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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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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Dynamics of anticipatory mechanisms during predictive context processing

Authors:

• Aurélie Bidet-Caulet

• P. G. Barbe

• S. Roux

• H. Viswanath

• C. Barthelemy

• N. Bruneau

• Robert T. Knight

• Frederique Bonnet-Brilhault

Date: 2012

DOI: 10.1111/j.1460-9568.2012.08223.x

PubMed: 22780698

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Abstract:

We employed an electroencephalography paradigm manipulating predictive context to dissociate the neural dynamics of anticipatory mechanisms. Subjects either detected random targets or targets preceded by a predictive sequence of three distinct stimuli. The last stimulus in the three-stimulus sequence (decisive stimulus) did not require any motor response but 100% predicted a subsequent target event. We showed that predictive context optimises target processing via the deployment of distinct anticipatory mechanisms at different times of the predictive sequence. Prior to the occurrence of the decisive stimulus, enhanced attentional preparation was manifested by reductions in the alpha oscillatory activities over the visual cortices, resulting in facilitation of processing of the decisive stimulus. Conversely, the subsequent 100% predictable target event did not reveal the deployment of attentional preparation in the visual cortices, but elicited enhanced motor preparation mechanisms, indexed by an increased contingent negative variation and reduced mu oscillatory activities over the motor cortices before movement onset. The present results provide evidence that anticipation operates via different attentional and motor preparation mechanisms by selectively pre-activating task-dependent brain areas as the predictability gradually increases.