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

doi:10.1016/j.jad.2023.11.068

. 2024 Feb 15:347:557-567.

doi: 10.1016/j.jad.2023.11.068. Epub 2023 Nov 23.

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

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
DOI: 10.1016/j.jad.2023.11.068

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

Özlü Aran et al. J Affect Disord. 2024.

. 2024 Feb 15:347:557-567.

doi: 10.1016/j.jad.2023.11.068. Epub 2023 Nov 23.

Authors

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
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.

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Conflict of interest statement

Declaration of competing interest No conflicts of interests were reported by the authors.

Figures

**Figure 1.. Study Overview and Timeline for Data Collection**
*Notes.* Mother-child free play interactions were coded for maternal unpredictable sensory signals and maternal sensitivity.

**Figure 2.. Unpredictable Maternal Sensory Signals (Entropy Rate) and Child Fearfulness/Anxiety**

**Figure 3.. Associations Between Unpredictable Maternal Sensory Signals (Entropy Rate) and Child Internalizing Behaviors Across Cohorts (effect sizes and confidence intervals are shown).**
*Notes*. *p < .05. Standardized beta coefficients indicating the relation between unpredictable maternal sensory signals and child internalizing outcomes are graphed with 95% confidence intervals.

See this image and copyright information in PMC

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References

1. Achenbach TM (1978). The Child Behavior Profile: I. Boys aged 6–11. Journal of Consulting and Clinical Psychology, 46, 478–488. 10.1037/0022-006X.46.3.478 - DOI - PubMed
1. Achenbach TM, & Rescorla L (2001). Manual for the ASEBA school-age forms and profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families.
1. Ainsworth MDS, Blehar MC, Waters E, & Wall SN (1978). Patterns of Attachment: A Psychological Study of the Strange Situation. Earlbaum. 10.4324/9780203758045 - DOI
1. Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A, & Stern H (2012). Fragmentation and Unpredictability of Early-Life Experience in Mental Disorders. American Journal of Psychiatry, 169(9), 907–915. 10.1176/appi.ajp.2012.11091347 - DOI - PMC - PubMed
1. Biringen Z, Moorlag A, Meyer B, Wood J, Aberle J, Altenhofen S, & Bennett S (2008). The Emotional Availability (EA) intervention with child care professionals. Journal of Early Childhood and Infant Psychology, 4, 39–52.

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[1] Achenbach TM (1978). The Child Behavior Profile: I. Boys aged 6–11. Journal of Consulting and Clinical Psychology, 46, 478–488. 10.1037/0022-006X.46.3.478 - DOI - PubMed

[2] Achenbach TM (1978). The Child Behavior Profile: I. Boys aged 6–11. Journal of Consulting and Clinical Psychology, 46, 478–488. 10.1037/0022-006X.46.3.478 - DOI - PubMed

[3] Achenbach TM, & Rescorla L (2001). Manual for the ASEBA school-age forms and profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families.

[4] Achenbach TM, & Rescorla L (2001). Manual for the ASEBA school-age forms and profiles. Burlington, VT: University of Vermont, Research Center for Children, Youth, and Families.

[5] Ainsworth MDS, Blehar MC, Waters E, & Wall SN (1978). Patterns of Attachment: A Psychological Study of the Strange Situation. Earlbaum. 10.4324/9780203758045 - DOI

[6] Ainsworth MDS, Blehar MC, Waters E, & Wall SN (1978). Patterns of Attachment: A Psychological Study of the Strange Situation. Earlbaum. 10.4324/9780203758045 - DOI

[7] Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A, & Stern H (2012). Fragmentation and Unpredictability of Early-Life Experience in Mental Disorders. American Journal of Psychiatry, 169(9), 907–915. 10.1176/appi.ajp.2012.11091347 - DOI - PMC - PubMed

[8] Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A, & Stern H (2012). Fragmentation and Unpredictability of Early-Life Experience in Mental Disorders. American Journal of Psychiatry, 169(9), 907–915. 10.1176/appi.ajp.2012.11091347 - DOI - PMC - PubMed

[9] Biringen Z, Moorlag A, Meyer B, Wood J, Aberle J, Altenhofen S, & Bennett S (2008). The Emotional Availability (EA) intervention with child care professionals. Journal of Early Childhood and Infant Psychology, 4, 39–52.

[10] Biringen Z, Moorlag A, Meyer B, Wood J, Aberle J, Altenhofen S, & Bennett S (2008). The Emotional Availability (EA) intervention with child care professionals. Journal of Early Childhood and Infant Psychology, 4, 39–52.

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

Affiliations

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

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