Local brain oscillations and inter-regional connectivity differentially serve sensory and expectation effects on pain

Abstract

Pain emerges from the integration of sensory information about threats and contextual information such as an individual's expectations. However, how sensory and contextual effects on pain are served by the brain is not fully understood so far. To address this question, we applied brief painful stimuli to 40 healthy human participants and independently varied stimulus intensity and expectations. Concurrently, we recorded electroencephalography. We assessed local oscillatory brain activity and inter-regional functional connectivity in a network of six brain regions playing key roles in the processing of pain. We found that sensory information predominantly influenced local brain oscillations. In contrast, expectations exclusively influenced inter-regional connectivity. Specifically, expectations altered connectivity at alpha (8-12 Hz) frequencies from prefrontal to somatosensory cortex. Moreover, discrepancies between sensory information and expectations, i.e., prediction errors, influenced connectivity at gamma (60-100 Hz) frequencies. These findings reveal how fundamentally different brain mechanisms serve sensory and contextual effects on pain.

Cue-based modulation of pain stimulus expectation: do ongoing oscillations reflect changes in pain perception? A registered report

“…Bott et al . [19] have provided interesting results using the same cue-based expectation paradigm as in a study by Nickel et al . [18], expanding the analysis from local oscillatory activity to interregional connectivity in a network of six pre-selected ROI associated with pain perception (such as contralateral primary somatosensory cortex, anterior cingulate and prefrontal cortices).…”

“…This is largely owing to the high signal-to-noise ratio in the periodic responses to the ultra-slow 0.2 Hz sustained periodic stimulation, which can even be differentiated from noise at an individual level [2]. Other investigations using cue-based expectation modulation while acquiring EEG data recruited between 10 and 20 participants per experiment [8,9,11,13,20] and more recent investigations recruited between 40 and 48 participants [18,19].…”

“…[18] regarding pre-stimulus activity in a predictive coding paradigm, changes in pain perception induced by expectation did not seem to have an effect on the modulation of ongoing oscillations. Another recent investigation found that, while expectations and prediction errors did not lead to any changes in local brain activity at the regions of interest (ROI), they did modulate the interregional connectivity within the chosen ROIs in the alpha and gamma frequency bands [19]. As discussed by Nickel et al .…”

It’s the Sound, not the Pulse: Peripheral Magnetic Stimulation Reduces Central Sensitization through Auditory Modulatory Effects

“…Most studies investigating brain oscillations and pain have focused on alpha and gamma oscillations as these are often the most prominent oscillation bands found to be associated with pain intensity [9,[16][17][18][19]22,51,58].…”

Pain reflects the informational value of nociceptive inputs

“…Pain not only serves as a warning signal, but it also teaches us to identify and avoid future threats [50]. This intimate link between pain and learning is supported by studies showing that the prediction error (PE) signals necessary to learn from pain are linked to activity in cerebral targets of ascending nociceptive pathways [24,29,48], as well as to changes in gamma oscillations in response to surprising pain [8,55]. However, it remains unclear if the learning processes related to pain occur separately from the processes associated with subjectively perceived pain [8] or if perceived pain is more deeply tied to its learning function [17,55].…”