Donna Rose Addis on the hippocampus, the future and brain networks

As the research stage of the book I am writing on imagination starts to wraps up, it was a real treat recently to chat to Donna Rose Addis, a Professor in Cognitive Neuroscience at the University of Auckland. One of the areas I’ve been researching, as a complete novice to neuroscience, has been what happens in our brains when we imagine.  I had read several papers she had written about the similarities between imagination and memory, our abilities to recall the past, and to imagine the future.

I wanted to check with her that I had correctly understood what I had been reading, namely that until recently, neuroscientists thought that different regions of the brain served different functions, “this bit does this, this bit does that”, an approach known as ‘localisationism’.  More recently, activities are understood in terms of networks, different parts of the brain that fire together when we do different things. The imagination is often attributed to something called the ‘Default Mode Network’, but recently Donna and others have shown that other networks also have a role to play.

So I started my absorbing conversation with Donna by checking whether I had understood this correctly, and asking her to talk a bit about the hippocampus (the part of the brain often associated with memory and imagination) and its relationship with the brain’s different networks (text follows below, or you can listen to the newly souped-up podcast here):

“The focus on the hippocampus was mainly because of individuals with damage to the hippocampus showing such dense amnesia. That’s where the idea that maybe the hippocampus is the seat of memory came from. As we’ve learned more through neuroimaging though, our ideas have developed.

We’ve transitioned into this idea that brain regions work together in networks. That isn’t to say that there aren’t critical regions – or “nodes” – within these networks. It might be that a particular node makes a critical contribution to the behaviour or ability, such as memory, or it is critical for up-regulating the rest of the network, or perhaps in passing information onto other nodes. If that is the case, then damage to just that single region can be devastating for that particular behaviour.

So although we have shifted from thinking about single regions supporting behaviours to focusing on networks, you can also think of it as the realisation that regions never work alone, and they are always situated within a neural context. So how a region might activate is dependent on the activation levels of other regions in that network.

The DMN is a fascinating network. As you mentioned, it is called the “default mode” because it is engaged when we’re not engaged in an external task and so when our mind is spontaneously wandering. But interestingly, when I started in research in the late 1990s, that same network was thought of as the ‘Autobiographical Retrieval Network’. It wasn’t until about 2001 that the idea of the DMN emerged, and many of us were saying, “Well, that’s just the memory network. What is this “default mode” they are talking about?” But we now know that when humans aren’t captured by something external, they are captured internally – they are moving through a memory space. They’re thinking about things they’ve done, using aspects of memory to think about the future, or to imagine events that haven’t happened or to rework past events.

So it isn’t surprising the DMN is the same brain network activated during memory tasks. But the way I think of it is that when in the default mode, the mind is just wandering through these types of memories in a low energy fashion; it isn’t intensely engaged. But when we actively search our memories, then we ramp up the activity in that network. For example, when we have people in the MRI scanner and we ask them to remember a specific event in the past or to imagine a specific event in the future, then we see even more activity in the DMN than when people are spontaneously mind wandering.

Joel Voss and Neal Cohen once described the hippocampus as ‘promiscuous’. It can be involved in many different tasks beyond memory, even tasks that 20 years ago we would not have thought of as hippocampally-dependent, such as perception. But then also the hippocampus is connected with different networks depending on what you’re doing. So often we do see it engaged and connected with the DMN, but then it can also be connected with the ECN as well.

Scott Barry Kaufmann at the Imagination Institute refers to the DMN as ‘the Imagination Network’, but would it be more correct to say that in a really imaginative person, it’s not just down to having a healthy DMN, it’s actually all those different networks that play a role in an imaginative person?

I would say so, though it likely depends on what the task is at hand, or if there is even a task. For instance, if you’re really having to think very laterally while trying to work out a particular problem –and by that I mean using cognitive strategies to generate different potential solutions in a conceptually expansive way, such as when you activate ideas that wouldn’t normally go together and are more distant from each other in conceptual space – then the Frontoparietal Control Network and ECN are going to come online to help with that.

But if you’re just mind wandering, and we can certainly be imaginative and come up with ideas in a spontaneous fashion, then I think it would likely be only the DMN engaged. What we’ve seen in our studies is that when participants are actually tasked with a difficult imagination task, then we see interactions between the ECN, the Frontoparietal Control Network, and also the Salience Network. This is probably because the imagination task is quite difficult and requires conceptual expansion to generate novel ideas. It could also be to do with the fact that when more than one network is contributing to a task, there needs to be some switching between these networks, as they come on- and off-line.

