Neonatal brainstem dysfunction after preterm birth predicts behavioral inhibition

Abstract

Background: Behavioral inhibition (BI), the tendency to withdraw or exhibit negative affect when experiencing stressful situations, is a major risk factor for the development of social anxiety. However, neonatal biologic origins of this progression are still unknown. Click here to enter text.This study aimed to extend frameworks of behavioral inhibition by exploring empirically the central role of neonatal brainstem electrophysiologic functions in the development of social disengagement and BI. Methods: Sixty-six preterm neonates (means AESD: gestation age = 33.1 AE 1.22 weeks, birth weight = 1775 + 346.7 g; 51% female) participated in a prospective longitudinal study. The infants were tested within the first 2 weeks of postnatal life using an auditory brainstem-evoked response test. Based on the typicality of the major ABR wave latencies, waves I, III and V, neonates were divided into two groups (compromised, CBSF-with at least one component ≥1.5 SDs from the mean for the respective gestation age; normal, NBSF, with all components within 1.5 SD around the mean), and were enrolled in a prospective longitudinal follow-up study. This report extends previous work from 4 m by testing responses to socioemotional challenges during the Separation-Reunion paradigm at 12 m. Results: Results show that infants with neonatal CBSF were more susceptible to be classified as BI at 12 m (age corrected for prematurity) than infants with NBSF (66% vs. 40%, respectively). The most striking symptom in the CBSF group was a disability to initiate self-regulatory activities in response to a socioemotional challenge, resulting in frequent passivity/dependency (p < .001). Statistical regression analysis revealed that face-to-face gaze engagement at 4 m moderates the risk related to neonatal CBSF for the emergence of BI at 12 m, but did not overturn the emergence of BI. Conclusion: Results support the hypothesis that neonatal brainstem dysfunction canalizes behavioral inhibition. These findings highlight, for the first time, the role of the early developing brainstem in later development of BI and in abilities to initiate self-regulatory behavior.

Increases in Arousal are More Long‐Lasting than Decreases in Arousal: On Homeostatic Failures During Emotion Regulation in Infancy

“…In future, it will be interesting to investigate this question in more detail in order to ascertain whether there is an optimum level between over‐ and understimulation (cf Gardner & Karmel, ; Kidd, Piantadosi, & Aslin, ) and how this differs between individuals. This may relate to previous research that has investigated early individual differences in infants’ preferences for high and low external stimulation from both a state (Gardner & Karmel, ; Geva, Gardner, & Karmel, ) and trait (Cohen et al., ; Gardner, Karmel, Magnano, Norton, & Brown, ; Gardner et al., ; Geva, Schreiber, Segal‐Caspi, & Markys‐Shiffman, ) perspective.…”

Auditory brainstem maturation in normal‐hearing infants born preterm: a meta‐analysis

“…The few studies measuring ABR in children born preterm at later ages -1 to 8 yearsconcluded that there is no significant difference with term-born children at those ages. 37 They used ABR measurement to determine whether an infant had normal or compromised brainstem function, and concluded that compromised brainstem function canalized behavioural inhibition in children born preterm at 12 months of age. Exposure to the extra-uterine environment in the third trimester of pregnancy slows down the myelination process, which is responsible for rapid synchronized conduction along the nerve.…”

Brainstem as a developmental gateway to social attention

“…Brainstem input mediates early social behavior. This is evident by its effects on gaze engagement (Geva et al., ), affective responses (Shinya, Kawai, Niwa, & Myowa‐Yamakoshi, ), vagal tone regulation (Porges, Doussard‐Roosevelt, Portales, & Greenspan, ), and initiation of social responses at infancy (Geva, Schreiber, Segal‐Caspi, & Markus‐Shiffman, ).…”

“…Brainstem connectivity to the limbic circuit supports emotional signaling and affect sharing (Porges, ; Prechtl, ; Tucker et al., ), social gaze engagement (Geva et al., ), and initiation of social regulation strategies (Geva et al., ). These relations suggest a potential role for brainstem‐related pathways, which mature at late term age, in setting a time‐sensitive window for later maturing limbic‐cortical neural networks that enable social attention (Doesburg et al., ; Geva & Feldman, ).…”

“…At 4 months, children with compromised brainstem function are more prone to avert their gaze when facing a social agent (Geva et al., ). Also, at 12 months, brainstem dysfunction increased the risk for behavioral inhibition, characterized by shyness and passivity (Geva et al., ). We anticipated traces of this phenotype at 8 years of age, expecting social gaze aversion in a triadic gaze engagement task (TGE), alerting deficits in the attention network task (ANT), lack of frontal alpha asymmetry, and theta power differences on EEG in children with neonatal brainstem dysfunctions.…”