Across ages and places: Unpredictability of maternal sensory signals and child internalizing behaviors

Özlü Aran; Danielle A Swales; Natasha A Bailey; Riikka Korja; Eeva Holmberg; Eeva Eskola; Saara Nolvi; Laura Perasto; Elisabeth Nordenswan; Hasse Karlsson; Linnea Karlsson; Curt A Sandman; Hal S Stern; Tallie Z Baram; Laura M Glynn; Elysia Poggi Davis

doi:10.1016/j.jad.2023.11.068

Across ages and places: Unpredictability of maternal sensory signals and child internalizing behaviors

J Affect Disord. 2024 Feb 15:347:557-567. doi: 10.1016/j.jad.2023.11.068. Epub 2023 Nov 23.

Authors

Özlü Aran¹, Danielle A Swales², Natasha A Bailey³, Riikka Korja⁴, Eeva Holmberg⁵, Eeva Eskola⁵, Saara Nolvi⁵, Laura Perasto⁶, Elisabeth Nordenswan⁵, Hasse Karlsson⁷, Linnea Karlsson⁸, Curt A Sandman⁹, Hal S Stern¹⁰, Tallie Z Baram¹¹, Laura M Glynn¹², Elysia Poggi Davis¹³

Affiliations

¹ Department of Psychology, University of Denver, Denver, CO, USA. Electronic address: ozlu.aran@du.edu.
² Department of Psychiatry, University of North Carolina at Chapel Hill, NC, USA. Electronic address: danielle_swales@med.unc.edu.
³ Department of Psychology, University of Virginia, Charlottesville, VA, USA.
⁴ University of Turku, Department of Psychology and Speech-Language Pathology, Turku, Finland; University of Turku, Department of Clinical Medicine, Turku Brain and Mind Center, FinnBrain Birth Cohort Study, Turku, Finland; Centre of Excellence in Learning Dynamics and Intervention Research (InterLearn), University of Turku, Turku, Finland.
⁵ University of Turku, Department of Psychology and Speech-Language Pathology, Turku, Finland; University of Turku, Department of Clinical Medicine, Turku Brain and Mind Center, FinnBrain Birth Cohort Study, Turku, Finland.
⁶ University of Turku, Department of Clinical Medicine, Turku Brain and Mind Center, FinnBrain Birth Cohort Study, Turku, Finland; Centre for Population Health Research, University of Turku and Turku University Hospital, Turku, Finland.
⁷ University of Turku, Department of Clinical Medicine, Turku Brain and Mind Center, FinnBrain Birth Cohort Study, Turku, Finland; Centre for Population Health Research, University of Turku and Turku University Hospital, Turku, Finland; Department of Psychiatry, Turku University Hospital and University of Turku, Turku, Finland.
⁸ University of Turku, Department of Clinical Medicine, Turku Brain and Mind Center, FinnBrain Birth Cohort Study, Turku, Finland; Centre of Excellence in Learning Dynamics and Intervention Research (InterLearn), University of Turku, Turku, Finland; Department of Clinical Medicine, Paediatrics and Adolescent Medicine, Turku University Hospital and University of Turku.
⁹ Department of Psychiatry and Human Behavior, University of California-Irvine, Irvine, CA, USA.
¹⁰ Department of Statistics, University of California-Irvine, Irvine, CA, USA.
¹¹ Department of Pediatrics, University of California-Irvine, Irvine, CA, USA; Department of Anatomy/Neurobiology, University of California-Irvine, Irvine, CA, USA; Department of Neurology, University of California-Irvine, Irvine, CA, USA.
¹² Department of Psychology, Chapman University, Orange, CA, USA.
¹³ Department of Psychology, University of Denver, Denver, CO, USA; Department of Pediatrics, University of California-Irvine, Irvine, CA, USA.

PMID: 38007106
PMCID: PMC10843791 (available on 2025-02-15)
DOI: 10.1016/j.jad.2023.11.068

Abstract

Background: Patterns of sensory inputs early in life play an integral role in shaping the maturation of neural circuits, including those implicated in emotion and cognition. In both experimental animal models and observational human research, unpredictable sensory signals have been linked to aberrant developmental outcomes, including poor memory and effortful control. These findings suggest that sensitivity to unpredictable sensory signals is conserved across species and sculpts the developing brain. The current study provides a novel investigation of unpredictable maternal sensory signals in early life and child internalizing behaviors. We tested these associations in three independent cohorts to probe the generalizability of associations across continents and cultures.

Method: The three prospective longitudinal cohorts were based in Orange, USA (n = 163, 47.2 % female, M_age = 1 year); Turku, Finland (n = 239, 44.8 % female, M_age = 5 years); and Irvine, USA (n = 129, 43.4 % female, M_age = 9.6 years). Unpredictability of maternal sensory signals was quantified during free-play interactions. Child internalizing behaviors were measured via parent report (Orange & Turku) and child self-report (Irvine).

Results: Early life exposure to unpredictable maternal sensory signals was associated with greater child fearfulness/anxiety in all three cohorts, above and beyond maternal sensitivity and sociodemographic factors. The association between unpredictable maternal sensory signals and child sadness/depression was relatively weaker and did not reach traditional thresholds for statistical significance.

Limitations: The correlational design limits our ability to make causal inferences.

Conclusions: Findings across the three diverse cohorts suggest that unpredictable maternal signals early in life shape the development of internalizing behaviors, particularly fearfulness and anxiety.

Keywords: Anxiety; Depression; Early-life stress; Internalizing behaviors; Maternal care; Unpredictability.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Animals
Anxiety*
Child
Child, Preschool
Emotions*
Female
Humans
Infant
Male
Maternal Behavior / psychology
Mothers / psychology
Prospective Studies

Abstract

Publication types

MeSH terms

Grants and funding