scholarly journals Temporal–spectral signaling of sensory information and expectations in the cerebral processing of pain

2022 ◽  
Vol 119 (1) ◽  
pp. e2116616119
Author(s):  
Moritz M. Nickel ◽  
Laura Tiemann ◽  
Vanessa D. Hohn ◽  
Elisabeth S. May ◽  
Cristina Gil Ávila ◽  
...  

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 which generate evoked potentials and oscillatory responses at different latencies and frequencies. 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. Here, we therefore 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.

2021 ◽  
Author(s):  
Moritz Nickel ◽  
Laura Tiemann ◽  
Vanessa Hohn ◽  
Elisabeth May ◽  
Cristina Gil Avila ◽  
...  

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.


2015 ◽  
Vol 27 (7) ◽  
pp. 1298-1307 ◽  
Author(s):  
Yuranny Cabral-Calderin ◽  
Carsten Schmidt-Samoa ◽  
Melanie Wilke

When our brain is confronted with ambiguous visual stimuli, perception spontaneously alternates between different possible interpretations although the physical stimulus remains the same. Both alpha (8–12 Hz) and gamma (>30 Hz) oscillations have been reported to correlate with such spontaneous perceptual reversals. However, whether these oscillations play a causal role in triggering perceptual switches remains unknown. To address this question, we applied transcranial alternating current stimulation (tACS) over the posterior cortex of healthy human participants to boost alpha and gamma oscillations. At the same time, participants were reporting their percepts of an ambiguous structure-from-motion stimulus. We found that tACS in the gamma band (60 Hz) increased the number of spontaneous perceptual reversals, whereas no significant effect was found for tACS in alpha (10 Hz) and higher gamma (80 Hz) frequencies. Our results suggest a mechanistic role of gamma but not alpha oscillations in the resolution of perceptual ambiguity.


2017 ◽  
Author(s):  
Michael B. Bone ◽  
Marie St-Laurent ◽  
Christa Dang ◽  
Douglas A. McQuiggan ◽  
Jennifer D. Ryan ◽  
...  

AbstractHalf a century ago, Donald Hebb posited that mental imagery is a constructive process that emulates perception. Specifically, Hebb claimed that visual imagery results from the reactivation of neural activity associated with viewing images. He also argued that neural reactivation and imagery benefit from the re-enactment of eye movement patterns that first occurred at viewing (fixation reinstatement). To investigate these claims, we applied multivariate pattern analyses to functional MRI (fMRI) and eye-tracking data collected while healthy human participants repeatedly viewed and visualized complex images. We observed that the specificity of neural reactivation correlated positively with vivid imagery and with memory for stimulus image details. Moreover, neural reactivation correlated positively with fixation reinstatement, meaning that image-specific eye movements accompanied image-specific patterns of brain activity during visualization. These findings support the conception of mental imagery as a simulation of perception, and provide evidence of the supportive role of eye-movement in neural reactivation.


2021 ◽  
Author(s):  
Silvia EP Bruzzone ◽  
Leonardo Bonetti ◽  
Tiina Paunio ◽  
Katri Kantojarvi ◽  
Marina Kliuchko ◽  
...  

Predictive processing of sounds depends on the constant updating of priors based on exposure to posteriors, which through repeated exposure mediates learning. The result of such corrections to the model is seen in musicians, whose lifelong training results in measurable plasticity of audio-motor brain anatomy and functionality. It has been suggested that the plasticity of auditory predictive processes depends on the interaction between the environment and the individual genetic substrate. However, empirical evidence to this is still missing. BDNF is a critical genetic factor affecting learning and plasticity, and its widely studied functional variant Val66Met single-nucleotide polymorphism offers a unique opportunity to investigate neuroplastic functional changes occurring upon a years-long training. We hypothesised that BDNF gene variations would be driving neuroplasticity of the auditory cortex in musically trained human participants. To this goal, musicians and non-musicians were recruited and divided in Val/Val and Met carriers and their brain activity measured with magnetoencephalography (MEG) while they listened to a regular auditory sequence containing different types of prediction errors. The auditory cortex responses to prediction errors was enhanced in Val/Val carriers who underwent intensive musical training, compared to Met and non-musicians. Our results point at a role of gene-regulated neurotrophic factors in the neural adaptations of auditory processing after long-term training.