We had a study come out last year in Neuropsychologia that was led by my post-doc Dr Reece Roberts. In this study, we had participants imagine future events in response to a set of their own personal details. So on one trial, a participant might be required to imagine a future event that involves “Dad”, “My garage” and “My new car”. That’s a fairly easy imagination task, because all those details are congruent – they come from the same aspect of that person’s life. However on other trials, we presented each participant with details that came from different spheres of their life such as family, work and sports team, such as “Dad”, “University gym” and “My laptop computer”. It’s quite a fun study and the most memorable of these random combinations was “Dad” in a “Laser tag park” with an “Inflatable boat”! And it’s much more difficult to imagine a future event involving these incongruent details. Participants have to come up with an idea, they’ve got to generate a structure or a framework for the event, and then retrieve the appropriate details to flesh that event out.

When people were doing this much more demanding task, we thought we might see more activity in the DMN, as its being driven much harder. However, we found lower activity in the DMN which likely reflects the fact that participants were less able to generate a really vivid and clear simulation of that event. Even though it was less activated, we did find that the DMN was strongly coupled with the Salience Network and Frontoparietal Control Network, including the anterior lateral prefrontal cortex that support conceptual expansion. This is probably what helped participants to think more laterally and figure out how to incorporate these disparate details into a story that makes sense.

It used to be, as I understand it, that people thought that the ECN and the DMN were like yin or yang. You were either in one or you were in the other, and as soon as you went into one, the other one disappeared, but now people are seeing that they actually bleed into each other a bit more.

That’s right. That was to do with the nature of the tasks people were doing. When the DMN was named as such, this was on the basis of observations that when participants were doing, say, a language task or a mathematics task, the DMN would be suppressed, but then it would become active during rest periods when participants were no longer focused on the external task. And in that way, these networks are anti-correlated with each other – they’re switching on and off. However, we now know that when participants are engaged in internally-generated tasks that actually utilise the DMN (such as memory and imagination), then we don’t see this anti-correlation between task and rest.

Rather the DMN is more active during task and less active during rest. It’s a modulation of activity levels in the same network rather than a switching of networks. The third situation we have seen is that if the task is internally-based but has particular demands that require some control over what the DMN is doing, then these networks work together – as we found during the incongruent imagination task in the study I just described. So while networks can be working in opposition to each other, they can also join forces to undertake challenging forms on internally-generated thought such as creativity.

And the hippocampus has a vital role to play in each of those?

That’s right. When we did our early work on imagination, we saw significant overlap in the hippocampus when people remembered the past and imagined the future. But then we also saw that the hippocampus was actually more active in the imagination task, which was quite a striking finding because up until that point, the field had thought of the hippocampus as a memory structure, but then we found it was more active during imagination. We were quite perplexed by that!

But if we consider evidence that the hippocampus allows the integration of information, then we can make sense of this finding. When we imagine a future event, we have to integrate details that may never have been integrated before. When you remember something, you are reintegrating details that already linkages (as you experienced those details together in the first place), so it’s not as demanding for the hippocampus. That was a really fascinating study, and it sparked off a decade of research for us looking into how the brain imagines.

And also presumably when we think we’re remembering, our imagination is filling in quite a lot of the gaps. I just got together with a friend of mine I haven’t seen for 30 years and we were remembering the same events almost completely differently!

That’s always very enlightening isn’t it, those experiences that show us just how malleable our memories are? I’ve just written a new paper on this idea that will be coming out in the Journal of the Royal Society of New Zealand in June where I argue that memory and imagination are the same thing. In both cases a simulation of experience is constructed by bringing together different kinds of perceptual elements from previous experiences, schematic information (what we know about how the world works and how events unfold), and semantic information (general facts and knowledge).

Depending on whether the simulation is a memory or an imagination, you will get different weightings of content: If it’s a memory there will most likely be more perceptual content, while if it’s an imagined event where a framework for the event must be generated, the simulation will likely contain more schematic information. But these differences in content are superficial because in both cases, the simulated event is a construction of reality, but a construction nonetheless.

I’ve interviewed people who work in the PTSD field who talk about how the hippocampus visibly shrinks during trauma, and the research around people growing up in states of fear, or high anxiety and hyper vigilance, leads to a contracted hippocampus. Some research suggests that growing up around noise leads to a smaller hippocampus. I wonder if you had a sense about what do we know about what are the ideal conditions for the hippocampus, and when we see the hippocampus being impacted in that way, presumably that then has a knock on impact to the networks that we’ve been discussing?

