Mind-wandering and metacognition: variation between internal and external thought predicts improved error awareness

Yesterday I published my first paper on mind-wandering and metacognition, with Jonny Smallwood, Antoine Lutz, and collaborators. This was a fun project for me as I spent much of my PhD exhaustively reading the literature on mind-wandering and default mode activity, resulting in a lot of intense debate a my research center. When we had Jonny over as an opponent at my PhD defense, the chance to collaborate was simply too good to pass up. Mind-wandering is super interesting precisely because we do it so often. One of my favourite anecdotes comes from around the time I was arguing heavily for the role of the default mode in spontaneous cognition to some very skeptical colleagues.  The next day while waiting to cross the street, one such colleague rode up next to me on his bicycle and joked, “are you thinking about the default mode?” And indeed I was – meta-mind-wandering!

One thing that has really bothered me about much of the mind-wandering literature is how frequently it is presented as attention = good, mind-wandering = bad. Can you imagine how unpleasant it would be if we never mind-wandered? Just picture trying to solve a difficult task while being totally 100% focused. This kind of hyper-locking attention can easily become pathological, preventing us from altering course when our behaviour goes awry or when something internal needs to be adjusted. Mind-wandering serves many positive purposes, from stimulating our imaginations, to motivating us in boring situations with internal rewards (boring task… “ahhhh remember that nice mojito you had on the beach last year?”). Yet we largely see papers exploring the costs – mood deficits, cognitive control failure, and so on. In the meditation literature this has even been taken up to form the misguided idea that meditation should reduce or eliminate mind-wandering (even though there is almost zero evidence to this effect…)

Sometimes our theories end up reflecting our methodological apparatus, to the extent that they may not fully capture reality. I think this is part of what has happened with mind-wandering, which was originally defined in relation to difficult (and boring) attention tasks. Worse, mind-wandering is usually operationalized as a dichotomous state (“offtask” vs “ontask”) when a little introspection seems to strongly suggest it is much more of a fuzzy, dynamic transition between meta-cognitive and sensory processes. By studying mind-wandering just as the ‘amount’ (or mean) number of times you were “offtask”, we’re taking the stream of consciousness and acting as if the ‘depth’ at one point in the river is the entire story – but what about flow rate, tidal patterns, fishies, and all the dynamic variability that define the river? My idea was that one simple way get at this is by looking at the within-subject variability of mind-wandering, rather than just the overall mean “rate”.  In this way we could get some idea of the extent to which a person’s mind-wandering was fluctuating over time, rather than just categorising these events dichotomously.

The EAT task used in my study, with thought probes.
The EAT task used in my study, with thought probes.

To do this, we combined a classical meta-cognitive response inhibition paradigm, the “error awareness task” (pictured above), with standard interleaved “thought-probes” asking participants to rate on a scale of 1-7 the “subjective frequency” of task-unrelated thoughts in the task interval prior to the probe.  We then examined the relationship between the ability to perform the task or “stop accuracy” and each participant’s mean task-unrelated thought (TUT). Here we expected to replicate the well-established relationship between TUTs and attention decrements (after all, it’s difficult to inhibit your behaviour if you are thinking about the hunky babe you saw at the beach last year!). We further examined if the standard deviation of TUT (TUT variability) within each participant would predict error monitoring, reflecting a relationship between metacognition and increased fluctuation between internal and external cognition (after all, isn’t that kind of the point of metacognition?). Of course for specificity and completeness, we conducted each multiple regression analysis with the contra-variable as control predictors. Here is the key finding from the paper:

Regression analysis of TUT, TUT variability, stop accuracy, and error awareness.
Regression analysis of TUT, TUT variability, stop accuracy, and error awareness.