2021 ◽  
Author(s):  
Thomas P Hein ◽  
Maria Herrojo Ruiz

AbstractAnxiety influences how the brain estimates and responds to uncertainty. These behavioural effects have been described within predictive coding and Bayesian inference frameworks, yet the associated neural correlates remain unclear. Recent work suggests that predictions in generative models of perception are represented in alpha-beta oscillations (8-30 Hz), while updates to predictions are driven by prediction errors weighted by precision (inverse variance; pwPE) and encoded in gamma oscillations (>30 Hz). We tested whether state anxiety alters the neural oscillatory activity associated with predictions and pwPE during learning. Healthy human participants performed a probabilistic reward-learning task in a volatile environment. In our previous work, we described learning behaviour in this task using a hierarchical Bayesian model, revealing more precise (biased) beliefs about the reward tendency in state anxiety, consistent with reduced learning in this group. The model provided trajectories of predictions and pwPEs for the current study, allowing us to assess their parametric effects on the time-frequency representations of EEG data. Using convolution modelling for oscillatory responses, we found that, relative to a control group, state anxiety increased alpha-beta activity in frontal and sensorimotor regions during processing pwPE, and in fronto-parietal regions during encoding predictions. No effects of state anxiety on gamma modulation were found. Our findings expand prior evidence on the oscillatory representations of predictions and pwPEs into the reward-learning domain. The results suggest that state anxiety modulates oscillatory correlates of pwPE and predictions in generative models, providing insights into a potential mechanism explaining biased belief updating and poorer reward learning.Significance StatementLearning plays a central role in clinical and subclinical anxiety. This study tests whether a temporarily-induced state of anxiety in healthy human participants alters the neural oscillatory patterns associated with predicting and learning from rewards. We found that precision-weighted prediction errors were associated with increases in alpha-beta oscillations in our state anxious group. This finding suggested that anxiety states may inhibit encoding of relevant signals conveying the discrepancy between the predicted and observed reward. State anxiety also increased alpha-beta activity during processing predictions, indicating a stronger reliance on prior beliefs about the reward tendency. The results identify the alteration in alpha-beta oscillations as a candidate mechanism explaining misestimation of uncertainty and maladaptive learning in anxiety.


Autism ◽  
2020 ◽  
Vol 24 (7) ◽  
pp. 1849-1859
Author(s):  
Thijs van Laarhoven ◽  
Jeroen J Stekelenburg ◽  
Mart LJM Eussen ◽  
Jean Vroomen

Autism spectrum disorder is a pervasive neurodevelopmental disorder that has been linked to a range of perceptual processing alterations, including hypo- and hyperresponsiveness to sensory stimulation. A recently proposed theory that attempts to account for these symptoms, states that autistic individuals have a decreased ability to anticipate upcoming sensory stimulation due to overly precise internal prediction models. Here, we tested this hypothesis by comparing the electrophysiological markers of prediction errors in auditory prediction by vision between a group of autistic individuals and a group of age-matched individuals with typical development. Between-group differences in prediction error signaling were assessed by comparing event-related potentials evoked by unexpected auditory omissions in a sequence of audiovisual recordings of a handclap in which the visual motion reliably predicted the onset and content of the sound. Unexpected auditory omissions induced an increased early negative omission response in the autism spectrum disorder group, indicating that violations of the prediction model produced larger prediction errors in the autism spectrum disorder group compared to the typical development group. The current results show that autistic individuals have alterations in visual-auditory predictive coding, and support the notion of impaired predictive coding as a core deficit underlying atypical sensory perception in autism spectrum disorder. Lay abstract Many autistic individuals experience difficulties in processing sensory information (e.g. increased sensitivity to sound). Here we show that these difficulties may be related to an inability to process unexpected sensory stimulation. In this study, 29 older adolescents and young adults with autism and 29 age-matched individuals with typical development participated in an electroencephalography study. The electroencephalography study measured the participants’ brain activity during unexpected silences in a sequence of videos of a handclap. The results showed that the brain activity of autistic individuals during these silences was increased compared to individuals with typical development. This increased activity indicates that autistic individuals may have difficulties in processing unexpected incoming sensory information, and might explain why autistic individuals are often overwhelmed by sensory stimulation. Our findings contribute to a better understanding of the neural mechanisms underlying the different sensory perception experienced by autistic individuals.


2016 ◽  
Vol 125 (2) ◽  
pp. 368-377 ◽  
Author(s):  
M. Stephen Melton ◽  
Jeffrey N. Browndyke ◽  
Todd B. Harshbarger ◽  
David J. Madden ◽  
Karen C. Nielsen ◽  
...  

