Prairie Voles: Recovering from a broken heart
A molecular signature found in the brains of monogamous prairie voles begins to decay after prolonged separation from their partner.
- Department of Evolution, Ecology and Behavior, University of Illinois, United States
Despite the best efforts of my hole-digging dog, my backyard is home to rodents who are in love. Furry prairie voles spend lots of time huddled underground, usually in pairs that work together to rear their pups. If the couple is separated, even for as long as two weeks, they still remain bonded and will reunite as tight as they were before (Getz et al., 1981). These humble rodents are famous for their monogamous behavior, and have been the subject of many eye-catching headlines (Tucker, 2014; Armitage, 2015). Part of their appeal is the possibility to understand the biological basis of love, devotion, and life-long attachment – topics that seem more suited to humanities than biology departments.
Most scientific research on prairie voles has focused on how monogamous pairs are formed, particularly the role of oxytocin, the famous ‘love hormone’ (Insel and Shapiro, 1992). However, less is known about what happens when these bonds get broken; what happens when one member of the pair outlives the other? Previous behavioral studies have shown that voles exhibit signs of distress when they are separated from their partner, but eventually adapt to this loss and seek out a new connection (Harbert et al., 2020). Now, in eLife, Zoe Donaldson and colleagues from the University of Colorado Boulder and Oregon Health and Science University – including Julie Sadino as first author – report what happens to voles as they recover from a broken heart (Sadino et al., 2023).
Sadino et al. studied male voles in same-sex and opposite sex pairs that had been housed together for two weeks and then separated for 48 hours or four weeks. Using a technique called vTRAP (short for translating ribosome affinity purification), they investigated which genes are expressed in the nucleus accumbens, a part of the brain that is engaged during pair formation in mammals, including humans (Walum and Young, 2018). The pattern of genes expressed (also known as the transcriptional signature) was measured before and after voles were separated, along with their behavior to see if these two factors are coordinated together. The female voles were also prevented from becoming pregnant to control for the potentially confounding influence of co-parenting together.
The experiments revealed that male voles stably express hundreds of genes in their nucleus accumbens when living with a partner, which remained unchanged even after the pair were separated for a few days. However, while the male voles continued to prefer the company of their partner even after long periods apart, the transcriptional signature in the nucleus accumbens started to decay as the voles spent more time away from each other.
These findings suggest that genes in the brains of the voles start to alter their expression before the voles lose preference for their old mate. This means that although voles may behaviorally resume their relationship after long periods of separation, elements of their transcriptome may be less optimistic that this reunion will happen. It is tempting to speculate that the genes that begin to change expression may somehow be involved in recovering from the loss of a partner.
Furthermore, while behavioral and genomic changes in the brain occurring over different timescales is not an entirely new finding (White et al., 2002), the results of Sadino et al. do offer some clues as to how this may work at a mechanistic level. For example, genes that were upregulated in bonded males, but downregulated after a few weeks of separation, follow a pattern that suggests they may have a role in coping with loss. In contrast, another set of genes, which was initially downregulated and then upregulated after weeks of separation, may be involved in helping to prime the vole to form a new bond.
Understanding the neural basis of complex social behaviors is a hard problem. However, the work by Sadino et al. – which uses a savvy experimental design to connect genes, the brain and animal behavior – shows how it can be done. Moreover, and somewhat surprisingly, other researchers recently reported that prairie voles do not require a receptor for oxytocin in order to form social attachments (Berendzen et al., 2023). It seems that there are actually many players coordinating this complex social behavior.
An immediate task for future work is to look at brain areas other than the nucleus accumbens, which is closely associated with reward. While pair bonding is rewarding, this may be independent from the cognitive aspects of separation, such as the memory of a lost companion or the willingness to find a new partner. Another priority is to explicitly connect the transcriptional signatures identified with the formation or degradation of the pair bond using functional tests, a challenge the scientific community studying these furry lovers is no doubt going after next.
References
-
The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bondingBehavioral Ecology and Sociobiology 8:189–194.https://doi.org/10.1007/BF00299829
-
The neural mechanisms and circuitry of the pair bondNature Reviews Neuroscience 19:643–654.https://doi.org/10.1038/s41583-018-0072-6
-
Social regulation of gonadotropin-releasing hormoneJournal of Experimental Biology 205:2567–2581.https://doi.org/10.1242/jeb.205.17.2567
Article and author information
Author details
Publication history
Copyright
© 2023, Bell
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,388
- views
-
- 55
- downloads
-
- 1
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Prairie Voles: Recovering from a broken heart
eLife 12:e87550.
https://doi.org/10.7554/eLife.87550
Further reading
-
- Neuroscience
Decoders for brain-computer interfaces (BCIs) assume constraints on neural activity, chosen to reflect scientific beliefs while yielding tractable computations. Recent scientific advances suggest that the true constraints on neural activity, especially its geometry, may be quite different from those assumed by most decoders. We designed a decoder, MINT, to embrace statistical constraints that are potentially more appropriate. If those constraints are accurate, MINT should outperform standard methods that explicitly make different assumptions. Additionally, MINT should be competitive with expressive machine learning methods that can implicitly learn constraints from data. MINT performed well across tasks, suggesting its assumptions are well-matched to the data. MINT outperformed other interpretable methods in every comparison we made. MINT outperformed expressive machine learning methods in 37 of 42 comparisons. MINT’s computations are simple, scale favorably with increasing neuron counts, and yield interpretable quantities such as data likelihoods. MINT’s performance and simplicity suggest it may be a strong candidate for many BCI applications.
-
- Developmental Biology
- Neuroscience
We established a volumetric trans-scale imaging system with an ultra-large field-of-view (FOV) that enables simultaneous observation of millions of cellular dynamics in centimeter-wide three-dimensional (3D) tissues and embryos. Using a custom-made giant lens system with a magnification of ×2 and a numerical aperture (NA) of 0.25, and a CMOS camera with more than 100 megapixels, we built a trans-scale scope AMATERAS-2, and realized fluorescence imaging with a transverse spatial resolution of approximately 1.1 µm across an FOV of approximately 1.5×1.0 cm2. The 3D resolving capability was realized through a combination of optical and computational sectioning techniques tailored for our low-power imaging system. We applied the imaging technique to 1.2 cm-wide section of mouse brain, and successfully observed various regions of the brain with sub-cellular resolution in a single FOV. We also performed time-lapse imaging of a 1-cm-wide vascular network during quail embryo development for over 24 hr, visualizing the movement of over 4.0×105 vascular endothelial cells and quantitatively analyzing their dynamics. Our results demonstrate the potential of this technique in accelerating production of comprehensive reference maps of all cells in organisms and tissues, which contributes to understanding developmental processes, brain functions, and pathogenesis of disease, as well as high-throughput quality check of tissues used for transplantation medicine.
