Some animals pair for life. These bonds are crucial for parental care, defence of territories and other resources, and well-being. We humans also form long term, special relationships with lovers and close friends. But what’s at the neurological heart of this process? Speaking with Chris Smith, Steven Phelps, at the University of Texas at Austin, wondered the same thing and set about developing a way to track in four dimensions - both throughout the brain and across time - how different regions of the nervous system respond to the building of a bond…
Steven - We wanted to make a map of the brain as it forms a bond. And to do that, we turn to the prairie vole, which is a rodent that lives in the Midwest, is famous for forming bonds between males and females as they mate repeatedly over the course of a day. And we do have a list of brain regions roughly 18 or so that were thought to be involved in pair bonding. But those were all regions that were chosen piecemeal based on bits of literature that we knew. And no one had taken a really systematic approach at looking at the brain in its entirety as a bond as being formed. And that that's really what was new about our experiment.
Chris - And that's what you did? You were actually able to document the entire brain as these bonds form?
Steven - Exactly. What we did was to create a three-dimensional model of the prairie vole brain that had boundaries between different brain regions built into the model so that we could take images of prairie vole brains as bonds were forming, and identify markers that are expressed in cells as they're active, visualise those markers and then map them back onto this brain. And with this three dimensional model, we could essentially count all the active neurons across the entire brain and assign them an address, say they belong to this brain region or to that brain region from animals at different key points in time as a bond is being formed.
Chris - How do you know that because you are registering activity in different brain regions when these bonds are forming, how do you know that that activity is linked exclusively to the bonding that's going on and not to the fact the animals are smelling each other, dancing around each other? There's lots of other things going on that could be mixed up with the bonding, but you don't know that they're actually part of the bonding process. They're just going on at the same time.
Steven - Well, of course, that's always a potential confound. We dealt with that in part through our experimental design. So we didn't look just at animals that were mating and forming bonds. We also looked at animals housed together as siblings. Mating is an essential part of bond formation in the prairie vole, as it is in humans and other species. Copulation initiates mechanisms of bond formation and repeated copulation that helps us form bonds. One thing that we really can't distinguish is brain activity related to sexual behaviour and brain activity related to bonding per se. And in the prairie vole they're kind of one and the same because the sexual behaviour leads to a bond. So we didn't feel like it was essential to tease those apart, but it would be really interesting to repeat our study using another species that has similar sexual behaviour but doesn't translate that sexual behaviour into a bond. And, and indeed that's one of the things we want to do next.
Chris - I was going to ask that precise question because there's another vole which doesn't form long-term bonds, isn't there? Mm-Hmm. <affirmative>. And so one could ask, do we see some of these areas you've identified as essential and part of the bonding process not lighting up in the brain of the animal that doesn't form these long-term bonds?
Steven - That's exactly what we would expect to see. And our interpretation of our findings is that we see different circuits in the brain lighting up at different points in time as a bond forms and early before a bond has really formed, but after a lot of mating has taken place. The circuits we see are circuits that are known to be involved in sexual behaviour. Later, though we see other kinds of circuits showing up that are not known to be involved in sexual behaviour per se. And we think these are are likely places where the experience of sex gets translated into some enduring bond. And these are areas I would expect not to show up in as other promiscuous species that don't form bonds like the meadow vole or the montane vole, famously.
Chris - And that's the key point here, which is have you found any additional areas which had been missed by previous attempts to, to study bonding, which also clearly fit in with our understanding of the neuro anatomy, the connectivity, and therefore the ultimate physiology, the behaviour of the animals, when they bond or don't bond?
Steven - Yes. We find in particular regions of the brain that are part of a network of emotionally related brain regions that we call the extended amygdala. And these are regions that receive lots of kind of complex sensory information. They're often involved in emotional regulation, often directed at specific individuals. They seem to encode aspects of the identity of our social partners. And we find some of these regions which project to hormonal centres that govern hormonal release. We find activity in these brain regions lights up in, in places not previously linked to bonding, but which make a lot of sense in terms of our understanding of the anatomy of the brain and its functions.
Chris - The amygdala is also linked to fear, isn't it? So is it possible that people are, are frightened to leave their partner or your voles are frightened to, to break up of what might be the consequence of of non-monogamy <laugh>?
Steven - That is a great question. The, the amygdala is linked to fear, but it's actually, when we think of fearfulness and the amygdala, we're usually talking about a really specific region of the amygdala called the central amygdala. And that doesn't really show up so much in our study. It's really other regions of the amygdala that have been implicated in social reward, in constellation behaviour and a variety of things that are showing up. It's probably not a change in fearfulness per se.
Chris - That's a relief. You considered both male and female animals? Mm-Hmm, <affirmative>, did they both use the same circuitry and did they use the same circuitry equivalently? So in other words, if you've got a female, are you seeing the same pattern of brain activity in the male and are you seeing the same extent or are the females really committed to the relationship? The males a bit so, or do they seem to be "even-stevens"?
Steven - We weren't sure what to expect because there's this idea in the literature that sexual dimorphism due to differences in sex steroids like testosterone, oestrogen, progesterone that are circulating in the body, we know that they produce some sex differences in the brain, including some differences in hormonal systems that are important for pair bonding and parental care. And so one thought in the literature is that even if the behaviour of males and females is the same, even if they both provide, provide parental care, even if they both pair bond, this is the case in this species, they might still rely on different brain mechanisms. So we really didn't know what we would see, but when we looked at males and females as they formed bonds, we found virtually no differences in the way their brains were activated by repeated mating and bond formation. So overall it seems there's very little sexual dimorphism, very little differences between males and females and how and what brain regions are active as they form a bond.
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