Neurobiological traces of grief: Examining the impact of offspring loss after birth on rat mothers’ brain and stress-coping behavior in the first week postpartum

Luisa Demarchi, Alice Sanson, Oliver J. Bosch
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Abstract

The bond between a mother and her infant is one of the strongest social bonds found in mammals. Consequently, the loss of an infant has immense psychological and physiological effects on the caregiver. Despite the significance of this bereavement, only a few studies have investigated the neurobiological impact of offspring loss in mothers. In an approach to fill this gap, we studied the effects of losing all pups the day after giving birth on rat mothers' brain and stress-coping behavior. Specifically, dams experienced 1-, 3-, or 6-days of total offspring loss. We analyzed the neuronal activity and oxytocin receptor (OXT-R) binding in the brain limbic and maternal network regions, as well as the stress response and stress-coping strategies. Following 1 day of loss, the mothers' neuronal activity increased in the limbic system resulting in a positive correlation between the prelimbic cortex and basolateral amygdala, while OXT-R binding was decreased in the central amygdala following up to 3 days of loss. At all three timepoints, plasma corticosterone concentrations did not differ either under basal conditions or following stressor exposure. Remarkably, following 6 days of offspring loss, the mothers showed a significant increase in passive stress-coping behavior, marking the first evidence of offspring loss affecting rat mothers' stress-coping behavior. Our results emphasize the significant impact of offspring loss on the mothers’ neuronal activity and brain oxytocin system thereby providing novel insight into the short-term neurobiological traces of grief and paving new avenues for future research in this field.

悲伤的神经生物学痕迹:研究出生后失去后代对大鼠母亲产后第一周大脑和压力应对行为的影响
母婴之间的纽带是哺乳动物中最牢固的社会纽带之一。因此,失去婴儿会对照顾者产生巨大的心理和生理影响。尽管这种丧子之痛意义重大,但只有少数研究调查了母亲失去后代对神经生物学的影响。为了填补这一空白,我们研究了产后第二天失去所有幼崽对大鼠母亲大脑和压力应对行为的影响。具体来说,母鼠经历了 1 天、3 天或 6 天的完全丧失后代。我们分析了大鼠大脑边缘和母性网络区域的神经元活动和催产素受体(OXT-R)结合情况,以及应激反应和应激应对策略。失去孩子1天后,母亲边缘系统的神经元活动增加,导致前边缘皮层和杏仁核基底外侧之间的正相关,而失去孩子3天后,杏仁核中央的OXT-R结合减少。在所有三个时间点上,血浆皮质酮浓度在基础条件下和暴露于应激源后都没有差异。值得注意的是,在失去后代6天后,大鼠母亲的被动压力应对行为显著增加,这是失去后代影响大鼠母亲压力应对行为的首个证据。我们的研究结果强调了失去后代对母鼠神经元活动和脑催产素系统的重大影响,从而为研究悲伤的短期神经生物学痕迹提供了新的视角,并为这一领域的未来研究铺平了新的道路。
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