Unpredictable maternal behavior is associated with a blunted infant cortisol response

Noroña-Zhou, Amanda; Morgan, Alyssa; Glynn, Laura M.; Sandman, Curt A.; Baram, Tallie Z.; Davis, Elysia Poggi

doi:10.1002/dev.21964

Cited by 28 publications

(33 citation statements)

References 49 publications

(65 reference statements)

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“…Discrepancies may be because of differences in the type of adversity and developmental stage at assessment, and none of these prior studies evaluated unpredictability. We focus on unpredictability as a type of early adversity that has been associated with long-term consequences for development (Glynn et al, 2018Howland et al, 2020;Noraña-Zhou et al, 2020). Patterns of sensory signals are known to shape the development of neural circuits involved in sensory systems, and we show that circuits involved in cognitive functions also may be affected.…”

Section: Discussionmentioning

confidence: 98%

“…Although it is clear that the quality of maternal care affects the risk for offspring psychological disorders and neurobiological changes later in life (Bowlby, 1950;Lebel et al, 2016;, less is known about how patterns of maternal behavior impact human development (Baram et al, 2012;Davis et al, 2017). Recent work has indicated that unpredictable patterns of maternal sensory signals during infancy are a novel contributor to impaired cognitive and emotional functions later in life (Chen and Baram, 2016;Molet et al, 2016b;Walker et al, 2017;Noraña-Zhou et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Aberrant Maturation of the Uncinate Fasciculus Follows Exposure to Unpredictable Patterns of Maternal Signals

et al. 2020

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Across species, unpredictable patterns of maternal behavior are emerging as novel predictors of aberrant cognitive and emotional outcomes later in life. In animal models, exposure to unpredictable patterns of maternal behavior alters brain circuit maturation and cognitive and emotional outcomes. However, whether exposure to such signals in humans alters the development of brain pathways is unknown. In mother-child dyads, we tested the hypothesis that exposure to more unpredictable maternal signals in infancy is associated with aberrant maturation of corticolimbic pathways. We focused on the uncinate fasciculus, the primary fiber bundle connecting the amygdala to the orbitofrontal cortex and a key component of the medial temporal lobe-prefrontal cortex circuit. Infant exposure to unpredictable maternal sensory signals was assessed at 6 and 12 months. Using high angular resolution diffusion imaging, we quantified the integrity of the uncinate fasciculus using generalized fractional anisotropy (GFA). Higher maternal unpredictability during infancy presaged greater uncinate fasciculus GFA in children 9-11 years of age (n = 69, 29 female). In contrast to the uncinate, GFA of a second corticolimbic projection, the hippocampal cingulum, was not associated with maternal unpredictability. Addressing the overall functional significance of the uncinate and cingulum relationships, we found that the resulting imbalance of medial temporal lobe-prefrontal cortex connectivity partially mediated the association between unpredictable maternal sensory signals and impaired episodic memory function. These results suggest that unbalanced maturation of corticolimbic circuits is a mechanism by which early unpredictable sensory signals may impact cognition later in life. Significance StatementOur prior work across species demonstrated that unpredictable patterns of maternal care are associated with compromised memory function. However, the neurobiological mechanisms by which this occurs in humans remain unknown. Here, we identify an association of exposure to unpredictable patterns of maternal sensory signals with the integrity of corticolimbic circuits involved in emotion and cognition using state-of-the-art diffusion imaging techniques and analyses. We find that exposure to early unpredictability is associated with higher integrity of the uncinate fasciculus with no effect on a second corticolimbic pathway, the cingulum. The resulting imbalance of corticolimbic circuit development is a novel mediator of the association between unpredictable patterns of maternal care and poorer episodic memory.

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Section: Discussionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Aberrant Maturation of the Uncinate Fasciculus Follows Exposure to Unpredictable Patterns of Maternal Signals

et al. 2020

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“…Adding this dimension would not only be consistent with the work of Dickerson and Kemeny (2004), but also of the work of Baram et al (2012) who have shown that fragmented and unpredictable stimulation during early development impairs cognitive development and increases the risk of mental disorders in rodent models and in humans. Recently this group has also shown that fragmented/unpredictable maternal behavior in infancy predicts a blunted cortisol response to pain stressors in the baby (Norona-Zhou et al, 2020).…”

Section: The Nature Of the Stimulusmentioning

confidence: 99%

Early adversity, stress, and neurobehavioral development

Gunnar

2020

Dev Psychopathol

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“…This, in turn, has been found to associate with decreased memory functions and anhedonia in pups (Brunson et al, 2005;Ivy et al, 2008;Rice et al, 2008;Molet et al, 2016). Recently, in humans, unpredictable maternal caregiving signals were found to be associated with decreased child cognitive functioning (Davis et al, 2017), child poorer effortful control (Davis et al, 2019) and infant's blunted cortisol response (Noroña-zhou et al, 2020). To date, little research exists, how maternal anxiety and depressive symptoms and maternal characteristics relate to the unpredictable care.…”

Section: Introductionmentioning

confidence: 99%

Maternal Anxiety Symptoms and Self-Regulation Capacity Are Associated With the Unpredictability of Maternal Sensory Signals in Caregiving Behavior

et al. 2020

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The unpredictability of maternal sensory signals in caregiving behavior has been recently found to be linked with infant neurodevelopment. The research area is new, and very little is yet known, how maternal anxiety and depressive symptoms and specific parental characteristics relate to the unpredictable maternal care. The aims of the current study were to explore how pre- and postnatal maternal anxiety and depressive symptoms and self-regulation capacity associate with the unpredictability of maternal sensory signals. The study population consisted of 177 mother-infant dyads. The unpredictability of the maternal sensory signals was explored from the video-recorded mother-infant free play situation when the infant was 8 months of age. Pre- and postnatal anxiety and depressive symptoms were measured by questionnaires prenatally at gwks 14, 24, 34, and 3 and 6 months postpartum. Maternal self-regulation capacity, a trait considered to be stable in adulthood, was assessed using adult temperament questionnaire when the infant was 12 months of age. We found that elevated prenatal maternal anxiety symptoms associated with higher unpredictability in the maternal care while depressive symptoms were unrelated to the unpredictability of maternal care. Moreover, the association was moderated by maternal self-regulation capacity, as higher anxiety symptoms during pre-and postnatal period were associated more unpredictability among the mothers with low self-regulation capacity. The combination of higher amount of maternal anxiety symptoms and lower self-regulation capacity seems to constitute specific risk for the unpredictable maternal care.

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Unpredictable maternal behavior is associated with a blunted infant cortisol response

Cited by 28 publications

References 49 publications

Aberrant Maturation of the Uncinate Fasciculus Follows Exposure to Unpredictable Patterns of Maternal Signals

Aberrant Maturation of the Uncinate Fasciculus Follows Exposure to Unpredictable Patterns of Maternal Signals

Early adversity, stress, and neurobehavioral development

Maternal Anxiety Symptoms and Self-Regulation Capacity Are Associated With the Unpredictability of Maternal Sensory Signals in Caregiving Behavior

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