Motor synchronization and impulsivity in pediatric borderline personality disorder with and without attention-deficit hyperactivity disorder: an eye-tracking study of saccade, blink and pupil behavior

Abstract

Shifting motor actions from reflexively reacting to an environmental stimulus to predicting it allows for smooth synchronization of behavior with the outside world. This shift relies on the identification of patterns within the stimulus – knowing when a stimulus is predictable and when it is not – and launching motor actions accordingly. Failure to identify predictable stimuli results in movement delays whereas failure to recognize unpredictable stimuli results in early movements with incomplete information that can result in errors. Here we used a metronome task, combined with video-based eye-tracking, to quantify temporal predictive learning and performance to regularly paced visual targets at 5 different interstimulus intervals (ISIs). We compared these results to the random task where the timing of the target was randomized at each target step. We completed these tasks in female pediatric psychiatry patients (age range: 11–18 years) with borderline personality disorder (BPD) symptoms, with (n = 22) and without (n = 23) a comorbid attention-deficit hyperactivity disorder (ADHD) diagnosis, against controls (n = 35). Compared to controls, BPD and ADHD/BPD cohorts showed no differences in their predictive saccade performance to metronome targets, however, when targets were random ADHD/BPD participants made significantly more anticipatory saccades (i.e., guesses of target arrival). The ADHD/BPD group also significantly increased their blink rate and pupil size when initiating movements to predictable versus unpredictable targets, likely a reflection of increased neural effort for motor synchronization. BPD and ADHD/BPD groups showed increased sympathetic tone evidenced by larger pupil sizes than controls. Together, these results support normal temporal motor prediction in BPD with and without ADHD, reduced response inhibition in BPD with comorbid ADHD, and increased pupil sizes in BPD patients. Further these results emphasize the importance of controlling for comorbid ADHD when querying BPD pathology.

Attentional Modulation of Eye Blinking Is Altered by Sex, Age, and Task Structure

“…So far, our lab has used the tasks described in this paper to differentiate saccade and pupil dynamics in multiple neurodegenerative and psychiatric cohorts ( Wang et al, 2016 ; Perkins et al, 2021 ; Habibi et al, 2022 ; Riek et al, 2023 ), making blinks an obvious next candidate for use in detecting clinically relevant deficits in cognitive pathways, especially given the findings described here. Alterations in blink behavior have already been observed in many neurological conditions ( Karson et al, 1984 ; Basso et al, 1996 ) but would benefit from the more temporally sensitive, probabilistic approaches to blink analysis implemented in this study to expose the higher-level mechanisms underlying the behavior ( Brien et al, 2023 ; Calancie et al, 2023 ).…”

“…Task structure, modality, and complexity all influence the timing and frequency of blinks, complicating our understanding of underlying processes (review by Stern et al, 1984 ). In tasks with discrete trial structure, blinks mark the start and end of a period of stimulus processing and/or response execution ( Siegle et al, 2008 ; Wascher et al, 2015 ; Calancie et al, 2022 , 2023 ). Here we used an interleaved pro-/anti-saccade task (IPAST) to assess blink timing within a discretely structured task with low perceptual load and varying cognitive difficulty.…”