Frontiers in Human

Automatic Sensory Predictions: A Review of Predictive Mechanisms in the Brain and Their Link to Conscious Processing

Abstract:

The human brain has the astonishing capacity of integrating streams of sensory information from the environment and forming predictions about future events in an automatic way. Despite being initially developed for visual processing, the bulk of predictive coding research has subsequently focused on auditory processing, with the famous mismatch negativity signal as possibly the most studied signature of a surprise or prediction error (PE) signal. Auditory PEs are present during various consciousness states. Intriguingly, their presence and characteristics have been linked with residual levels of consciousness and return of awareness. In this review we first give an overview of the neural substrates of predictive processes in the auditory modality and their relation to consciousness. Then, we focus on different states of consciousness - wakefulness, sleep, anesthesia, coma, meditation, and hypnosis - and on what mysteries predictive processing has been able to disclose about brain functioning in such states. We review studies investigating how the neural signatures of auditory predictions are modulated by states of reduced or lacking consciousness. As a future outlook, we propose the combination of electrophysiological and computational techniques that will allow investigation of which facets of sensory predictive processes are maintained when consciousness fades away.

Authors:

  • Ruxandra I. Tivadar

  • Robert T. Knight

  • Athina Tzovara

Date: 2021

DOI: https://doi.org/10.3389/fnhum.2021.702520

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Anterior thalamic high frequency band activity is coupled with theta oscillations at rest

ABSTRACT

Cross-frequency coupling (CFC) between slow and fast brain rhythms, in the form of phase–amplitude coupling (PAC), is proposed to enable the coordination of neural oscillatory activity required for cognitive processing. PAC has been identified in the neocortex and mesial temporal regions, varying according to the cognitive task being performed and also at rest. PAC has also been observed in the anterior thalamic nucleus (ATN) during memory processing. The thalamus is active during the resting state and has been proposed to be involved in switching between task-free cognitive states such as rest, in which attention is internally-focused, and externally-focused cognitive states, in which an individual engages with environmental stimuli. It is unknown whether PAC is an ongoing phenomenon during the resting state in the ATN, which is modulated during different cognitive states, or whether it only arises during the performance of specific tasks. We analyzed electrophysiological recordings of ATN activity during rest from seven patients who received thalamic electrodes implanted for treatment of pharmacoresistant focal epilepsy. PAC was identified between theta (4–6 Hz) phase and high frequency band (80–150 Hz) amplitude during rest in all seven patients, which diminished during engagement in tasks involving an external focus of attention. The findings are consistent with the proposal that theta–gamma coupling in the ATN is an ongoing phenomenon, which is modulated by task performance.

AUTHORS

  • Catherine M. Sweeney-Reed

  • Tino Zauhle

  • Jürgen Voges

  • Friedhelm Schmitt

  • Lars Buentjen

  • Viola Borchardt

  • Hermann Hinrichs

  • Hans-Jochen Heinze

  • Michael D. Rugg

  • Robert T. Knight

Date: 2017

DOI: 10.3389/fnhum.2017.00358

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Atypical brain mechanisms of prediction according to uncertainty in autism

ABSTRACT

Resistance to change is often reported in autism and may arise from an inability to predict events in uncertain contexts. Using EEG recorded in 12 adults with autism and age-matched controls performing a visual target detection task, we characterized the influence of a certain context (targets preceded by a predictive sequence of three distinct stimuli) or an uncertain context (random targets) on behavior and electrophysiological markers of predictive processing. During an uncertain context, adults with autism were faster than controls to detect targets. They also had an enhancement in CNV amplitude preceding all random stimuli—indexing enhanced preparatory mechanisms, and an earlier N2 to targets—reflecting faster information processing—compared to controls. During a certain context, both controls and adults with autism presented an increase in P3 amplitude to predictive stimuli—indexing information encoding of the predictive sequence, an enhancement in CNV amplitude preceding predictable targets—corresponding to the deployment of preparatory mechanisms, and an earlier P3 to predictable targets—reflecting efficient prediction building and implementation. These results suggest an efficient extraction of predictive information to generate predictions in both controls and adults with autism during a certain context. However, adults with autism displayed a failure to decrease mu power during motor preparation accompanied by a reduced benefit in reaction times to predictable targets. The data reveal that patients with autism over-anticipate stimuli occurring in an uncertain context, in accord with their sense of being overwhelmed by incoming information. These results suggest that adults with autism cannot flexibly modulate cortical activity according to changing levels of uncertainty.