As you can see in the bottom right, we clearly replicated the relationship of increased overall TUT predicting poorer stop performance. Individuals who report an overall high intensity/frequency of mind-wandering unsurprisingly commit more errors. What was really interesting, however, was that the more variable a participants’ mind-wandering, the greater error-monitoring capacity (top left). This suggests that individuals who show more fluctuation between internally and externally oriented attention may be able to better enjoy the benefits of mind-wandering while simultaneously limiting its costs. Of course, these are only individual differences (i.e. correlations) and should be treated as highly preliminary. It is possible for example that participants who use more of the TUT scale have higher meta-cognitive ability in general, rather than the two variables being causally linked in the way we suggest.  We are careful to raise these and other limitations in the paper, but I do think this finding is a nice first step.

To ‘probe’ a bit further we looked at the BOLD responses to correct stops, and the parametric correlation of task-related BOLD with the TUT ratings:

Activations during correct stop trials.
Activations during correct stop trials.
Deactivations to stop trials (blue) and parametric correlation with TUT reports (red)
Deactivations to stop trials (blue) and parametric correlation with TUT reports (red)

As you can see, correct stop trials elicit a rather canonical activation pattern on the motor-inhibition and salience networks, with concurrent deactivations in visual cortex and the default mode network (second figure, blue blobs). I think of this pattern a bit like when the brain receives the ‘stop signal’ it goes, (a la Picard): “FULL STOP, MAIN VIEWER OFF, FIRE THE PHOTON TORPEDOS!”, launching into full response recovery mode. Interestingly, while we replicated the finding of medial-prefrontal co-variation with TUTS (second figure, red blob), this area was substantially more rostral than the stop-related deactivations, supporting previous findings of some degree of functional segregation between the inhibitory and mind-wandering related components of the DMN.

Finally, when examining the Aware > Unaware errors contrast, we replicated the typical salience network activations (mid-cingulate and anterior insula). Interestingly we also found strong bilateral activations in an area of the inferior parietal cortex also considered to be a part of the default mode. This finding further strengthens the link between mind-wandering and metacognition, indicating that the salience and default mode network may work in concert during conscious error awareness:

Activations to Aware > Unaware errors contrast.
Activations to Aware > Unaware errors contrast.

In all, this was a very valuable and fun study for me. As a PhD student being able to replicate the function of classic “executive, salience, and default mode” ‘resting state’ networks with a basic task was a great experience, helping me place some confidence in these labels.  I was also able to combine a classical behavioral metacognition task with some introspective thought probes, and show that they do indeed contain valuable information about task performance and related brain processes. Importantly though, we showed that the ‘content’ of the mind-wandering reports doesn’t tell the whole story of spontaneous cognition. In the future I would like to explore this idea further, perhaps by taking a time series approach to probe the dynamics of mind-wandering, using a simple continuous feedback device that participants could use throughout an experiment. In the affect literature such devices have been used to probe the dynamics of valence-arousal when participants view naturalistic movies, and I believe such an approach could reveal even greater granularity in how the experience of mind-wandering (and it’s fluctuation) interacts with cognition. Our findings suggest that the relationship between mind-wandering and task performance may be more nuanced than mere antagonism, an important finding I hope to explore in future research.

Citation: Allen M, Smallwood J, Christensen J, Gramm D, Rasmussen B, Jensen CG, Roepstorff A and Lutz A (2013) The balanced mind: the variability of task-unrelated thoughts predicts error monitoringFront. Hum. Neurosci7:743. doi: 10.3389/fnhum.2013.00743

The 2011 Mind & Life Summer Research Institute: Are Monks Better at Introspection?

As I’m sitting in the JFK airport waiting for my flight to Iceland, I can’t help but let my mind wander over the curious events of this year’s summer research institute (SRI). The Mind & Life Institute, an organization dedicated to the integration and development of what they’ve dubbed “contemplative science”, holds the SRI each summer to bring together clinicians, neuroscientists, scholars, and contemplatives (mostly monks) in a format that is half conference and half meditation retreat. The summer research institute is always a ton of fun, and a great place to further one’s understanding of Buddhism & meditation while sharing valuable research insights.

