Parental experience is linked with lower vasopressin receptor 1a binding and decreased postpartum androgens in titi monkeys

Abstract

Parenting induces many neurological and behavioral changes that enable parents to rear offspring. Vasopressin plays an important role in this process via its effects on cognition, affect, and neuroplasticity, and in some cases, via interactions with decreased parental androgens. Thus far, the role of these hormones has been primarily studied in rodents. To address this gap, we explored vasopressin receptors and androgens in titi monkeys, a pair-bonding and biparental primate species. In Studies 1 and 2, we used receptor autoradiography to correlate arginine vasopressin receptor 1a (AVPR1a) binding in the hippocampus (Study 1, n = 10) and the rest of the forebrain (Study 2, n = 23) with parental status, parental experience, parity, infant carrying, and pair affiliation. We found that parents exhibited lower AVPR1a binding than non-parents throughout most brain regions assessed, with especially strong effects in the hippocampus (β = -.61), superior colliculus (β = -.88), lateral septum (β = -.35), and medial preoptic area (β = -.29). The other measures of parental experience also tended to be negatively associated with AVPR1a binding across different brain regions. In Study 3 (n = 44), we compared pre- and postpartum urinary androgen levels in parents and non-parents and found that mothers exhibited a sustained androgen decrease across 3-4 months postpartum (relative to 3 months prepartum; β ranged from -.72 to -.62 for different comparisons). For males, we found that multiparous fathers exhibited decreased androgen levels at 1-2 weeks postpartum (β = -.25) and at 3-4 months postpartum (β = -.40) compared to the prepartum, indicating both immediate and long-term reductions with subsequent paternal experience. Together, the results of this study suggest that decreases in AVPR1a binding and circulating androgens are associated with parental behavior and physiology in titi monkeys.

Keywords: AVPR1a binding; infant care; pair bonding; parental androgen suppression; parental brain.

Figure 1.

Brain Regions Quantified in Study 1. The figure shows the brain regions quantified in Study 1 on three representative AVPR1a autoradiograms (the image on the left side shows the unlabeled autoradiogram, and the image on the right shows the same autoradiogram with the regions of interest that we quantified). Ref. Region (reference region) indicates the approximate segment of white matter that we sampled to correct AVPR1a binding density values from each section for background binding levels. The black line at the bottom left corner of each panel indicates 25 microns. See Table 2 for a full list of abbreviations and for how the regions were grouped for analyses.

Figure 2.

Brain Regions Quantified in Study 2. The figure shows the brain regions quantified in Study 2 on three representative AVPR1a autoradiograms (the image on the left side shows the unlabeled autoradiogram, and the image on the right shows the same autoradiogram with the regions of interest that we quantified). Panels A and B correspond to a section targeting the frontal cortex, and panels C and D correspond to a section targeting the NAcc. Panels E and F correspond to a section targeting the MPOA. Ref. Region (reference region) indicates the approximate segment of white matter that we sampled to correct AVPR1a binding density values from each section for background binding levels. The black line at the bottom left corner of each panel indicates 25 microns. See Table 2 for a full list of abbreviations and for how the regions were grouped for analyses.

Figure 3.

Beta Estimates of Primary AVPR1a Binding Analyses (Studies 1–2). The figure shows the overall negative relationship (indicated by the standardized beta estimates on the x axis) between parental status (the first panel) and AVPR1a binding in each grouping of brain regions (the y axis). The results for active parental status (active parents vs. retired parents), parity (multiparous vs. primiparous parents), total parenting time, sex, infant carrying (yellow columns), and each pair affiliation state (controlling for parental status; the green columns) are also shown. Negative estimates indicate lower AVPR1a binding in parents (for parental status), active parents (for active parental status), multiparous parents (for parity), and males (for sex). Estimates from Study 1 (S1) are depicted with circles and estimates from Study 2 (S2) are depicted with diamonds. The overall effect sizes for each study are shown at the bottom of each panel (the darker grey segments of the panels). The error bars represent the 95% confidence intervals of each estimate. The solid black vertical line indicates a beta estimate of 0 (no association); confidence intervals that overlapped this line were not significant (ns, indicated by white points) and confidence intervals that did not were significant (p < .05, indicated by dark grey points).

Figure 4.

Effects of Dichotomous Parental Status, Parity, and Active Parental Status on Lower AVPR1a Binding (Studies 1–2). The graph shows the effects of dichotomous parental status, parity, and active parental status (labeled on the x axis) on lower AVPR1a binding (on the y axis) for selected brain regions of interest (indicated in the panel titles) in Study 1 (S1) and Study (S2). Darker-colored bars indicate the group with the most parental experience (i.e., parents, multiparous parents, and active parents). Error bars indicate ± 1 standard error. Asterisks (*) indicate the comparison was significant at p < 0.05. Abbreviations: Primip. Indicates primiparous parents, Multip. Indicates multiparous parents, Act. P indicates active parents, Ret. P indicates retired parents. The data can be further visualized using the following interactive R Shiny dashboards for Study 1 (https://alexander-baxter.shinyapps.io/Titi_AVPR1a_Baxter2023_Study1/) and Study 2 (https://alexander-baxter.shinyapps.io/Titi_AVPR1a_Baxter2023_Study2/).

Figure 5.

Urinary Androgens in Parents and Non-Parents Across the Pre- and Post-Partum (Study 3). The graph shows changes in average urinary androgen levels (on the y axis) across sampling time point bins (on the x axis) by parental status (the top two panels) and by parity level (the bottom two panels). Data for males are shown in the left column and data for females are shown in the right column. Error bars indicate ±1 standard error. The black vertical dashed line delineates the prepartum sampling time point from the postpartum sampling time points. For the analyses of parental status, data from all subjects were used (the parent group included both primiparous and multiparous parents; however, the non-parent group did not include the two high androgen outliers for the female non-parents at the 2 month and 3–4-month time points). For the analyses by parity, only data from subjects that were sampled once as a primiparous parent and once as a multiparous parent were used. Note, the error bars shown on the graph do not necessarily reflect how the standard errors were calculated in the multilevel analyses (which included random effects for Subject ID and Offspring ID). This is why some of the significant comparisons reported in the results section have overlapping error bars in this graph, and why some of the comparisons that have non-overlapping error bars in this graph were not significantly different in the analyses. See the Results section for a full summary of which comparisons were significantly different. Abbreviations: M indicates months, W indicates weeks, Pre indicates prepartum, Post indicates postpartum.