Evaluating the Modulation of the Acoustic Startle Reflex in Children and Adolescents via Vertical EOG and EEG: Sex, Age, and Behavioral Effects

Anastasios E Giannopoulos; Ioanna Zioga; Panos Papageorgiou; Panagiota Pervanidou; Gerasimos Makris; George P Chrousos; Xanthi Stachtea; Christos Capsalis; Charalabos Papageorgiou

doi:10.3389/fnins.2022.798667

Evaluating the Modulation of the Acoustic Startle Reflex in Children and Adolescents via Vertical EOG and EEG: Sex, Age, and Behavioral Effects

Front Neurosci. 2022 Apr 6:16:798667. doi: 10.3389/fnins.2022.798667. eCollection 2022.

Authors

Anastasios E Giannopoulos¹, Ioanna Zioga^{2

3}, Panos Papageorgiou⁴, Panagiota Pervanidou⁵, Gerasimos Makris⁵, George P Chrousos⁵, Xanthi Stachtea⁶, Christos Capsalis¹, Charalabos Papageorgiou⁶

Affiliations

¹ School of Electrical and Computer Engineering, National Technical University of Athens, Athens, Greece.
² Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, Netherlands.
³ First Department of Psychiatry, Eginition Hospital, National and Kapodistrian University of Athens Medical School, Athens, Greece.
⁴ Department of Electrical and Computer Engineering, University of Patras, Patras, Greece.
⁵ Unit of Developmental and Behavioral Pediatrics, First Department of Pediatrics, School of Medicine, "Aghia Sophia" Children's Hospital, National and Kapodistrian University of Athens, Athens, Greece.
⁶ Neurosciences and Precision Medicine Research Institute "COSTAS STEFANIS" (UMHRI), University Mental Health, Athens, Greece.

Abstract

Acoustic startle reflex (ASR) constitutes a reliable, cross-species indicator of sensorimotor and inhibitory mechanisms, showing distinct signature in cognitive aging, sex, and psychopathological characterization. ASR can be modulated by the prepulse inhibition (PPI) paradigm, which comprises the suppression of reactivity to a startling stimulus (pulse) following a weak prepulse (30- to 500-ms time difference), being widely linked to inhibitory capabilities of the sensorimotor system. If the prepulse-pulse tones are more clearly separated (500-2,000 ms), ASR amplitude is enhanced, termed as prepulse facilitation (PPF), reflecting sustained or selective attention. Our study aimed to investigate early-life sensorimotor sex/age differences using Electroencephalographic recordings to measure muscular and neural ASR in a healthy young population. Sixty-three children and adolescents aged 6.2-16.7 years (31 females) took part in the experiment. Neural ASR was assessed by two different analyses, namely, event-related potentials (ERPs) and first-derivative potentials (FDPs). As expected, PPF showed enhanced responses compared with PPI, as indicated by eyeblink, ERP and FDP measures, confirming the gating effect hypothesis. Sex-related differences were reflected in FDPs, with females showing higher ASR than males, suggesting increased levels of poststartle excitability. Intragroup age effects were evaluated via multipredictor regression models, noticing positive correlation between age versus eyeblink and ERP responses. Attention-related ERPs (N100 and P200) showed distinct patterns in PPI versus PPF, potentially indicative for alternative attentional allocation and block-out of sensory overload. Screening measures of participants' neurodevelopmental (assessed by Wechsler Intelligence Scale for Children) and behavioral (assessed by Child Behavior Checklist) markers were also associated with increased N100/P200 responses, presumably indexing synergy between perceptual consistency, personality profiling, and inhibitory performance. Conclusively, modulation of ASR by PPI and PPF is associated with biological sex and internal/external personality traits in childhood and adolescence, potentially useful to guide symptomatology and prevention of psychopathology.

Keywords: EEG; acoustic startle reflex; first-derivative potential; prepulse facilitation; prepulse inhibition; sensorimotor gating.