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 (PPD 13-14) 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 facilitates 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.

Collateral Pathways from the Ventromedial Hypothalamus Mediate Defensive Behaviors

“…Consistent with this hypothesis, activation of the PAG fiber terminals induced a weak increase of Fos expression in the AHN and vice versa (Figure S3). To eliminate the indirect recruitment of a collateral projection, we tried to block back propagation of action potentials using several approaches, including halorhodopsin (NpRH3.0), lidocaine, tetrodotoxin (TTX) and bupivacaine (Gradinaru et al, 2010; Pereira and Morrell, 2009). Among the four tested methods, injection of 0.3 μl of 4% bupivacaine completely blocked behavioral changes induced by light stimulation, and lasted for at least 45 min (Figure S6A).…”

Neuroanatomical and neurochemical basis of parenting: Dynamic coordination of motivational, affective and cognitive processes

“…Substantial evidence indicates that the mPOA regulates behavioral activation aspects of parenting through interactions with components of the mesocorticolimbic dopamine (DA) system (Numan and Smith 1984; Numan and Stolzenberg 2009). Accordingly, the motivational impairments in rat maternal behavior after interference with accumbens DA are remarkably similar to the effects of mPOA functional inactivation (Keer and Stern1999; Numan et al 2005a,b;Pereira and Morrell 2009;Silva et al 2003).…”

“…In virtually all mammalian species studied, interference with mPOA function or with mPOA lateral efferent connections severely disrupts both the onset and early postpartum expression of maternal behavior (Arrati et al 2006;Cohn and Gerall 1989;Gray and Brooks 1984;Jacobson et al 1980;Lee et al 2000;Numan 1974;Numan et al 1988;Pereira and Morrell 2009;Perrin et al 2007 Many studies have shown that the mPOA is a primary neural site where the hormones of pregnancy act to synchronize maternal responsiveness to young-related sensory stimuli at parturition (Bridges 1990;Numan 2006). The mPOA contains receptors for all the hormones involved in the rapid onset of maternal behavior, including receptors for estradiol, prolactin, and oxytocin, of which numbers increase toward the end of pregnancy and the early postpartum period (Bakowska and Morrell 1997;Champagne et al 2001;Insel 1990;Numan et al 1999;Pi and Grattan 1999a,b,c;Scott et al 2000;Shughrue et al 1997;Wagner and Morrell 1996;Walsh et al 1990).…”

Common and divergent psychobiological mechanisms underlying maternal behaviors in non-human and human mammals

“…In contrast to the detrimental effects of mPOA lesions on the expression of rat maternal behavior during early lactation, Pereira and Morrell (2009) recently found that temporary deactivation of the mPOA with an anesthetic during the second week of lactation in rats increased maternal behavior, which is a time when the behavior normally declines. These intriguing results suggest that the mPOA undergoes a functional reorganization across the postpartum period that changes in the mother’s behavior in accordance with the needs of her aging offspring, and additional studies further examining this possibility will be a great contribution to the literature.…”