Pain is an attention hog. Normally, our awareness constantly fluctuates from our immediate environment, away to thoughts of the past or future, and back again. But a painful stimulus grabs one’s attention. People vary in how they attend to ongoing pain; some focus on it, while others can let their minds wander. A new imaging study from Karen Davis and colleagues at the University of Toronto, Canada, illuminates the brain circuitry underlying fluctuations in attention during pain and how activity in the brain differs between people who can zone out during pain and others who remain laser focused on the sensation.
A key factor in the tendency to wander away from pain appears to be communication between descending antinociceptive circuits and the default-mode network (DMN), a set of interconnected brain structures involved in attention.
The work, presented by Aaron Kucyi at the annual meeting of the Society for Neuroscience in San Diego, California, US, November 9-13, 2013, was published in the Proceedings of the National Academy of Sciences (Kucyi et al., 2013).
In the study, 51 healthy subjects received transcutaneous electrical nerve stimulation (TENS) on the forearm to create a moderately painful sensation. Importantly, subjects were instructed to avoid directing their attention either toward or away from the pain. Whereas previous studies have looked at directed attention during pain, the researchers did not instruct subjects on a particular task. “We wanted to see the natural fluctuations without any manipulation,” Davis told PRF.
Kucyi then came up with a metric to describe how each subject attended to pain. After 20 seconds of pain, subjects received a “thought probe” that directed them to indicate whether they were thinking only or mostly about the pain, or only or mostly about something else. After 20 such trials, the subjects were given a score for their “intrinsic attention to pain,” or IAP, which ranged from +2 (always thinking about pain) to -2 (always thinking about something else). While subjects’ attention to pain varied significantly from trial to trial within a session, the overall IAP score for each person was consistent between two sessions, suggesting that the tendency to attend to pain behaved like an intrinsic trait. Also, when asked to categorize the “something else” they thought about other than pain as either external sensory distractions in the room, internal thoughts about the task at hand, or mind wandering unrelated to the immediate situation, individuals showed consistency in the type of distraction they reported.
The investigators measured subjects’ tendency to mind wander under normal, non-pain conditions using a daydreaming frequency questionnaire and found no difference between people with a lower or higher attention to pain. That suggests that “daydreamers” are not necessarily good at tuning out pain, and that the two characteristics are different aspects of personality, Kucyi told PRF.
To look at the underlying neural correlates of fluctuations in attention during pain, the investigators re-did the pain trials with the same subjects while performing functional magnetic resonance imaging (fMRI). As expected, when subjects reported thinking about pain, pain-related brain regions including the thalamus and somatosensory cortices were more active. Attending to pain also invoked activity in the insula and the temporoparietal junction, areas associated with “attending to one’s sensory environment,” Davis told PRF.
The researchers next examined activity in the default-mode network (DMN), a set of functionally connected brain structures that are active in the resting or wandering mind but deactivated when attention is engaged. The network includes the medial prefrontal cortex (mPFC) and the posterior cingulate cortex (PCC)/precuneus, which communicate with one another via rich axonal connections. (For a review about the DMN, see Raichle and Snyder, 2007.)
When subjects paid attention to the painful stimulus, the DMN nodes deactivated, as expected. But when subjects thought about something else, DMN activity depended on the nature of the thoughts. The DMN was deactivated when subjects were distracted from pain by noises in the room or by thinking about the upcoming task, but if the distraction was due to mind wandering, the DMN was not deactivated. Under that condition, “its activity level looks similar to when someone is resting with no painful stimulation,” Kucyi explained.
“In the context of pain, the role of the DMN remains under debate, but it has also been quite understudied,” Kucyi told PRF in an email. Whereas some studies have shown pain-related DMN deactivation, others have reported DMN activation, and some have found more complex relationships (see Loggia et al., 2012). “Our study shows for the first time that the way pain engages the DMN depends on how people are paying attention to pain,” he added.
The investigators next looked at the functional interaction of the DMN and the periaqueductal gray (PAG), the hub of the brain’s antinociceptive descending pain modulatory system. The opioid-rich midbrain structure connects with the cingulate and prefrontal cortex—attention-related brain centers involved in cognitive control of pain—and sends projections down to the spinal cord.
When attention wandered away from pain, the MRI images showed functional interactions between the PAG and the DMN not seen when attention was on pain. “That suggests that the DMN is talking to the PAG,” Davis said.
“We know there is structural connectivity between the mPFC [a key node in the DMN] and the PAG,” Davis said. By using diffusion tensor imaging to visualize white matter tracts between the two brain regions, the investigators revealed differences in brain structure that tracked individual differences in attention to pain. “People with a high IAP had the weakest connectivity between regions, but people who could easily tune out the pain had greater connectivity between the regions,” Davis told PRF.
Finally, to further investigate the contribution of mPFC-PAG communication to individual differences in IAP, the team looked at the strength of functional connectivity in the two regions in subjects in the absence of pain. A resting BOLD fMRI signal, averaged over nine minutes, indicated that functional connectivity between the brain regions did not influence IAP. The investigators next measured dynamic fluctuations in connectivity within much shorter time windows. When they analyzed the variability in the connectivity, which indicates spontaneous fluctuations in attention, they saw that people who more readily disengaged from pain (those with a low IAP score), had more fluctuations in mPFC-PAG functional connectivity, whereas high IAP scorers who focused on pain had more static connectivity.
Did people whose minds wandered away from pain see any benefit—less pain intensity or unpleasantness, for example? “We cannot infer whether people who pay less attention to pain are also less bothered by it,” Kucyi said in an email. Because they wanted to examine freely fluctuating attention, the researchers could not ask subjects to rate pain, which would have drawn attention to the pain. The finding that PAG was active when the subjects were disengaged from pain presents the alluring possibility that certain attention states can engage endogenous pain modulation, but that question remains to be answered in future work.
The findings illustrate how the brain manages its switching of attention during pain, Davis explained. Once those switching mechanisms are understood, she added, they could be targeted with various strategies to better manage pain.
Stephani Sutherland, PhD, is a neuroscientist, yogi, and freelance writer in Southern California, US.
Image: Aaron Kucyi and Karen Davis.