Distraction modulates connectivity of the cingulo-frontal cortex and the midbrain during pain—an fMRI analysis

TLDR

Neuroimaging has mapped a human pain network, yet the cerebral mechanisms of pain modulation remain poorly understood. The study investigated healthy volunteers with fMRI during experimental heat pain and distraction induced by a visual incongruent color‑word Stroop task. A factorial design enabled categorical and covariation analysis of innocuous and noxious heat with and without distraction. Pain without distraction produced activation patterns similar to prior studies, while distraction reduced pain ratings and pain‑related activation—especially in the medial pain system—and increased activation of the cingulo‑frontal cortex, periaqueductal gray, and posterior thalamus, with covariation analysis revealing functional interaction among these structures during distraction but not during pain alone, suggesting top‑down modulation of pain by the cingulo‑frontal cortex.

Abstract

Neuroimaging studies with positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) have delineated a human pain network in vivo. Despite the recognition of cerebral structures engaged in pain transmission, the cerebral mechanisms involved in pain modulation are still not well understood. Here, we investigated healthy volunteers using fMRI during experimental heat pain and distraction induced by a visual incongruent color-word Stroop task. A factorial design permitted categorical and covariation analysis of four conditions, namely innocuous and noxious heat; with and without distraction. Pain without distraction evoked an activation pattern similar to that observed in previous neuroimaging pain studies. Distraction was associated with a significant reduction of the visual analogue scale (VAS) ratings for pain intensity and unpleasantness and a reduction of pain-related activation in multiple brain areas, particularly in the so-called ‘medial pain system’. Distraction significantly increased the activation of the cingulo-frontal cortex including the orbitofrontal and perigenual anterior cingulate cortex (ACC), as well as the periaquaeductal gray (PAG) and the posterior thalamus. Covariation analysis revealed functional interaction between these structures during pain stimulation and distraction, but not during pain stimulation per se. According to our results, the cingulo-frontal cortex may exert top–down influences on the PAG and posterior thalamus to gate pain modulation during distraction.