The changing role of the medial preoptic area in the regulation of maternal behavior across the postpartum period: facilitation followed by inhibition

Abstract

Maternal behavior in rats undergoes considerable plasticity in parallel to the developmental stage of the pups, resulting in distinct patterns of maternal behavior and care at different postpartum time points. The medial preoptic area (mPOA) of the hypothalamus is one critical neural substrate underlying the onset and early expression of maternal behavior in rats but little is known about its specific functional role in the evolving expression of maternal behavior across the postpartum period. The present study uses a reversible local neural inactivation method to examine the role of the mPOA in the regulation of maternal behavior throughout the postpartum period, particularly extending into the late postpartum, a little examined period. This approach avoids the compensatory plasticity in CNS that occurs after permanent lesions, and allows the repeated testing of same individuals. Early (PPD7-8) and late (PPD13-14) postpartum maternal behavior was evaluated in female rats following infusions of bupivacaine or vehicle into the mPOA or into control areas. As expected, mPOA inactivation severely but transiently disrupted early postpartum maternal behavior whereas infusion of vehicle or inactivation of adjacent control sites did not. Later in the postpartum period, however, transient mPOA inactivation facilitated the expression of maternal behaviors, highly contrasting the behavioral expression levels characteristic of late postpartum. Results strongly demonstrate that the mPOA is differentially engaged throughout postpartum in orchestrating appropriate maternal responses with the developmental stage of the pups.

Figure 1

Schematic representation, based on the microscopic analysis of cresyl violet-stained sections, of infusion sites for female rats tested for maternal behavior following infusion treatments. (A) mPOA cannulated postpartum females tested at both early and late postpartum stages; (B) mPOA cannulated postpartum females tested only in late postpartum, and (C) postpartum females with cannulae located immediately dorsal to the mPOA (dorsal control). Circles represent the most ventral extent of the injector tracks in the brain. Plates were taken from the atlas of Paxinos and Watson (1997). Numbers beside each plate indicate the distance from bregma in millimeters.

Figure 2

Effect of transient inactivation of the mPOA on median ± SIQR number of active maternal responses over a 30 min-behavioral test. Female rats were tested on early PPD 7 and 8 and then again on late PPD13 and 14. Data shown is for the behavioral control females and for mPOA cannulated females following either vehicle or inactivation treatment with 2% bupivacaine. *Significant difference at P<0.05 on bupivacaine versus saline test days (within-group comparison, Wilcoxon matched-pairs signed-ranks test) and versus the behavioral control females (between-group comparison, Mann-Whitney U test).

Figure 3

Replication of late postpartum group: Effect of transient inactivation of the mPOA on median ± SIQR number of active maternal responses over a 30 min-behavioral test. An additional independent group of mPOA cannulated female rats was tested only on late PPD13 and 14, following either vehicle or bupivacaine treatment. *Significant difference at P<0.05 on bupivacaine versus saline test days (within-group comparison, Wilcoxon matched-pairs signed-ranks test) and versus the behavioral control females (between-group comparison, Mann-Whitney U test).

Figure 4

Effect of transient inactivation of dorsal sites to the mPOA on median ± SIQR number of active maternal responses over a 30 min-behavioral test. No significant differences in early and/or late postpartum maternal behavior were found in females following vehicle and bupivacaine treatment.

Figure 5

A. Locomotor activity (mean ± SEM) graphed in 5-min intervals over a 60min-test session for postpartum females with bilateral infusions of either 2% bupivacaine or vehicle into the mPOA. B. Schematic representation, based on the microscopic analysis of cresyl violet-stained sections, of infusion sites for female rats tested for locomotor activity. Plates were taken from the atlas of Paxinos and Watson (1997). Numbers beside each plate indicate the distance from bregma in millimeters.