Abstract Background Limited information exists on the effects of temporary functional deafferentation (TFD) on brain activity after peripheral nerve block (PNB) in healthy humans. Increasingly, resting-state functional connectivity (RSFC) is being used to study brain activity and organization. The purpose of this study was to test the hypothesis that TFD through PNB will influence changes in RSFC plasticity in central sensorimotor functional brain networks in healthy human participants. Methods The authors achieved TFD using a supraclavicular PNB model with 10 healthy human participants undergoing functional connectivity magnetic resonance imaging before PNB, during active PNB, and during PNB recovery. RSFC differences among study conditions were determined by multiple-comparison–corrected (false discovery rate–corrected P value less than 0.05) random-effects, between-condition, and seed-to-voxel analyses using the left and right manual motor regions. Results The results of this pilot study demonstrated disruption of interhemispheric left-to-right manual motor region RSFC (e.g., mean Fisher-transformed z [effect size] at pre-PNB 1.05 vs. 0.55 during PNB) but preservation of intrahemispheric RSFC of these regions during PNB. Additionally, there was increased RSFC between the left motor region of interest (PNB-affected area) and bilateral higher order visual cortex regions after clinical PNB resolution (e.g., Fisher z between left motor region of interest and right and left lingual gyrus regions during PNB, −0.1 and −0.6 vs. 0.22 and 0.18 after PNB resolution, respectively). Conclusions This pilot study provides evidence that PNB has features consistent with other models of deafferentation, making it a potentially useful approach to investigate brain plasticity. The findings provide insight into RSFC of sensorimotor functional brain networks during PNB and PNB recovery and support modulation of the sensory–motor integration feedback loop as a mechanism for explaining the behavioral correlates of peripherally induced TFD through PNB.


2019 ◽  
Author(s):  
Hame Park ◽  
Christoph Kayser

AbstractMultisensory stimuli create behavioral flexibility, e.g. by allowing us to derive a weighted combination of the information received by different senses. They also allow perception to adapt to discrepancies in the sensory world, e.g. by biasing the judgement of unisensory cues based on preceding multisensory evidence. While both facets of multisensory perception are central for behavior, it remains unknown whether they arise from a common neural substrate. In fact, very little is known about the neural mechanisms underlying multisensory perceptual recalibration. To reveal these, we measured whole-brain activity using MEG while human participants performed an audio-visual ventriloquist paradigm designed to reveal multisensory integration within a trial, and the (trial-by-trial) recalibration of subsequent unisensory judgements. Using single trial classification and behavioral modelling, we localized the encoding of sensory information within and between trials, and determined the behavioral relevance of candidate neural representations. While we found neural signatures of perceptual integration within temporal and parietal regions, of these, only medial superior parietal activity retained multisensory information between trials and combined this with current evidence to mediate perceptual recalibration. These results suggest a common neural substrate of sensory integration and trial-by-trial perceptual recalibration, and expose the medial superior parietal cortex as a flexible hub that links present and previous evidence within and between senses to guide behavior.


2020 ◽  
Author(s):  
Elisabeth S. May ◽  
Vanessa D. Hohn ◽  
Moritz M. Nickel ◽  
Laura Tiemann ◽  
Cristina Gil Ávila ◽  
...  

AbstractPain protects the body. However, pain can also occur for longer periods without serving protective functions. Such chronic pain conditions are difficult to treat. Thus, a better understanding of the underlying neural mechanisms and new approaches for the treatment of pain are urgently needed. Here, we investigated a causal role of oscillatory brain activity for pain and explored the potential of transcranial alternating current stimulation (tACS) as a new treatment approach for pain. To this end, we investigated whether tACS can modulate pain and pain-related autonomic activity in 29 healthy human participants using a tonic heat pain paradigm as an experimental model of chronic pain. In 6 recording sessions, participants received tACS over prefrontal or somatosensory cortices at alpha or gamma frequencies or sham tACS. During tACS, pain ratings and autonomic responses were collected. TACS did not modulate pain intensity, the stability of pain ratings or the translation of the noxious stimulus into pain. Likewise, tACS did not change autonomic responses. Bayesian statistics further indicated a lack of tACS effects in most conditions. The only exception was alpha tACS over somatosensory cortex where evidence for tACS effects was inconclusive. Taken together, the present study did not find significant tACS effects on tonic experimental pain in healthy human participants. However, considering the conceptual plausibility of using tACS to modulate pain and the urgent need for novel pain treatments, further tACS studies are warranted. Based on the present findings, such studies might apply refined stimulation protocols targeting alpha oscillations in somatosensory cortices.


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