Distal Pup Cues Evoke Dopamine Responses in Hormonally Primed Rats in the Absence of Pup Experience or Ongoing Maternal Behavior

Abstract

During the early postpartum period or following estrogen/progesterone administration, pups elicit maternal behavior accompanied by a robust dopamine (DA) response in the nucleus accumbens (NAC) of female rats (Afonso et al., 2009). To determine whether DA responds to ostensibly "salient" stimuli in the absence of consummatory behaviors, we examined NAC shell DA responses during restricted (stimuli placed in a perforated box), and unrestricted access to pup and food stimuli. Microdialysis samples were collected from female rats that were either cycling and postpartum (Experiment 1), or after ovariectomy and treated with empty and hormone-filled capsules (Experiment 2). Relative to nonprimed controls, hormonally primed females had suppressed basal DA concentrations and facilitated pup-evoked DA responses, regardless of stimulus access condition. In contrast, food-evoked DA responses were unchanged by hormonal priming and were greater when females consumed food compared with distal (restricted) exposure to food. During pup and food restriction conditions, the lack of any "appetitive" behavioral differences, even in pup experienced postpartum females, was surprising. In Experiment 3, we confirmed that postpartum dams allocated time equivalently to restricted pup and food stimuli, even after pup deprivation. This was in sharp contrast to the effects of deprivation during the unrestricted access phase. Together, our data demonstrated that, in hormonally primed females, distal pup cues could evoke DA responses without prior stimulus experience, ongoing maternal (behavioral) responses, or clear evidence of robust pup saliency. The results suggest that NAC DA response reflects a state of responsiveness related to basal DA suppression in the hormonally primed female rat.

Neural mechanisms of mother–infant bonding and pair bonding: Similarities, differences, and broader implications

“…Such stimuli are conceived as representing a generic pup stimulus. In the absence of DA release triggered by pup stimuli, as would occur in naive nulliparous females (see Afonso et al, 2013), the responsiveness of VP is suppressed by NA inhibition and appetitive maternal responses, such as retrieval of pups, do not occur. Due to the proposed depressing action of DA on NA, triggered by pup stimuli at the level of the hormone-primed MPOA/vBST in parturient rats, VP becomes more easily excited by BMA/BLA glutamate input, and the stimulated output of VP then promotes maternal behavior.…”

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

“…In mothers, but not in non-maternal virgins, the release of DA is considerably greater to pups than to food stimuli (Afonso et al, 2009; 2011) and in different studies relates to the duration of pup-sniffing and licking (Afonso et al, 2009; 2013). Furthermore, because the hormones of pregnancy reduce basal DA levels in the NA shell in female rats, the magnitude of pup-evoked increase in DA release is enhanced, possibly functioning to increase the saliency of the pups (Afonso et al, 2008; 2009; 2011; 2013). Blocking the resultant D1 receptor activity (but not D2 receptor activity) in the NAC greatly impairs maternal retrieval and licking of pups (Keer & Stern, 1999; Numan, Numan, Pliakou, et al, 2005a), whereas stimulating NAC D1 receptors stimulates the behaviors in nulliparous rats (Stolzenberg et al, 2007).…”

“…It is now well known that this shift in the new mothers’ behavior at parturition has a blood-borne basis (Terkel & Rosenblatt, 1972) and comes about through the action of hormones (reviewed in Bridges, 1990; Lonstein et al, 2014; Numan et al, 2006; Numan & Insel, 2003) that both reduce the females’ natural avoidance of some novel stimuli (Fleming, Cheung, Myhal, & Kessler, 1989) and specifically alters the salience of the offspring (Afonso, Shams, Jin, & Fleming, 2013; Fleming et al, 1989). Decades of research show that periparturitional hormones affect maternal behavior at different times in different species, and do so to different extents.…”

“…DA release in the core and shell regions of the NAC rises in mother rats before and during interaction with pups (Afonso et al, 2013; Afonso, King, Novakov, Burton, & Fleming, 2011; Afonso, King, Chatterjee, & Fleming, 2009; Champagne & Chretien, 2004; Hansen, Bergvall, & Nyiredi, 1993; Lavi-Avnon et al, 2008; Pereira & Morrell, 2011). In mothers, but not in non-maternal virgins, the release of DA is considerably greater to pups than to food stimuli (Afonso et al, 2009; 2011) and in different studies relates to the duration of pup-sniffing and licking (Afonso et al, 2009; 2013). Furthermore, because the hormones of pregnancy reduce basal DA levels in the NA shell in female rats, the magnitude of pup-evoked increase in DA release is enhanced, possibly functioning to increase the saliency of the pups (Afonso et al, 2008; 2009; 2011; 2013).…”

Hormonal and non-hormonal bases of maternal behavior: The role of experience and epigenetic mechanisms

“…Lactating females that engage in interactions with pups have elevated dopamine release in the ventral striatum and NA (Champagne et al, 2004;Hansen et al, 1993) and females that engage in higher levels of maternal care have increased dopaminergic projections from the VTA to the NA (Shahrokh et al, 2010). Both pup sensitization and parity result in enhanced dopamine release in response to pup cues and hormonal treatments that enhance pup sensitization also enhance DA release in the NA (Afonso et al, 2008(Afonso et al, , 2009(Afonso et al, , 2013 and stimulate signaling though D1 receptors (Stolzenberg et al, 2010). These experience-dependent changes may account for the maintenance of maternal behavior following the reduced hormone levels occurring in the postpartum period and account to the long-term enhancements in maternal behavior as a function of previous interactions with pups (Lee et al, 1999(Lee et al, , 2000.…”