Individual brain regulation as learned via neurofeedback is related to affective changes in adolescents with autism spectrum disorder

Abstract

Background: Emotions often play a role in neurofeedback (NF) regulation strategies. However, investigations of the relationship between the induced neuronal changes and improvements in affective domains are scarce in electroencephalography-based studies. Thus, we extended the findings of the first study on slow cortical potential (SCP) NF in autism spectrum disorder (ASD) by linking affective changes to whole-brain activity during rest and regulation.

Methods: Forty-one male adolescents with ASD were scanned twice at rest using functional magnetic resonance imaging. Between scans, half underwent NF training, whereas the other half received treatment as usual. Furthermore, parents reported on their child's affective characteristics at each measurement. The NF group had to alternatingly produce negative and positive SCP shifts during training and was additionally scanned using functional magnetic resonance imaging while applying their developed regulation strategies.

Results: No significant treatment group-by-time interactions in affective or resting-state measures were found. However, we found increases of resting activity in the anterior cingulate cortex and right inferior temporal gyrus as well as improvements in affective characteristics over both groups. Activation corresponding to SCP differentiation in these regions correlated with the affective improvements. A further correlation was found for Rolandic operculum activation corresponding to positive SCP shifts. There were no significant correlations with the respective achieved SCP regulation during NF training.

Conclusion: SCP NF in ASD did not lead to superior improvements in neuronal or affective functioning compared to treatment as usual. However, the affective changes might be related to the individual strategies and their corresponding activation patterns as indicated by significant correlations on the whole-brain level. Trial registration This clinical trial was registered at drks.de (DRKS00012339) on 20th April, 2017.

Keywords: Autism spectrum disorder; Emotion regulation; Functional magnetic resonance imaging; Neurofeedback; Slow cortical potentials.

Fig. 1

Results of the resting brain activity and brain regulation task analyses. The increase in the percent amplitude of fluctuations (PerAF) of the anterior cingulate cortex over both, the slow cortical potentials (SCP) neurofeedback and treatment as usual (TAU) group, is visualized in the top-left diagram. The middle-left diagram shows a PerAF increase in the precentral gyrus of the TAU and generally higher values in the SCP group. The bottom-left plot shows the PerAF changes over both groups in the temporal gyrus with stronger increases in the TAU group. The right scatter plots show the correlation of the brain regulation task (Pearson’s r corresponding to the parametric analysis as implemented in Statistical Parametric Mapping and Spearman’s due to potential outliers): The difference between the “Up” and “Down” conditions (i.e., fMRI differentiation) was anticorrelated with changes on the Lability/Negativity (ERC ΔLN) subscale of the Emotion Regulation Checklist. The SCP positivity condition correlated with changes on the Emotion Regulation (ERC ΔER) subscale. Changes on the Griffith Empathy Measure Cognitive Empathy (GEM ΔCE) subscale again significantly correlated with fMRI differentiation. The whole-brain 3D models were created using BrainNet Viewer 1.7 [73]