The Restless Resting State, and Why Brain Scanning is Still Valid
By Thomas Zoëga Ramsøy
Is brain scanning data invalid? A recent meta-analysis study published in the esteemed journal PNAS (http://www.pnas.org/content/113/28/7900.abstract) has suggested that decades of brain research studies should be questioned! An estimated 40,000 studies using the established and used method fMRI (or functional Magnetic Resonance Imaging) may be hampered by a software bug that has gone undetected for too long.
In the study, several brain scanning studies of the so-called “resting-state data” suggest that as many as 70% of “positive findings” may indeed be false. That is, 7 out of 10 reported “brain blobs” found when people are resting inside a brain scanner may in fact never be there!
This is a very interesting finding indeed. It sure reminds us of the need for replications in science, a part of scientific housecleaning that is never honoured as part of a scientist’s career. It is worth noting that the finding pertains to only one type of neuroimaging studies, fMRI (and most likely only the so-called blood oxygenation level dependent, or BOLD, fMRI), and not other methods such as electroencephalography (EEG) or magnetoencephalography (MEG). Still, the problem could be substantial, as many of our insights about the brain may be unsupported.
But is it really that bad? There is a saying that “extraordinary claims require extraordinary evidence” and here, we have a problem. Indeed, one major caveat of the study is the assumption that the resting-state data, used in this meta-analysis, can be treated as equal between individual. After all, when asking people to rest (often between more active tasks), we can assume that the brain at rest is similar for us all, correct? Instead, decades of psychological studies of the mind at rest – including mind-wandering and Task Unrelated Images and Thoughts – have shown extreme degrees of variation both within and between individuals. What follows are inspired by a yet unpublished manuscript that I have co-authored with Prof. Bernard J Baars from the Neuroscience Institute, which I hope can help put a perspective to the intended killing of fMRI.
The restless resting state
Considerable attention has been called to a putative “resting state” of the brain, observed during designated rest breaks in neuroimaging experiments. Robust brain differences have been found between task-related (TR) and task-unrelated (rest break) conditions. Some scientists speculate that TU brain activity may reflect a special state of the brain, sometimes called a “resting state,” “default mode,” or a “baseline condition”. We suggest that the explanatory use of these terms is premature. Instead, a large empirical literature points to an alternative account: people during rest breaks are reverting to their normal, spontaneous stream of thought, which is subjectively rich and self-relevant, highly variable, multimodal, often explicitly goal-directed, and probably functional. Even the word “state” may be premature, since it suggests a stable condition of the brain. Instead, some five decades of psychological studies shows TU activities to be dynamic, heterogeneous, shaped by emotional and motivational primes, and focused on current life concerns. The term “spontaneous thought” might therefore be a more accurate label for task-unrelated brain activity.
The spontaneous brain
Scientists tend to be cautious about self-reported experiences, but some facts about consciousness are as predictable as objects falling in earth gravity. The entire field of psychophysics relates precisely controlled stimuli to reliable subjective reports. Even endogenous events can be reported reliably, as in experimental studies of verbal rehearsal and visual imagery, and their brain correlates. Less well-known is almost a half century of thought-sampling studies, using real-time reports under known conditions. One of the oldest psychological demonstrations is to simply close one’s eyes and try to stop the flow of thought. We can read sources over some 26 centuries reporting how difficult that is to accomplish. The flow of spontaneous experience appears to have its own persistence and “urgency,” as William James wrote a century ago. Some five decades of systematic psychological research supports the notion that spontaneous cognition is not random, but reflects “current, personal concerns”. There is also evidence for repetitive long-term themes in spontaneous mentation, influenced by major life events, traumatic experiences, and implicit goals. In everyday life, spontaneous, apparently unstructured thinking may be the most common kind of goal-directed thought.
What happens when people go from a focused, externally instructed cognitive task to a condition that is not heavily structured by external demands? To many subjects, designated rest breaks may be a chance to get back to a normal, spontaneous, self-relevant, and active stream of thought. In the 1960’s and 1970’s a number of studies in experimental psychology focused on internally generated images and thoughts, which showed that depriving the mind from sensory information stimulated the occurrence of internally generated experiences. TU thoughts were studied in a more elaborate and specific research program called Task Unrelated Images and Thoughts (TUITS). Here, subjects were asked to report with regular intervals the content of their thoughts. This could either be performed in laboratory settings, in which subjects were given a tasks of varying difficulty and attentional load, or they could focus on more everyday settings, where subjects were interrupted at random times during a day, and were to write down their ongoing thoughts. One of the general findings from this research was that there is a continuous shifting of attention between externally and internally generated sources of information. Furthermore, spontaneous thoughts were found to be rather repetitive and predictable, always returning to “current concerns”. The content of thought was found to become increasingly unrelated to external events as these external events become more static and predictable. In this sense, the more boring the task, the more did people spend time (during testing) on task-irrelevant thoughts.
More recently, the study of TUITS has re-emerged in the scientific literature. A portion of this research has focused on detailed observations about the influence of TUITS on cognitive performance and a detailed examination of the intrusiveness of the task unrelated thoughts on both ongoing and later performance. Other studies have begun to couple the occurrence of TUITS to measurable physiological changes such as increased heart rate during TUITS. As with the original TUIT studies, these results confirm that increases in task difficulty, altering the attentional load, make TUITS become significantly less frequent. On the other hand, the easier the task – leading to more automatic behaviour – the more TUITS are reported by subjects. In this sense, a rest state is only at one extreme of how much attentional load is put on a subject’s mind. At the other end are highly energy- and attention-demanding tasks such as working memory 2-back or 3-back tasks. The conditions we are comparing in a resting state study are vital to our interpretation of the results.
Daydreaming was also studied in the same period as TUITS was explored. Using the “Imaginal processes inventory” it was shown that people were aware of some daydreaming every day, and that daydreams ranged from “obvious wishful thinking to elaborate and complex visions of frightening or guilty encounters”. Furthermore, factor analyses have revealed three major types of daydreaming: positive-constructive; guilty-dysphoric; and a poor attentional control pattern characterized by fleeting thoughts and an inability to focus on extended fantasy. At the same time, the test-retest reliability of daydreaming reports has been found to be high. As such, the literature on TUITS and daydreaming, both highly relevant inputs to the study of RS, is both rich in number of studies and in information about the richness of conscious content during such periods.
The non-death of fMRI findings
So what may initially seem like a failure of replication of brain scanning data, may in fact be a failure to understand the human mind. Many neuroscientists just don’t know the psychological literature enough to see that that the human mind does not “do anything” when asked to rest and relax. Indeed, as we have seen above, the mind is never at rest, and when not given an explicit task, it will defer to an inner state of “current concerns.”
So the basic assumption of this meta-analysis is flawed, and we should treat the conclusion accordingly. Analysing resting state brain activity and assuming that the results will be convergent is the same as claiming that every human mind at any time is thinking about the same things.
That said, we still replications of brain scanning studies, as we would need whether one scanning method is valid. Here, neuroscience fortunately has a vast toolbox, and now classical work from leading figures such as Nicos Logosthetis has provided clear links between fMRI studies and other measures of brain activity. For example, Logosthetis’ work has clearly shown that fMRI activation “blobs” are related to dendritic activity, rather than axonal activity. Still, there is nothing in these data to support a claim that fMRI data are invalid. Indeed, extraordinary claims have not been supported by extraordinary evidence in this case.
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