Gaze-based attention refocusing training in virtual reality for adult attention-deficit/hyperactivity disorder

Abstract

Background: Attention-deficit/hyperactivity disorder (ADHD) is characterized by substantial interindividual heterogeneity that challenges the systematic assessment and treatment. Considering mixed evidence from previous neurofeedback research, we present a novel feedback system that relies on gaze behavior to detect signs of inattention while performing a neuropsychological attention task in a virtual seminar room. More specifically, an audiovisual feedback was given whenever participants averted their gaze from the given task.

Methods: Eighteen adults with ADHD and 18 healthy controls performed a continuous performance task (CPT) in virtual reality under three counterbalanced conditions in which either gaze-based feedback, sham feedback, or no feedback was provided. In all conditions, phases of high and low virtual distraction alternated. CPT errors and reaction times, proportions of gaze dwell times (e.g., task focus or distraction focus), saccade characteristics, EEG theta/beta ratios, head movements, and an experience sampling of ADHD symptoms were analyzed.

Results: While patients can be discriminated well from healthy controls in that they showed more omission errors, higher reaction times, higher distraction-related dwell times, and more head movements, the feedback did not immediately improve task performance. It was also indicated that sham feedback was rather associated with an aggravation of symptoms in patients.

Conclusions: Our findings demonstrate sufficient suitability and specificity for this holistic ADHD symptom assessment. Regarding the feedback, a single-session training was insufficient to achieve learning effects based on the proposed metacognitive strategies. Future longitudinal, multi-session trials should conclusively examine the therapeutic efficacy of gaze-based virtual reality attention training in ADHD.

Trial registration: drks.de (identifier: DRKS00022370).

Keywords: ADHD; Adults; Attention training; Continuous performance task; Distractors; EEG; Eye-tracking; Metacognition; Self-regulation; Therapy; Treatment; Virtual reality.

Fig. 1

The virtual seminar room (VSR) into which the participants immersed via a head-mounted display. A First-person view of the virtual seminar room in which the continuous performance task is presented on the canvas at the front wall. B Real world side view of participant in the virtual reality lab. C One of the distractor events played during a distractor phase: avatar in the front is standing up and walking to a cabinet, thereby attracting the attention of the participant as indicated by the visualized pink gaze vector (not visible for study participants). D Gaze-based feedback provision. Whenever the participant’s gaze shifted away from the canvas for more than 2 s or the gaze was directed at a distractor for at least 0.5 s, audiovisual feedback was automatically played (combined black fade-in and sound effect). For a video presentation of this feedback, see Supplementary Material 1

Fig. 2

Participant flow and experimental design. A 36 participants underwent all three feedback conditions in counterbalanced order on experiment Day 2. First, instructions were shown and a short continuous performance task (CPT) trial block was run. Then, the task block started, combined with either the real feedback, sham feedback, or no feedback. Following each 18-min CPT block, participants underwent experience sampling (ES) and a short break (P). Within each feedback block, time phases with distracting events (DP) and phases without distracting events (NDP) were alternated in three-minute cycles. At the end of the experiment, the VRSQ was completed and a recognition task (RT) regarding presented distractors was conducted. B Distractor phase design. Audio, visual, or audiovisual distractors were presented every 30 s during DP. C Implementation of the CPT. The CPT was presented on a canvas with a stimulus interval of 100 ms and an interstimulus interval of 1100 ms. D Outcome parameters of the study. Abbreviations: ADHD: Attention-deficit/hyperactivity disorder, ES: Experience sampling, D: Distractor, DP: Distractor phase, HC: Healthy control, ISI: Interstimulus interval, NDP: Non-distractor phase, P: Pause, RT: Recognition task, VRSQ: Virtual Reality Sickness Questionnaire

Fig. 3

Results of the continuous performance task (A—C) and gaze behavior analysis (D—G). The number of (A) commission errors, (B) omission errors and (C) mean reaction times are depicted for each feedback condition and both distractor phase types. D A composite distractibility score of the participants’ gaze behavior is depicted. The score reflects the sum of (F) the time spent gazing on distractors and (G) gaze wandering, divided by (E) the amount of time participants were looking onto the canvas on which the continuous performance task was presented. E to G show relative times for each of the three derived gaze parameters. Bars represent feedback conditions and are grouped by patients with ADHD and HC. Error bars indicate the SEM. Abbreviations: ADHD: Attention-deficit/hyperactivity disorder, CPT: Continuous performance task, DP: Distractor phase, HC: Healthy control, NDP: Non-distractor phase

Fig. 4

EEG wavelet analysis. Time–Frequency spectra of the wavelet analysis for (A) patients with ADHD and (B) HC across feedback conditions and phase types at electrode Fz. Dashed squares indicate analyzed time windows of interest (0.5—4.5 s) and frequency ranges of interest (theta [4 -7 Hz], beta [13—30 Hz]). C Comparison of the theta/beta ratio power for each group and between distractor phases and feedback conditions. Error bars indicate the SEM. Abbreviations: ADHD: Attention-deficit/hyperactivity disorder, DP: Distractor phase, HC: Healthy control, NDP: Non-distractor phase

Fig. 5

Exploratory correlation analysis. Correlation matrices including indications of statistical significance based on Benjamini–Hochberg corrected p-values are separately reported for both groups, the ADHD group (left of and below the diagonal) and HC (right of and above the diagonal). Correlations were calculated separately for the (A) real feedback, (B) sham feedback and (C) no feedback condition. Accordingly, correlations with the number of triggered feedback are not presented for the latter condition. The color coding of the strength of the Pearson correlations is shown on the right. Higher contrasts and greater circle seizes indicate stronger correlations. Abbreviations: Canvas ATT: Time of task focus indicated by attended canvas dwell times, CE: Commission errors, CPT: Continuous performance task, Distractor ATT: Attended distractors percentage dwell times, Distr. Score: Distractibility score, ES ADHD-SYM: Experience sampling self-rated ADHD symptoms, Head MOV: Head movements, IDA-R SYM: ADHD symptoms observer-rated via the IDA-R, No. feedbacks: Total number of feedback triggered, No. saccades: Total number of saccades, OE: Omission errors, RT: Reaction times, Saccade DUR: Average saccade durations, SB: ADHD symptoms self-rated via the ADHS-SB. *p < .05, **p < .01, ***p < .001