Reproductive experience modified dendritic spines on cortical pyramidal neurons to enhance sensory perception and spatial learning in rats

Abstract

Behavioral adaptations during motherhood are aimed at increasing reproductive success. Alterations of hormones during motherhood could trigger brain morphological changes to underlie behavioral alterations. Here we investigated whether motherhood changes a rat’s sensory perception and spatial memory in conjunction with cortical neuronal structural changes. Female rats of different statuses, including virgin, pregnant, lactating, and primiparous rats were studied. Behavioral test showed that the lactating rats were most sensitive to heat, while rats with motherhood and reproduction experience outperformed virgin rats in a water maze task. By intracellular dye injection and computer-assisted 3-dimensional reconstruction, the dendritic arbors and spines of the layer III and V pyramidal neurons of the somatosensory cortex and CA1 hippocampal pyramidal neurons were revealed for closer analysis. The results showed that motherhood and reproductive experience increased dendritic spines but not arbors or the lengths of the layer III and V pyramidal neurons of the somatosensory cortex and CA1 hippocampal pyramidal neurons. In addition, lactating rats had a higher incidence of spines than pregnant or primiparous rats. The increase of dendritic spines was coupled with increased expression of the glutamatergic postsynaptic marker protein (PSD-95), especially in lactating rats. On the basis of the present results, it is concluded that motherhood enhanced rat sensory perception and spatial memory and was accompanied by increases in dendritic spines on output neurons of the somatosensory cortex and CA1 hippocampus. The effect was sustained for at least 6 weeks after the weaning of the pups.

Pregnancies alters spine number in cortical and subcortical limbic brain regions of old rats

“…Another hormone that raises its levels in the post‐pregnancy stage is prolactin, whose receptors are located in the PFC and the hippocampus, among others (Bakowska & Morrell, ; Cabrera‐Reyes, Vergara‐Castañeda, Rivero‐Segura, & Cerbón, ). Recent studies have also suggested that this hormone may improve cognition and play a neuroprotective role, showing an increase in the density of dendritic spines in the PFC and CA1 of the hippocampus during lactation (Carretero et al, ; Chen et al, ; Salmaso, Quinlan, Brake, & Woodside, ). However, to know if this hormone participates in the changes described in the present work, it is necessary to study only the effect of pregnancy without lactation to resolve this question.…”

The parental umwelt: Effects of parenthood on sensory processing in rodents

“…Most studies have focused on plasticity of S1. In Sprague–Dawley rats, for example, the density of dendritic spines on pyramidal neurones in S1 layers III and V increased during pregnancy, increased further during lactation, and declined by 6 weeks after weaning 163 . Xerri et al 164 found that the S1 representation of the nipple‐bearing regions of the ventral trunk was roughly twice as large in lactating rats as in pup‐naïve virgin females and non‐lactating primiparous females whose first litter had been removed on the day of birth.…”

Neuromodulation of maternal circuits by oxytocin

“…This implies that active nursing is required for S1 map plasticity, rather than parturition alone. In addition, increase in dendritic spine density in layer III and V pyramidal neurons of the somatosensory cortex is more prominent in lactating dams after two weeks of lactation onset, compared to pregnant females (Chen et al, 2017) but the thickness of the rat somatosensory cortex is increased almost immediately after parturition (Hamilton et al, 1977). …”

“…In contrast, map extension appears much later (at two weeks after nursing onset) but it is maintained until weaning (Rosselet et al, 2006). In addition, increased dendritic spine density in layer III and V pyramidal neurons remains up to six weeks after weaning (Chen et al, 2017). …”