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      Infant attachment predicts bodily freezing in adolescence: evidence from a prospective longitudinal study

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          Abstract

          Early life-stress, particularly maternal deprivation, is associated with long-lasting deviations in animals’ freezing responses. Given the relevance of freezing for stress-coping, translational research is needed to examine the relation between insecure infant-parent attachment and bodily freezing-like behavior in humans. Therefore, we investigated threat-related reductions in body sway (indicative of freezing-like behavior) in 14-year-old adolescents ( N = 79), for whom attachment security was earlier assessed in infancy. As expected, insecure (vs. secure) attachment was associated with less body sway for angry vs. neutral faces. This effect remained when controlling for intermediate life events. These results suggest that the long-lasting effects of early negative caregiving experiences on the human stress and threat systems extend to the primary defensive reaction of freezing. Additionally, we replicated earlier work in adults, by observing a significant correlation (in adolescents assessed as securely attached) between subjective state anxiety and reduced body sway in response to angry vs. neutral faces. Together, this research opens venues to start exploring the role of freezing in the development of human psychopathology.

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          Most cited references44

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          The face in the crowd revisited: a threat advantage with schematic stimuli.

          Schematic threatening, friendly, and neutral faces were used to test the hypothesis that humans preferentially orient their attention toward threat. Using a visual search paradigm, participants searched for discrepant faces in matrices of otherwise identical faces. Across 5 experiments, results consistently showed faster and more accurate detection of threatening than friendly targets. The threat advantage was obvious regardless of whether the conditions favored parallel or serial search (i.e., involved neutral or emotional distractors), and it was valid for inverted faces. Threatening angry faces were more quickly and accurately detected than were other negative faces (sad or "scheming"), which suggests that the threat advantage can be attributed to threat rather than to the negative valence or the uniqueness of the target display.
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            Neural organization of the defensive behavior system responsible for fear.

            M Fanselow (1994)
            This paper applies the behavior systems approach to fear and defensive behavior, examining the neural circuitry controlling fear and defensive behavior from this vantage point. The defensive behavior system is viewed as having three modes that are activated by different levels of fear. Low levels of fear promote pre-encounter defenses, such as meal-pattern reorganization. Moderate levels of fear activate post-encounter defenses. For the rat, freezing is the dominant post-encounter defensive response. Since this mode of defense is activated by learned fear, forebrain structures such as the amygdala play a critical role in its organization. Projections from the amygdala to the ventral periaqueductal gray activate freezing. Extremely high levels of fear, such as those provoked by physical contact, elicit the vigorous active defenses that compose the circa-strike mode. Midbrain structures such as the dorsolateral periaqueductal gray and the superior colliculus play a crucial role in organizing this mode of defense. Inhibitory interactions between the structures mediating circa-strike and post-encounter defense allow for the rapid switching between defensive modes as the threatening situation varies.
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              Variations in maternal care in infancy regulate the development of stress reactivity.

              Naturally occurring variations in maternal care in early postnatal life are associated with the development of individual differences in behavioral and hypothalamic-pituitary-adrenal responses to stress in the rat. These effects appear to be mediated by the influence of maternal licking/grooming on the development of central systems that serve to activate (corticotropin-releasing factor) or inhibit (gamma-aminobutyric acid) the expression of behavioral and endocrine responses to stress through effects on forebrain noradrenergic systems. Importantly, individual differences in maternal care are transmitted from mother to daughter, providing a mechanism for the behavioral transmission of individual differences in stress reactivity across generations.
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                Author and article information

                Contributors
                Journal
                Front Behav Neurosci
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Media S.A.
                1662-5153
                12 October 2015
                2015
                : 9
                : 263
                Affiliations
                [1] 1Behavioural Science Institute (BSI), Radboud University Netherlands
                [2] 2Donders Institute for Brain, Cognition and Behaviour, Radboud University Netherlands
                [3] 3Faculty of Psychology and Educational Sciences, Open University of the Netherlands Heerlen, Netherlands
                Author notes

                Edited by: Regina Marie Sullivan, The Nathan S. Kline Institute and NYU School of Medicine, USA

                Reviewed by: Christopher Cain, The Nathan S. Kline Institute for Pscyhiatric Research and NYU School of Medicine, USA; C.W.E.M Quaedflieg, Maastricht University, Netherlands

                *Correspondence: Hannah C. M. Niermann, Behavioural Science Institute (BSI) and Donders Institute for Brain, Cognition and Behaviour, Radboud University, Montessorilaan 3, 6525 HR Nijmegen, Netherlands h.niermann@ 123456psych.ru.nl
                Article
                10.3389/fnbeh.2015.00263
                4617177
                26557062
                c4e5047f-47e4-436a-b959-313519028c5f
                Copyright © 2015 Niermann, Ly, Smeekens, Figner, Riksen-Walraven and Roelofs.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 15 July 2015
                : 11 September 2015
                Page count
                Figures: 3, Tables: 1, Equations: 34, References: 67, Pages: 10, Words: 8964
                Funding
                Funded by: Royal Netherlands Academy of Arts and Sciences 10.13039/501100001722
                Award ID: 705AO-2379
                Funded by: Netherlands Organisation for Scientific Research 10.13039/501100003246
                Award ID: 406-13-022
                Award ID: #453-12-001
                Funded by: European Research Council 10.13039/501100000781
                Award ID: ERC_StG2012_313749
                Categories
                Neuroscience
                Original Research

                Neurosciences
                freezing,adolescent,infant,attachment,longitudinal
                Neurosciences
                freezing, adolescent, infant, attachment, longitudinal

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