I was lucky enough to receive a Varela award for my work in meta-cognition and mental training and so this was my second year attending. I chose to take a slightly different approach from my first visit, when I basically followed the program and did whatever the M&L thought was the best use of my time. This meant lots of meditation- more than two hours per day not including the whole-day, silent “mini-retreat”. While I still practiced this year, I felt less obliged to do the full program, and I’m glad I took this route as it provided me a somewhat more detached, almost outsider view of the spectacle that is the Mind & Life SRI.

When I say spectacle, it’s important to understand how unconventional of a conference setting the SRI really is. Each year dozens of ambitious neuroscientists and clinicians meet with dozens of Buddhist monks and western “mindfulness” instructors. The initial feeling is one of severe culture clash; ambitious young scholars who can hardly wait to mention their Ivy League affiliations meet with the austere and almost ascetic approach of traditional Buddhist philosophy. In some cases it almost feels like a race to “out-mindful” one another, as folks put on a great show of piety in order to fit into the mood of the event. It can be a bit jarring to oscillate between the supposed tranquility and selflessness of mindfulness with the unabashed ambition of these highly talented and motivated folk- at least until things settle down a bit.

Nonetheless, the overall atmosphere of the SRI is one of serenity and scholarship. It’s an extremely fun, stimulating event, rich with amazingly talented yoga and meditation instructors and attended by the top researchers within the field. What follows is thus not meant as any kind of attack on the overall mission of the M&L. Indeed, I’m more than grateful to the institute for carrying on at least some form of Francisco Varela’s vision for cognitive science, and of course for supporting my own meditation research. With that being said, we turn to the question at hand: are monks objectively better at introspection? The answer for nearly everyone at the SRI appear to be “yes”, regardless of the scarcity of data suggesting this to be the case.

Enactivism and Francisco Varela

Francisco Varela, founder of EnactivismBefore I can really get into this issue, I need to briefly review what exactly “enactivism” is and how it relates to the SRI. The Mind & Life institute was co-founded by Francisco Varela, a Chilean biologist and neuroscientist who is often credited with the birth and success of embodied and enactive cognitive science. Varela had a profound impact on scientists, philosophers, and cognitive scientists and is a central influence in my own theoretical work. Varela’s essential thesis was outlined in his book “The Embodied Mind”, in which Varela, Thompson, and Rosch, attempted to outline a new paradigm for the study of mind. In the book, Varela et al rely on examples from cross-cultural psychology, continental phenomenology, Buddhism, and cognitive science to argue that cognition (and mind) is essentially an embodied, enactive phenomenon. The book has since spawned a generation of researchers dedicated in some way to the idea that cognition is not essentially, or at least foundationally, computational and representational in form.

I don’t here intend to get into the roots of what enactivism is; for the present it suffices to say that enactivism as envisioned by Varela involved a dedication to the “middle way” in which idealism-objectivism duality is collapsed in favor of a dynamical non-representational account of cognition and the world. I very much favor this view and try to use it productively in my own research. Varela argued throughout his life that cognition was not essentially an internal, info-processing kind of phenomenon, but rather an emergent and intricately interwoven entity that arose from our history of structural coupling with the world.  He further argued that cognitive science needed to develop a first-person methodology if it was to fully explain the rich panorama of human consciousness.

A simpler way to put this is to say that Varela argued persuasively that minds are not computers “parachuted into an objective world” and that cognition is not about sucking up impoverished information for representation in a subjective format. While Varela invoked much of Buddhist ontology, including concepts of “emptiness” and “inter-relatedness”, to develop his account continental phenomenologists like Heidegger and Merleau-Ponty also heavily inspired his vision of 4th wave cognitive science.  At the SRI there is little mention of this; most scholars are unaware of the continental literature or that phenomenology is not equal to introspection. Indeed I had to cringe when one to-be-unnamed young scientist declared a particular spinal pathway to be “the central pathway for embodiment”.

