Prediction and action in cortical pain processing

Abstract

Predicting that a stimulus is painful facilitates action to avoid harm. But does the prediction of upcoming painful events engage the same or different processes than acting to avoid or reduce current pain? In this fMRI experiment, we investigated brain activity as a function of current and predicted painful or nonpainful thermal stimulation, and the ability of voluntary action to affect the duration of the upcoming stimulation. Participants (n = 30) performed a task which involved the administration of a painful or nonpainful stimulus (S1), which predicted an immediately subsequent very painful or nonpainful stimulus (S2). Participants' task was to press a response button within a short time window upon the presentation of a response cue during S1. On action-effective trials, pressing the button within the specified time window reduced the duration of the upcoming stimulation. On action-ineffective trials, pressing the button had no effect on upcoming stimulation. Predicted pain increased activation in regions including anterior cingulate cortex (ACC), midcingulate cortex (MCC), and insula; however, activation in ACC and MCC depended on whether a meaningful action was performed, with MCC activation showing a direct relationship with motor output. Region-of-interest analyses revealed that insula's responses for predicted pain were also modulated by potential action consequences, especially in the left hemisphere, albeit without a direct relationship with motor output. Taken together, these findings suggest that cortical pain processing is not specifically tied to the sensory stimulus, but instead depends on the consequences of that stimulus for sensorimotor control of behavior.

Whole brain surface-based morphometry and tract-based spatial statistics in migraine with aura patients: difference between pure visual and complex auras

“…This concords with previous studies reporting deactivation of extensive occipital, frontal and temporal cortical areas during central sensitization (Iannetti et al, 2005) that is known to be one of the mechanisms underlying hyperalgesia and allodynia during the migraine headache phase (Coppola et al, 2013). In particular, the large calcarine area is involved in the processing of cognitive, affective, and sensory aspects of pain (Coghill et al, 1999;Coppola et al, 2010), the postcentral gyri in that of pain-related emotions and upcoming pain prediction (Yoshino et al, 2017;Koppel et al, 2022) in conjunction with the middle cingulate cortex and the insula (both thinned in MA). The insula, in turn, is a hub highly connected with areas of the temporal and frontal lobes, the latter showing thinned cortical areas both in MA and MA+.…”

Hierarchical predictive coding in distributed pain circuits

“…In a recent study, participants performed a task that involved predicting a painful or nonpainful stimulus based on the administration of another painful or nonpainful stimulus. It was found that predicted pain increased activations in the ACC, MCC, AIC, and MIC; the MCC activation showed a direct relationship with the motor output, whereas the insula activation was modulated by potential action consequences (Koppel et al, 2023). However, because of the limited spatiotemporal resolution, human neuroimaging only provides correlational findings.…”

“…In a cross-modality (pain vs. sound) pain study, it has been reported that the AIC response correlates with unsigned intensity PEs as a modality-unspecific aversive surprise signal, whereas dorsal PIC encodes the modality-specific signed intensity PE (Horing and Büchel, 2022). Importantly, pain processing in AIC is modulated by both prediction and action, suggesting its role in mediating pain anticipation (Koppel et al, 2023). Together, the AIC and PIC provide a neural mechanism for predictive coding, and aberrant pain processing may be interpreted as disturbed weighting of predictions and PEs.…”