Very interesting question. I’ve looked at this a bit in terms of looking at autobiographical memory and future thinking in depression which is associated with changes in the function of the hippocampus as well as the networks we’ve talked about. Along with this, the ability to think about the past and the future in specific detail is reduced in depression.

What is common to all of the things that you mentioned – trauma, fear, anxiety, noise, poverty – is stress. You may have heard about the stress hormone cortisol and how that has a very detrimental impact on the hippocampus. Exposure to increased levels of cortisol causes this atrophy, or shrinkage, of the hippocampus.

It used to be thought of as a one way street – that increases in cortisol impacted the hippocampus which then impacted cognition. What research has now shown is that the hippocampus itself is actually involved in stress regulation, in terms of its connectivity with the amygdala and also with the HPA (hypothalamic–pituitary–adrenal) axis. So once the hippocampus is damaged by stressful experiences, a person then experiences subsequent events as more stressful which leads to more cortisol release and further hippocampal damage. It just becomes a vicious cycle.

And like you said, one can become hypervigilant and very reactive to stress. In my studies on depression, I used an instrument called the PERI Life Events Scale – a list of the most stressful events people experience (such as death of a spouse, divorce, illness, moving house, losing a job, etc.) Participants are asked to indicate how many events they had experienced and how stressed they were. While there was no difference between our depressed and non-depressed participants in terms of the number of events that they experienced, people with a history of depression rated their experience of these events as much more stressful. I think that’s really interesting because this heightened stress response maintains and furthers their hippocampal atrophy. And it is also not surprising that the more episodes of depression one has experienced, the more severe the hippocampal atrophy.

The other part of your question was about the ideal conditions for the hippocampus. What might enhance its function and the ability to imagine. A number of studies have shown positive effects of exercise. The hippocampus is one of the few regions in the brain that can actually regenerate. It can birth new neurons, a process we call neurogenesis, and exercise can increases neurogenesis and thus hippocampal volume and function. While we are not exactly sure how exercise has this positive effect on neurogenesis, it may be by way of increased blood or oxygen – and perhaps in part by counteracting stress! Anti-depressants also work to increase the volume of the hippocampus in individuals with depression.

Being socially active might also be a part of these effects (often these studies involve group exercise programmes). In my research with older adults, those who are engaged in life –  engaged in relationships, politics, hobbies, whatever it is – then they’re usually processing more information, making links between ideas. All of this is really good for keeping your hippocampus going – you’re basically stimulating it.

So would it be a reasonable leap to suggest that in a culture which is increasingly traumatised, or increasingly stressed, the more stress that you put on a population, the more fearful a population is, then the less imaginative it’s going to be and the less able it’s going to be to imagine the future?

Absolutely. I agree there has been a general societal increase in stress. In modern society, we’re constantly bombarded with information and we can consider that as being in a perpetually noisy environment, if you like. So like that study that you mentioned earlier, if you’re constantly bombarded with information, and having to filter and deal with this relentless stream of information, then this creates an ongoing level of stress. For instance, those of us who work in the information economy are having to deal with email, social media, and other forms of knowledge that are generated in a very speeded up fashion. Much faster than when we received a few letters a week!

I spoke to Dr Larry Rosen, co-author of ‘The Distracted Mind’. He says we’re in the middle of a ‘Cognition Crisis’. I wonder if you had a thought about how that relates to imagination? What happens to our imagination when our attention span is shot to pieces? And to the networks we talked about?

If you think about what’s happening cognitively when you’re distracted, it’s actually that your attention is being grabbed by something. Perhaps it used to be that we were distracted by our minds wandering, but what’s happening to us now is that our attention is being grabbed by incoming alerts and bits of new knowledge. We actually have very little time to let our minds wander. That’s a rare kind of state now as we’re constantly engaged, looking at things, processing that information, deciding how to deal with it (do we act on it, save it for later, filter it out?) This definitely has an impact in that it depletes cognitive resources, and keeps the ECN engaged at the cost of the DMN.

I suppose one of the things is that when we have very little time to let our mind wander, like you said, that’s really basically that we use our DMN very little. Because at those times when our DMN could be taking over, we’re thinking, “Hmm, I’m slightly bored. Where’s my phone?”

I know!

So, what happens when our DMN gets used less and less and less? What are the impacts of that?

That is a very intriguing question that has not, to my knowledge, been looked at. But I imagine that there would be less strengthening between the nodes of the DMN, or maybe we become less adept at switching between the DMN and other networks, for instance.

We all experience that fog when you go back to work at the end of the summer. Down in New Zealand right now it’s the end of summer and we’re all just going back to work and trying to get our brains back into the swing of it again. But if you’re never in the swing of it, because you’re too busy looking at social media or on your phone, perhaps it then becomes very difficult then to engage these networks efficiently and effectively.

