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.

Figure 1.

For intact cycling/postpartum (Experiment 1) and OVX sham/hormone-treated (Experiment 2) female rats, schematics of anatomical unilateral placements (anterior to bregma, according to Paxinos and Watson, 1986) of the “active zone” (shaded lines) of microdialysis probes in the nucleus accumbens shell at three different locations.

Figure 2.

For intact cycling (n = 5) or postpartum (n = 6) female rats (Experiment 1), in vivo DA assessments before and during restricted and unrestricted access to pup and food stimuli. A, Basal DA level data (mean ± SEM) represent the average DA concentration of 3 samples collected before any stimuli exposure. Postpartum females had decreased basal DA concentrations compared with their cycling controls: ^ap < 0.05, parity difference. B, After basal collection, the time course for in vivo DA responses relative to basal DA concentrations (mean ± SEM percentage of basal concentration) during restricted access to pups and food (counterbalanced); and unrestricted access to pups, then food.

Figure 3.

Parity, stimulus, and access had selective effects on (A) DA that was unrelated to (B) behavior in the intact female rat (Experiment 1). A, DA response data (mean ± SEM) represent average percentage of basal concentration. Postpartum (n = 6) females during restriction had increased pup-evoked compared with food-evoked DA, and compared with the cycling (n = 5) group had increased pup-evoked DA, regardless of access type. When unrestricted, cycling females had increased food-evoked compared with pup-evoked DA responses. In all females, DA responses to unrestricted food were increased compared with restricted access. B, Time spent (mean ± SEM) in behaviors directed toward each of the restricted stimuli and during unrestricted pup access. Among postpartum dams, but not among cycling controls, the time spent with unrestricted access to pups was significantly greater than the time spent with pups in the box. ^ap < 0.05, parity difference for pup stimuli during a given access. ^#p < 0.05, access difference for a given parity and stimulus. *p < 0.05, stimulus difference for a given parity and access.

Figure 4.

For OVX sham-treated (n = 5) or hormone-treated (n = 7) female rats (Experiment 2), in vivo DA assessments before and during restricted and unrestricted access to pup and food stimuli. A, Basal DA level data (mean ± SEM) represent the average DA concentration of 3 samples collected before any stimuli exposure. Hormone-treated females had decreased basal DA concentrations compared with their sham controls: ^ap < 0.05, treatment difference. B, After basal collection, the time course for in vivo DA responses relative to basal DA concentrations (mean ± SEM percentage of basal concentration) during restricted access to pups and food (counterbalanced); and unrestricted access to pups, then food.

Figure 5.

Treatment, stimulus, and access had selective effects on (A) DA that were unrelated to (B) behavior in the OVX female rat (Experiment 2). A, DA response data (mean ± SEM) represent average percentage of basal concentration. Hormone-treated females (n = 7) had increased pup-evoked DA compared with the sham group (n = 5), regardless of access type; however, this effect during unrestricted access was facilitated. During restriction, hormone-treated females had increased pup-evoked compared with food- evoked DA; and during the unrestricted phase, sham-treated females showed the reverse. Both treatment groups showed increased DA responses to unrestricted food compared with restricted access. B, Time spent (mean ± SEM) in behaviors directed toward each of the restricted stimuli and during unrestricted pup access. Among hormone-treated females, but not among sham controls, the time spent with unrestricted access to pups was significantly greater than the time spent with pups in the box. ^ap < 0.05, treatment difference for pup stimuli during a given access. ^#p < 0.05, access difference for a given treatment and stimulus. *p < 0.05, stimulus difference for a given treatment and access.

Figure 6.

For recently postpartum female rats (n = 16), mean (±SEM) time spent on a given side with simultaneous access to pups and food in a restricted and then unrestricted manner (Experiment 3). Postpartum rats show altered time allocation to the stimuli only during unrestricted access and after 5 or 10 h deprivation from pup (P) and food (F) stimuli (i.e., 5P5F, 10P10F, 5P10F, 10P5F). During unrestricted access, postpartum dams spent increased time with pups and decreased time with food compared with: (1) the no deprivation condition (0P0F, average across the 4 d), (2) the restricted access to stimuli, and (3) each other. When both pup and food deprivations were maximal (i.e., 10P10F), postpartum dams had further decreases in time spent on the side associated with unrestricted food stimuli. ^dp < 0.05, different from other deprivation conditions during unrestricted access for a given stimulus. After deprivation: ^#p < 0.05, access difference for a given stimulus; and *p < 0.05, unrestricted stimulus difference.