This is a stark misunderstanding of just what embodiment means, and I would argue renders it a relatively trivial add-on to the information processing paradigm- something most enactivists would like to strongly resist. I politely pointed the gentleman to the example work of Ulric Neisser, who argued for the ecological embodied self, in which the structure of the face is said to pre-structure human experience in particular ways, i.e. we typically experience ourselves as moving through the world toward a central fovea-centered point. Embodiment is an external, or pre-noetic structuring of the mind; it follows no nervous pathway but rather structures the possibilities of the nervous system and mind. I hope he follows that reference down the rabbit hole of the full possibilities of embodiment- the least of which is body-as-extra-module.

Still, I certainly couldn’t blame this particular scientist for his mis-understanding; nearly everyone at the SRI is totally unfamiliar with externalist/phenomenal perspectives, which is a sad state of affairs for a generation of scientists being supported by grants in Varela’s name. Regardless of Varela’s vision for cognitive science, his thesis regarding introspectionism is certainly running strong: first-person methodologies are the hot topic of the SRI, and nearly everyone agreed that by studying contemplative practitioners’ subjective reports, we’d gain some special insight into the mind.  Bracketing whether introspection is what Varela really meant by neurophenomenology (I don’t think it is- phenomenology is not introspection) we are brought to the central question: are Buddhist practitioners expert introspectionists?

Expertise and Introspectionism

Expert introspectionists?Varela certainly believed this to some degree. It’s not entirely clear to me that the bulk of Varela’s work summates to this maxim, but it’s at least certainly true that in papers such as his seminal “Neurophenomenology: a methodological remedy to the hard problem?” he argued that a careful first-person methodology could reap great benefits in this arena. Varela later followed up this theoretical thesis with his now well-known experiment conducted with then PhD student and my current mentor Antoine Lutz.

While I won’t reproduce the details of this experiment at length here, Lutz and Varela demonstrated that it was in fact possible to inform and constrain electrophysiological measurements through the collection and systemization of first-person reports. It’s worth noting here that the participants in this experiment were every day folks, not meditation practitioners, and that Lutz & Varela developed a special method to integrate the reports rather than taking them simply at face value. In fact, while Varela did often suggest that we might through careful contemplation and collaboration with the Buddhist tradition refine first person methodologies and gain insight into the “hard-problem”, he never did complete these experiments with practitioners, a fact that can likely be attributed to his pre-mature death at the hand of aggressive hepatitis.

Regardless of Varela’s own work, it’s fascinating to me that at today’s SRI, if there is one thing nearly everyone seems to explicitly agree on, it’s that meditation practitioners have some kind of privileged access to experience. I can’t count how many discussions seemed to simply assume the truth of this, regardless of the fact that almost no empirical research has demonstrated any kind of increased meta-cognitive capacity or accuracy in adept contemplatives.

While Antoine and I are in fact running experiments dedicated to answering this question, the fact remains that this research is largely exploratory and without strong empirical leads to work from. While I do believe that some level of meditation practice can provide greater reliability and accuracy in meta-cognitive reports, I don’t see any reason to value the reports of contemplative practitioners above and beyond those of any other particular niche group. If I want to know what it’s like to experience baseball, I’m probably going to ask some professional baseball players and not a Buddhist monk. At several points during the SRI I tried to express just this sentiment; that studying Buddhist monks gives us a greater insight into what-it-is-like to be a monk and not much else. I’m not sure if I succeeded, but I’d like to think I planted a few seeds of doubt.

There are several reasons for this. First, I part with Varela where he assumes that the Buddhist tradition and/or “Buddhist Psychology” have particularly valuable insights (for example, emptiness) that can’t be gleaned from western approaches. It might, but I don’t buy into the idea that the Buddhist tradition is its own kind of scientific approach to the mind; it’s not- it’s religion. For me the middle way means a lifelong commitment to a kind of meta-physical agnosticism, and I refuse to believe that any human tradition has a vast advantage over another. This was never more apparent than during a particularly controversial talk by John Dunne, a Harvard contemplative scholar, whose keynote was dedicated to getting scientists like myself to go beyond the traditional texts and veridical reports of practitioners and to instead engage in what he called “trialogue” in order to discover “what it is practitioners are really doing”. At the end of his talk one of the Dalai Lama’s lead monks actually took great offense, scolding John for “misleading the youth with his western academic approach”. The entire debacle was a perfect case-in-point demonstration of John’s talk; one cannot simply take the word of highly religious practitioners as some kind of veridical statement about the world.