AUTHORS

  • Alix Thillay

  • Mathieu Lemaire

  • S. Roux

  • Emmanuelle Houy-Durand

  • C. Barthelemy

  • Robert T. Knight

  • Aurélie Bidet-Caulet

  • Frederique Bonnet-Brilhault

Date: 2016

DOI: 10.3389/fnins.2016.00317

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Behavioral and EEG Evidence for Auditory Memory Suppression

ABSTRACT

The neural basis of motivated forgetting using the Think/No-Think (TNT) paradigm is receiving increased attention with a particular focus on the mechanisms that enable memory suppression. However, most TNT studies have been limited to the visual domain. To assess whether and to what extent direct memory suppression extends across sensory modalities, we examined behavioral and electroencephalographic (EEG) effects of auditory TNT in healthy young adults by adapting the TNT paradigm to the auditory modality. Behaviorally, suppression of memory strength was indexed by prolonged response time (RTs) during the retrieval of subsequently remembered No-Think words. We examined task-related EEG activity of both attempted memory retrieval and inhibition of a previously learned target word during the presentation of its paired associate. Event-related EEG responses revealed two main findings: (1) a centralized Think > No-Think positivity during auditory word presentation (from approximately 0–500 ms); and (2) a sustained Think positivity over parietal electrodes beginning at approximately 600 ms reflecting the memory retrieval effect which was significantly reduced for No-Think words. In addition, word-locked theta (4–8 Hz) power was initially greater for No-Think compared to Think during auditory word presentation over fronto-central electrodes. This was followed by a posterior theta increase indexing successful memory retrieval in the Think condition. The observed event-related potential pattern and theta power analysis are similar to that reported in visual TNT studies and support a modality non-specific mechanism for memory inhibition. The EEG data also provide evidence supporting differing roles and time courses of frontal and parietal regions in the flexible control of auditory memory.




AUTHORS

  • Maya Cano

  • Robert T. Knight

Date: 2016

DOI: 10.3389/fnhum.2016.00133

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Sustained attention and prediction: distinct brain maturation trajectories during adolescence

ABSTRACT

Adolescence is a key period for frontal cortex maturation necessary for the development of cognitive ability. Sustained attention and prediction are cognitive functions critical for optimizing sensory processing, and essential to efficiently adapt behaviors in an ever-changing world. The aim of the current study was to investigate the brain developmental trajectories of attentive and predictive processing through adolescence. We recorded EEG in 36 participants from the age of 12–24 years (three age groups: 12–14, 14–17, 18–24 years) to target development during early and late adolescence, and early adulthood. We chose a visual target detection task which loaded upon sustained attention, and we manipulated target predictability. Continued maturation of sustained attention after age 12 was evidenced by improved performance (hits, false alarms (FAs) and sensitivity) in a detection task, associated with a frontal shift in the scalp topographies of the Contingent Negative Variation (CNV) and P3 responses, with increasing age. No effect of age was observed on predictive processing, with all ages showing similar benefits in reaction time, increases in P3 amplitude (indexing predictive value encoding and memorization), increases in CNV amplitude (corresponding to prediction implementation) and reduction in target-P3 latency (reflecting successful prediction building and use), with increased predictive content. This suggests that adolescents extracted and used predictive information to generate predictions as well as adults. The present results show that predictive and attentive processing follow distinct brain developmental trajectories: prediction abilities seem mature by the age of 12 and sustained attention continues to improve after 12-years of age and is associated with maturational changes in the frontal cortices.




AUTHORS

  • Alix Thillay

  • S. Roux

  • Valerie Gissot

  • Isabelle Carteau-Martin

  • Robert T. Knight

  • Frederique Bonnet-Brilhault

  • Aurélie Bidet-Caulet

Date: 2015

DOI: 10.3389/fnhum.2015.00519, 2015

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