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Early maternal care and amygdala habituation to emotional stimuli in adulthood.

ABSTRACT: Evidence suggests that maternal care constitutes a protective factor for psychopathology which may be conditional on the level of family adversity. Given that psychopathology is frequently linked with social deficits and the amygdala with social functioning, we investigated the impact of early maternal care on amygdala function under high vs low familial risk for psychopathology. Amygdala activity and habituation during an emotional face-matching paradigm was analyzed in participants of an epidemiological cohort study followed since birth (n = 172, 25 years). Early mother-infant interaction was assessed during a standardized nursing and play setting at the age of 3 months. Information on familial risk during the offspring's childhood and on the participants' lifetime psychopathology was obtained with diagnostic interviews. An interaction between maternal stimulation and familial risk was found on amygdala habituation but not on activation, with higher maternal stimulation predicting stronger amygdala habituation in the familial risk group only. Furthermore, amygdala habituation correlated inversely with Attention Deficit Hyperactivity Disorder (ADHD) diagnoses. The findings underline the long-term importance of early maternal care on the offspring's socioemotional neurodevelopment and of interventions targeting maternal sensitivity early in life, particularly by increasing maternal interactive behavior in those with familial risk.

SUBMITTER: Holz NE

PROVIDER: S-EPMC8483279 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Early maternal care and amygdala habituation to emotional stimuli in adulthood.

Holz Nathalie E NE Häge Alexander A Plichta Michael M MM Boecker-Schlier Regina R Jennen-Steinmetz Christine C Baumeister Sarah S Meyer-Lindenberg Andreas A Laucht Manfred M Banaschewski Tobias T Brandeis Daniel D

Social cognitive and affective neuroscience 20210901 10

Evidence suggests that maternal care constitutes a protective factor for psychopathology which may be conditional on the level of family adversity. Given that psychopathology is frequently linked with social deficits and the amygdala with social functioning, we investigated the impact of early maternal care on amygdala function under high vs low familial risk for psychopathology. Amygdala activity and habituation during an emotional face-matching paradigm was analyzed in participants of an epide ...[more]

PMID: 33963390

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Project description:Over the past two decades, evidence has accumulated that the human amygdala exerts some of its functions also when the observer is not aware of the content, or even presence, of the triggering emotional stimulus. Nevertheless, there is as of yet no consensus on the limits and conditions that affect the extent of amygdala's response without focused attention or awareness. Here we review past and recent studies on this subject, examining neuroimaging literature on healthy participants as well as brain-damaged patients, and we comment on their strengths and limits. We propose a theoretical distinction between processes involved in attentional unawareness, wherein the stimulus is potentially accessible to enter visual awareness but fails to do so because attention is diverted, and in sensory unawareness, wherein the stimulus fails to enter awareness because its normal processing in the visual cortex is suppressed. We argue this distinction, along with data sampling amygdala responses with high temporal resolution, helps to appreciate the multiplicity of functional and anatomical mechanisms centered on the amygdala and supporting its role in non-conscious emotion processing. Separate, but interacting, networks relay visual information to the amygdala exploiting different computational properties of subcortical and cortical routes, thereby supporting amygdala functions at different stages of emotion processing. This view reconciles some apparent contradictions in the literature, as well as seemingly contrasting proposals, such as the dual stage and the dual route model. We conclude that evidence in favor of the amygdala response without awareness is solid, albeit this response originates from different functional mechanisms and is driven by more complex neural networks than commonly assumed. Acknowledging the complexity of such mechanisms can foster new insights on the varieties of amygdala functions without awareness and their impact on human behavior.

Project description:ObjectiveBorderline personality disorder is the prototypical disorder of emotion reactivity and dysregulation, yet there remains limited understanding of its neurocognitive correlates. Two mechanisms that may underlie anomalous reactivity in response to negative stimuli among patients with borderline personality disorder are impairment in habituation and exaggerated sensitization of activity in the neural salience network, including the amygdala, anterior insula, and dorsal anterior cingulate cortex. The authors aimed to reveal the most plausible mechanism by examining the effect of repeated exposure to emotional images both within and across study sessions.MethodA total of 75 participants (patients with borderline personality disorder, N=26; patients with avoidant personality disorder included as a psychopathological control group, N=25; and healthy control subjects, N=24) were included in the study analyses. All participants viewed five presentations of the same set of negative and neutral images at each of two sessions, separated by approximately 3 days, while functional MRI data were acquired. Salience network activity, as measured by blood-oxygen-level-dependent signal in anatomically defined regions of interest across the salience network, was compared across the three groups for each presentation at each of the two study sessions. Self-reported negative affect was measured for each trial.ResultsSalience network activity showed a main effect of within-session habituation across all groups and sessions. However, a group-by-session interaction was present, such that only patients with borderline personality disorder showed increased salience network activity in response to the images reencountered at the second session, and this increased salience network sensitization predicted greater sensitization in self-reported negative affect.ConclusionsThese results elucidate the neural mechanisms by which patients with borderline personality disorder appraise negative social situations as exaggeratedly salient and suggest potential neurocognitive intervention targets.

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Early maternal care and amygdala habituation to emotional stimuli in adulthood.

Publications

Early maternal care and amygdala habituation to emotional stimuli in adulthood.

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