One of the things that I don’t have any data for but feels to me like something that I’ve observed, is that when I was growing up in the 70s and 80s, we talked about the future all the time. All the comics you got as children were all about, “The future is going to be like this, the future is going to be like that.” Nobody really talks about the future very much anymore. It’s become something that’s really complicated and scary, and we see the rise of all these movements who say, “Hey, let’s make it like it used to be. Let’s go backwards.” This sort of ‘retrotopia’ kind of a thing. Do you think that reflects that somehow we’re becoming less able to look to the future, and why might that be?

One of the things that has been observed in people with anxiety, and depression, is a reduced ability to think about the past and the future in specific detail. What I found in my study on depression is that it was more difficult for those with depression to imagine future events relative to remembering past events.

This finding harks back to what I was saying before about imagining something that you’ve not experienced before – one has to bring ideas together and this might require some degree of lateral thinking about how to link disparate ideas in a way that makes sense. Interestingly, we found that when depressed individuals were able to imagine future events, their ECN and DMN were activated more than in non-depressed individuals. In other words, in depression, it took more engagement of these brain networks to get to the same cognitive outcome – an imagined future event.

One theory of why past and future thinking is impaired in depression centres of avoidance. That depressed individuals learn that thinking about personal events in detail can be upsetting and destabilising, and so they learn to avoid doing it.

I would agree that, in addition to brain changes, avoidance is likely also playing a role. And perhaps this is more the case in those with anxiety who tend to think about the future in a negative way. This is distinct from depression where people are less able to think about positive future events, but in anxiety it’s that negative future events come to mind much more readily.

Interesting.

So it’s like being heightened to the negative – so it would make sense that one would start to avoid thinking about the future. And avoidance would involve the ECN regulating the activities of the DMN to stop these thoughts coming into mind.

Some argue that the imagination is value neutral. Some would argue that if you’re Florence Nightingale reimagining the healthcare system, or you’re Donald Trump, you’re both imaginative people, you’re just imagining in different ways. I wonder from what you’ve said there, whether it’s actually that the natural state of the imagination which we see in young children, is a positive solutions-focused sort of creative, positive thing. And that what happens in someone like Donald Trump when you read about his childhood, which was just appallingly stressful, and traumatic, and neglected and awful, and the same with Hitler (for example) that actually the people that come up with the really negative imaginative visions of the future, their imagination is being filtered through lenses of trauma and stress and distrust. Whereas actually if we are able to have, for example, an education system that really values imagination and creativity, and where young people aren’t squeezed by testing and all this kind of stuff, and are actually more able to flourish, that actually it’s more likely that we’re going to get the imagination applied to more positive visions of the future, rather than more fear based ones. Or is that just me, because I’m coming from a more sort of progressive political position, saying anyone I don’t agree with must have a damaged imagination?

What you’re saying certainly fits with that data: that people who have experienced anxiety and trauma do think about the future in more negative terms. It makes sense that if you’re hypervigilant, you are on the lookout for the negative. You really are experiencing the world, like you said, through a negative lens. I would argue that this would extend to your memory and your imagination as well. There is a lot of evidence that we remember things that are congruent with our mood.

How do you mean?

So if you are in a negative state – if you’re in a low mood or feeling depressed – you tend to remember or imagine things that are negative. Our mood influences our search for memory, or for imagination. You really hit the nail on the head when you talk about how children are able to think in a very imaginative, free, way. That really is the basis of creativity – the exploration of ideas, and first just allowing different ideas to come together. This is known as divergent thinking – the ability to just generate ideas – which can be enhanced by bringing together things that might not normally go together. We can then evaluate the ideas we’re generated – convergent thinking – where we determine whether the ideas fit with the task at hand or the problem we’re trying to solve.

In New Zealand we talk about ‘Kiwi ingenuity’, where you can do anything with “Number 8 wire” – the gauge of wire used for sheep fences! We really do have a strong ‘can-do’ culture of thinking laterally to figure out solutions with our limited resources (all the more limited by our isolation). It really is a case of not having what is usually used to achieve ‘X’, and then figuring out a solution with other things that are available.

To do this, you do have to think very creatively – laterally – through different kinds of solutions. This is something we really value here in New Zealand, especially because we are on the other side of the world and often don’t have access to all the things that other places have. And interestingly, we often tend to be a bit further behind the rest of the Western world in terms of societal shifts – and perhaps that also includes changes that have made life stressful. So maybe we do still have a bit more capacity in that sense. What you said about testing children in schools, that really resonates with me because I just think that is just such a terrible way to bash creative thinking and imagination out of kids. It really restricts their thinking.

