Abstract
There are bi-directional interactions between the autonomic nervous system (ANS) and pain. This is likely underpinned by a substantial overlap between brain areas of the central autonomic network and areas involved in pain processing and modulation. To date, however, relatively little is known about the neuronal substrates of the ANS-pain association. Here, we acquired resting state fMRI scans in 21 healthy subjects at rest and during tonic noxious cold stimulation. As indicators of autonomic function, we examined how heart rate variability (HRV) frequency measures were influenced by tonic noxious stimulation and how these variables related to participants’ pain perception and to brain functional connectivity in regions known to play a role in both ANS regulation and pain perception, namely the right dorsal anterior cingulate cortex (dACC) and periaqueductal gray (PAG). Our findings support a role of the cardiac ANS in brain connectivity during pain, linking functional connections of the dACC and PAG with measurements of low frequency (LF)-HRV. In particular, we identified a three-way relationship between the ANS, cortical brain networks known to underpin pain processing, and participants’ subjectively reported pain experiences. LF-HRV both at rest and during pain correlated with functional connectivity between the seed regions and other cortical areas including the right dorsolateral prefrontal cortex (dlPFC), left anterior insula (AI), and the precuneus. Our findings link cardiovascular autonomic parameters to brain activity changes involved in the elaboration of nociceptive information, thus beginning to elucidate underlying brain mechanisms associated with the reciprocal relationship between autonomic and pain-related systems.
Highlights
Neural networks involved in pain processing are intimately linked to the autonomic nervous system (ANS) (Benarroch, 2006): On the one hand, the body’s response to pain is defined by changes in ANS parameters (Kyle and McNeil, 2014); on the other, alterations in autonomic arousal can influence the experience of pain (Terkelsen et al, 2004)
We found an overall increase in logLF-heart rate variability (HRV) from Baseline to Cold-pain [mean (SD) = 2.91 (0.41) and 2.94 (0.46), respectively; F(1,17) = 7.79, p = 0.013]
As regards logHF-HRV, we did not observe a significant difference between Baseline and Cold-pain conditions (F < 1), nor was there an effect of Interval (F < 1) or a Condition × Interval interaction effect (F < 1)
Summary
Neural networks involved in pain processing are intimately linked to the autonomic nervous system (ANS) (Benarroch, 2006): On the one hand, the body’s response to pain is defined by changes in ANS parameters (Kyle and McNeil, 2014); on the other, alterations in autonomic arousal can influence the experience of pain (Terkelsen et al, 2004). There is growing interest in mindfulness-based and other mind-body interventions in the treatment and management of pain (Stanos, 2012; Goyal et al, 2014), with changes in autonomic balance one of the likely underlying mechanisms of action (Tang et al, 2015). One possible mechanism underlying this pain-autonomic interaction is the baroreflex, the negative feedback loop used to maintain stable blood-pressure (Suarez-Roca et al, 2018). This mechanism has been associated with observed reduction in pain perception in healthy controls during spontaneous high blood pressure (during which baroreceptors are activated) and during mechanical stimulation of baroreceptors (Edwards et al, 2001; Duschek et al, 2007; Reyes del Paso et al, 2014). Decreased baroreceptor sensitivity has been described in some chronic pain conditions (Davydov et al, 2018)
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