence cognitive abilities in birds by testing a line of zebra finches selectively bred to respond to an acute stressor with high plasma corticosterone (CORT) levels. Cognitive performance was assessed by spatial and visual one-trial associative memory tasks. Task performance in the high CORT birds was compared with that of the random-bred birds from a control breeding line. The birds selected for high CORT in response to an acute stressor performed less well than the controls in the spatial task, but there were no significant differences between the lines in performance during the visual task. The birds from the two lines did not differ in their plasma CORT levels immediately after the performance of the memory tasks; nevertheless, there were significant differences in peak plasma CORT between the lines. The high CORT birds also had significantly lower mineralocorticoid receptor mRNA expression in the hippocampus than the control birds. There was no measurable difference between the lines in glucocorticoid receptor mRNA density in either the hippocampus or the paraventricular nucleus. Together, these findings provide evidence to suggest that stress hormones have important regulatory roles in avian spatial cognition.

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Section: Discussionsupporting

confidence: 92%

Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches ( Taeniopygia guttata ) selected for acute high corticosterone response to stress

et al. 2006

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“…It is therefore possible that the behavioural changes found here among the adult offspring of Babesia-treatment mothers were mediated by maternal corticosterone through foetal testosterone modulation. Interestingly, other studies have also found that offspring behavioural changes due to maternal stress are not evident before weaning in either the mother or offspring, but emerge later when the offspring reaches adulthood (Casolini et al 1997), as was the case in our study (see the electronic supplementary material).…”

Section: Discussionsupporting

confidence: 84%

Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy

et al. 2008

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Maternal experience before and during pregnancy is known to play a key role in offspring development. However, the influence of social cues about disease in the maternal environment has not been explored. We indirectly exposed pregnant mice to infected neighbours by housing them next to non-contagious conspecifics infected with Babesia microti. We examined the effect of this indirect immunological exposure on both the females and their adult offspring. Exposed females had higher levels of serum corticosterone and increased kidney growth compared with those with uninfected neighbours. These exposed females subsequently produced offspring that as adults showed an accelerated immune response to B. microti and less aggression in social groups. We suggest that ambient information regarding disease is used adaptively to maximize offspring survival and reproductive success in a challenging environment. Our results shed light on the impact of social information and maternal effects on life histories, and have important consequences for our understanding of epidemiology and individual disease susceptibility in humans and other animals. They also lead us to question the suitability of some laboratory housing conditions during experimental procedures, which may impact negatively upon both animal welfare and the validity of animal science.

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“…The hippocampus, a key brain structure underlying spatial learning (Morris et al, 1982;Sutherland et al, 1982), is both a major target of the stress hormone corticosterone (CORT), an end product of the HPA axis, and one of the major driving forces that provide input to the HPA axis (McEwen and Sapolsky, 1995;de Kloet et al, 1998). Early-life stimulation and differences in maternal characteristics both result in long-lasting changes in the HPA axis and enhancement in spatial learning (Meaney et al, 1988;Catalani et al, 1993Catalani et al, , 2000Casolini et al, 1997;Liu et al, 1997;Tang, 2001;Tang et al, 2003Tang et al, , 2006Akers et al, 2008). What remains controversial is the relative contribution of the neonatal stimulation itself and maternal influence toward the programming of the adult function (Denenberg, 1999;Pryce and Feldon, 2003;Macrì and Würbel, 2006;Parker et al, 2006;Tang et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Neonatal Novelty-Induced Persistent Enhancement in Offspring Spatial Memory and the Modulatory Role of Maternal Self-Stress Regulation

Tang

Reeb‐Sutherland²,

Yang³

et al. 2011

J. Neurosci.

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Development of spatial memory in the rat is influenced by both maternal and nonmaternal aspects of the postnatal environment. Yet it remains poorly understood how these two aspects of the postnatal environment interact to program offspring cognitive development. By considering the joint influence of neonatal environmental novelty and maternal self-stress regulation on the development of spatial memory function in Long-Evans hooded rats, we show a persistent neonatal novelty-induced enhancement in spatial reference and working memory functions among the same individual offspring from juvenility to adulthood and a contrasting transient maternal modulatory influence on this novelty-related enhancement present during only juvenility. Specifically, at and only at juvenility, for mothers with good self-stress regulation as indexed by a low circulating basal corticosterone level, offspring showed a novelty-induced enhancement in spatial memory function, whereas for mothers with poor self-stress regulation, indexed by a high basal corticosterone level, offspring showed little enhancement or even small impairments. These findings indicate that maternal and nonmaternal postnatal environments exert separate but interacting influences on offspring cognitive development and support a maternal modulation model of cognitive development that considers maternal self-stress regulation as an important factor among the multitude of maternal influences.

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Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life

Cited by 89 publications

References 40 publications

Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches ( Taeniopygia guttata ) selected for acute high corticosterone response to stress

Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches ( Taeniopygia guttata ) selected for acute high corticosterone response to stress

Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy

Neonatal Novelty-Induced Persistent Enhancement in Offspring Spatial Memory and the Modulatory Role of Maternal Self-Stress Regulation

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