The Torrance Test for Creative Thinking looks at different aspects of creativity and probably the main one is divergent thinking. You know, “Here’s a paper cup. You’ve got 2 minutes, as many different uses for it as possible… The cow jumped over the moon, what happened next? You’ve got 2 minutes.” That sort of thing. As a way of measuring divergent thinking, it’s a really interesting snapshot. How do you measure how imaginative a population is? Do you have any thoughts on that? Is The Torrance Test for Creative Thinking, and a mass study of divergent thinking, a good proxy for how imaginative a population is, or what else would you want to look at?

I remember once doing a panel discussion on creativity, and the first question I got from the audience was from someone who was very creative, who said, “That test is crap. You’re not tapping into anything that is like my experience of being creative.” This is one of the issues with a lot of different kinds of psychological measures, that we’re trying to capture something that’s hugely complex, but in a way that we can break down the components of that complex process.

Divergent thinking tasks allow you to look at the process of generating ideas in a very controlled way, so then we can compare it across people, across populations. If that’s your goal, then I actually do think that something like divergent thinking – and convergent thinking – tasks are perfect for this.

We combine these tasks with more in-depth measures. For instance, we audio-record participants while they simulate experiences, and then we go through and, in a very laborious manner, parse every bit of information they generate, and then classify each one according to different coding schemes. That takes huge man hours to do this, but yields a rich picture of how we imagine.

There are ways of running transcripts through algorithms that pick out certain word types, but this sort of coding can never really replace the way in which a human can score these imaginings. We can enter the narrative that somebody is actually creating, and that is a crucial aspect of coding a simulation – to really capture the essence of the internal representation the person is describing in a much more nuanced way than divergent thinking tasks can. So while it can’t be used in mass testing (the types of studies that we do have around 20 people), we get a very in-depth look at the way in which people bring information together to create these simulations.

If you had a mass divergent thinking sample, like she has going back over time, that showed that kind of decline, that at least would be maybe an indicator that there was something worth looking at here?

Yeah, absolutely.

If that was the case, that actually there was a steady and persistent decline in divergent thinking in a society, what else would you expect to see? What other things might you look for that would confirm that that was happening, that you might see in different areas of life and culture, do you think?

Things like looking at examples of ingenuity and creativity, and whether that’s changing over time. That’s quite a hard question in and of itself. How ingenious is a particular society? We might determine that the number of products that are being created now is probably exponentially greater than it was 30 years ago, but that is confounded with the fact that our access to information and our exposure to different ideas has also expanded so rapidly.

It’s really hard to tease apart whether there is a true cohort effect – a change in ingenuity over successive generations – because you need to have everything else being equal to really determine that, especially things that could contribute to an increase. But the fact that the evidence you cite is in the opposite direction – that there’s a decrease in divergent thinking – then this decrease is in spite of the increased exposure to all varieties of ideas that comes with globalism. That makes me think that perhaps individuals are not able to process all this information in a way that yields creative ideas.

What for you would be the ideal conditions for a very vibrant imagination? When I think of it, I think the imagination needs time, and space, and somebody who’s feeling safe, and somebody who’s well nourished. What would you think of as being the ideal conditions for a really active, vibrant imagination?

All of those things that you just mentioned. Having things that capture your interest around you, like nature or books or whatever is inspiring and interesting to you. Having exposure to different ideas but not in a stressful way – that bombardment of information needs to be minimized. And along with this, an absence of pressure is critical, so that you’re able to explore. I know for myself, I’ve really noticed that as the pressures of academia, and the sheer amount of information we deal with daily, have increased exponentially over the last 10 years, I don’t have the mental space to think and to be creative that I used to have. It’s almost like sometimes that my creative capacity has completely disappeared which is really sad given my job is to think creatively. So I believe an absence of pressure is critical.

The other thing, though, is that sometimes we need to have a goal or a problem we’re trying to solve. Sometimes this is when the best ideas emerge, spontaneously (but not randomly) popping into mind while we’re doing menial tasks (that’s the DMN at work). Having goals, having questions, being curious. These are, to some extent, personality traits. Some people are just inherently curious about the world around them. Apparently I was curious about everything from the moment I could walk and talk, or actually from before I could even talk – I used to babble non-stop while pointing at things around me, and from there I’ve always been observant and detail-orientated, and also intent on figuring out how things in the world fit together, and how they work. Maybe this is why I’m both a creative type and a scientist!