This isn’t to say that we can’t learn a great deal about experience, and the mind, through meditation and careful introspection. I think at an early level it’s enough to just sit with ones breath and suspend beliefs about what exactly experience is. I do believe that in our modern lives; we spend precious little time with the body and our minds, simply observing what arises in a non-partial way.  I agree with Sogyal Rinpoche that we are at times overly dis-embodied and away from ourselves. Yet this practice isn’t unique to Buddhism; the phenomenological reduction comes from Husserl and is a practice developed throughout continental phenomenology. I do think that Buddhism has developed some particularly interesting techniques to aid this process, such as Vipassana and compassion-meditation, that can and will shed insights for the cognitive scientist interested in experience, and I hope that my own work will demonstrate as much.

But this is a very different claim from the one that says monastic Buddhists have a particularly special access to experience. At the end of the day I’m going to hedge my bets with the critical, empirical, and dialectical approach of cognitive science. In fact, I think there may be good reasons to suspect that high-level practitioners are inappropriate participants for “neurophenomenology”. Take for example, the excellent and controversial talk given this year by Willoughby Britton, in which she described how contemplative science had been too quick to sweep under the rug a vast array of negative “side-effects” of advanced practice. These effects included hallucination, de-personalization, pain, and extreme terror. This makes a good deal of sense; advanced meditation practice is less impartial phenomenology and more a rigorous ritualized mental practice embedded in a strong religious context. I believe that across cultures many religions share techniques, often utilizing rhythmic breathing, body postures, and intense belief priming to engender an almost psychedelic state in the practitioner.

What does this mean for cognitive science and enactivism? First, it means we need to respect cultural boundaries and not rush to put one cultural practice on top of the explanatory totem pole. This doesn’t mean cognitive scientists shouldn’t be paying attention to experience, or even practicing and studying meditation, but we have to be careful not to ignore the normativity inherent in any ritualized culture. Embracing this basic realization takes seriously individual and cultural differences in consciousness, something I’ve argued for and believe is essential for the future of 4th wave cognitive science. Neurophenomenology, among other things, should be about recognizing and describing the normativity in our own practices, not importing those of another culture wholesale. I think that this is in line with much of what Varela wrote, and luckily, the tools to do just this are richly provided by the continental phenomenological tradition.

I believe that by carefully bracketing meta-physical and normative concepts, and investigating the vast multitude of phenomenal experience in its full multi-cultural variety, we can begin to shed light on the mind-brain relationship in a meaningful and not strictly reductive fashion. Indeed, in answering the question “are monks expert introspectionists” I think we should carefully question the normative thesis underlying that hypothesis- what exactly constitutes “good” experiential reports? Perhaps by taking a long view on Buddhism and cognitive science, we can begin to truly take the middle way to experience, where we view all experiential reports as equally valid statements regarding some kind of subjective state. The question then becomes primarily longitudinal, i.e. do experiential reports demonstrate a kind of stability or consistency over time, how do trends in experiential reports relate to neural traits and states, and how do these phenomena interact with the particular cultural practices within which they are embedded. For me, this is the central contribution of enactive cognitive science and the best way forward for neurophenomenology.

Disclaimer: I am in no way suggesting enactivists cannot or should not study advanced buddhism if that is what they find interesting and useful. I of course realize that the M&L SRI is a very particular kind of meeting, and that many enactive cognitive scientists can and do work along the lines I am suggesting. My claim is regarding best practices for the core of 4th wave cognitive science, not the fringe. I greatly value the work done by the M&L and found the SRI to be an amazingly fruitful experience.