The influence of offspring, parity, and oxytocin on cognitive flexibility during the postpartum period

Abstract

Pregnancy and the postpartum period are times of profound behavioral change including alterations in cognitive function. This has been most often studied using hippocampal-dependent tasks assessing spatial learning and memory. However, less is known about the cognitive effects of motherhood for tasks that rely on areas other than the hippocampus. We have previously shown that postpartum females perform better on the extradimensional phase of an attentional set shifting task, a measure of cognitive flexibility which is dependent on the medial prefrontal cortex (mPFC). The present experiments aimed to extend this work by examining the importance of postpartum stage as well as offspring and parity in driving improved mPFC cognitive function during motherhood. We also examined whether the neuropeptide oxytocin, which plays a role in regulating numerous maternal functions, mediates enhanced cognitive flexibility during motherhood. Our results demonstrate that compared to virgin females, cognitive flexibility is enhanced in mothers regardless of postpartum stage and is not affected by parity since both first (primiparous) and second (biparous) time mothers showed the enhancement. Moreover, we found that improved cognitive flexibility in mothers requires the presence of offspring, as removal of the pups abolished the cognitive enhancement in postpartum females. Lastly, using an oxytocin receptor antagonist, we demonstrate that oxytocin signaling in the mPFC is necessary for the beneficial effects of motherhood on cognitive flexibility. Together, these data provide insights into the temporal, experiential and hormonal factors which regulate mPFC-dependent cognitive function during the postpartum period.

Figure 1

(Top) Schematic diagram of the attentional set shifting apparatus. A fixed Plexiglas panel divided the distal third of the arena into two sections, and a digging pot was placed in each section. A removable divider separated the proximal third of the arena from the rest, forming a start box. To begin a trial, a rat was placed in the start box, and the divider lifted. (Bottom) Timeline for attentional set shifting procedure.

Figure 2

Mothers during the second (PD10-11) and third (PD20-21) postpartum weeks required fewer trials to reach criteria on the EDS phase of the AST as compared to virgin females and PD10-11 postpartum females whose offspring were removed shortly after birth. All groups performed similarly on the SD, CD, IDS and REV phases of the task. Bars represent mean + SEM, * p < 0.05.

Figure 3

Both primiparous and biparous mothers during the second postpartum week (PD10-11) required fewer trials to reach criteria on the EDS phase than virgin females. Both groups of mothers performed similarly to virgins on all other phases of the task. Bars represent mean + SEM, * p < 0.05.

Figure 4

(Left) PD10-11 mothers that received a bilateral infusion of an OT-R antagonist into the mPFC immediately before the EDS phase of the attentional set shifting task required more trials to reach criterion than PD10-11 mothers that received a bilateral saline infusion. The number of trials to reach criterion for the other task phases did not differ between saline and OT-R antagonist mothers. (Right) Locations of cannula placements within the mPFC. White circles = saline; Black circles = OT-R antagonist. Bars represent mean + SEM, * p < 0.05.