Complex patterns of dopamine‐related gene expression in the ventral tegmental area of male zebra finches relate to dyadic interactions with long‐term female partners

Abstract

Dopaminergic projections from the ventral tegmental area (VTA) to multiple efferent targets are implicated in pair bonding, yet the role of the VTA in the maintenance of long-term pair bonds is not well characterized. Complex interactions between numerous neuromodulators modify activity in the VTA, suggesting that individual differences in patterns of gene expression in this region may explain individual differences in longterm social interactions in bonded pairs. To test this hypothesis we used RNA-seq to measure expression of over 8000 annotated genes in male zebra finches in established male-female pairs. Weighted gene co-expression network analysis identified a gene module that contained numerous dopamine-related genes with TH found to be the most connected gene of the module. Genes in this module related to male agonistic behaviors as well as bonding-related behaviors produced by female partners.Unsupervised learning approaches identified two groups of males that differed with respect to expression of numerous genes. Enrichment analyses showed that many dopamine-related genes and modulators differed between these groups, including dopamine receptors, synthetic and degradative enzymes, the avian dopamine transporter and several GABA-and glutamate-related genes. Many of the bonding-related behaviors closely associated with VTA gene expression in the two male groups were produced by the male's partner, rather than the male himself. Collectively, results highlight numerous candidate genes in the VTA that can be explored in future studies and raise the possibility that the molecular/genetic organization of the VTA may be strongly shaped by a social partner and/or the strength of the pair bond.

After the Honeymoon: Neural and Genetic Correlates of Romantic Love in Newlywed Marriages

“…Although one study showed dopamine release in the prefrontal cortex while viewing the face of a new romantic partner (Takahashi et al, 2015), here we used genetic markers to confirm direct involvement of dopamine in the midbrain/VTA. Interestingly, our results are consistent with a recent study which showed that dopamine-related gene expression in the VTA of male zebra finches was associated with pair-bonding behaviors (nesting and courtship) of their female pair (Alger et al, 2020). Also, individual differences in social interactions in long-term zebra finch pairs Other colored regions did not meet the statistical requirements for whole-brain analysis or were not an ROI.…”

Differences in dopamine and opioid receptor ratios in the nucleus accumbens relate to physical contact and undirected song in pair-bonded zebra finches.

“…The observer conducted daily 20 min observations of each established pair in a random order for 5 days (Days 17–21 after pairing). We selected this observation frequency and duration based on our past studies in European starlings and zebra finches in which 20 min observations across 4–5 days revealed strong correlations between behavior and neuronal markers, including mRNA (e.g., Alger et al, 2011, 2020; DeVries et al, 2015; Kelm et al, 2011) and a survey of observation durations in zebra finches which range from 5 to 15 to 30 min in different studies (Banerjee et al, 2013; Bolund et al, 2012; Tomaszycki & Adkins-Regan, 2006). Observations began between 30 min and 5 h 30 min after the lights turned on.…”

“…DIFFERENCES IN DOPAMINE AND OPIOID RECEPTOR RATIOS Alger et al, 2011Alger et al, , 2020DeVries et al, 2015;Kelm et al, 2011) and a survey of observation durations in zebra finches which range from 5 to 15 to 30 min in different studies (Banerjee et al, 2013;Bolund et al, 2012;Tomaszycki & Adkins-Regan, 2006). Observations began between 30 min and 5 h 30 min after the lights turned on.…”

“…In contrast to the numerous studies on courtship and the formation of pair bonds in both birds and mammals, less is known about the neural regulation of behaviors that occur after pair bonding that reinforce the bond and contribute to reproductive success (Aragona et al, 2006; Lowrey & Tomaszycki, 2014; Prior & Soma, 2015; Resendez et al, 2012). A recent RNA-seq study on male zebra finches with long-term female partners indicated that male pair-bond related behaviors and the behaviors of his partner related to a gene module in the male’s ventral tegmental area (VTA) that contains many dopamine-related genes (Alger et al, 2020). The VTA sends dopaminergic projections to several areas, including the nucleus accumbens (NAc).…”

Sex differences in 3D: Differentiation, dimorphism, or dependence?

“…But how do females select a male partner? Alger et al address this question in zebra finches, using computational approaches to identify subgroups of males that exhibit distinct patterns of gene expression in the ventral tegmental area (VTA). Intriguingly, these divisions were most tightly predictive of the behavior of the male's female partner, even more so than the behavior of the male himself.…”