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

Olivia G Calancie; Ashley C Parr; Don C Brien; Jeff Huang; Isabell C Pitigoi; Brian C Coe; Linda Booij; Sarosh Khalid-Khan; Douglas P Munoz

doi:10.3389/fnins.2023.1179765

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

Front Neurosci. 2023 Jun 22:17:1179765. doi: 10.3389/fnins.2023.1179765. eCollection 2023.

Authors

Affiliations

¹ Queen's Eye Movement Lab, Centre for Neuroscience Studies, Queen's University, Kingston, ON, Canada.
² Department of Psychiatry, University of Pittsburgh, Pittsburgh, PA, United States.
³ Department of Psychiatry, McGill University, Montreal, QC, Canada.
⁴ Research Centre and Eating Disorders Continuum, Douglas Mental Health University Institute, Montreal, QC, Canada.
⁵ Divison of Child and Youth Psychiatry, Department of Psychiatry, School of Medicine, Queen's University, Kingston, ON, Canada.

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.

Keywords: arousal; eye movement; metronome; predict saccade; psychiatric disease; psychotropic medication; response inhibition.