Temporal-spectral signaling of sensory information and expectations in the cerebral processing of pain

Abstract

The perception of pain is shaped by somatosensory information about threat. However, pain is also influenced by an individual’s expectations. Such expectations can result in clinically relevant modulations and abnormalities of pain. In the brain, sensory information, expectations (predictions), and discrepancies thereof (prediction errors) are signaled by an extended network of brain areas. These brain areas generate evoked potentials and oscillatory responses at different latencies and frequencies. Recent evidence has provided first insights into how oscillatory responses at different frequencies signal predictions and prediction errors. However, a comprehensive picture of how evoked and oscillatory brain responses signal sensory information, predictions, and prediction errors in the processing of pain is lacking so far. We therefore built upon a neuroimaging study which investigated the spatial signalling of sensory information, predictions and predictions errors in the processing of pain (Geuter et al., 2017). To complement and extend this study, we applied brief painful stimuli to 48 healthy human participants and independently modulated sensory information (stimulus intensity) and expectations of pain intensity while measuring brain activity using electroencephalography (EEG). Pain ratings confirmed that pain intensity was shaped by both sensory information and expectations. In contrast, Bayesian analyses revealed that stimulus-induced EEG responses at different latencies (the N1, N2, and P2 components) and frequencies (alpha, beta, and gamma oscillations) were shaped by sensory information but not by expectations. Expectations, however, shaped alpha and beta oscillations before the painful stimuli. These findings indicate that commonly analyzed EEG responses to painful stimuli are more involved in signaling sensory information than in signaling expectations or mismatches of sensory information and expectations. Moreover, they indicate that the effects of expectations on pain are served by brain mechanisms which differ from those conveying effects of sensory information on pain.