A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect

Previous research findings have linked caregiver deprivation and emotional neglect with sensitivity to threatening cues. The present preliminary study investigated whether dysfunctions of the medial temporal lobe could underlie these associations. Using fMRI, we measured medial temporal lobe responses to emotional faces (angry, fearful, happy, neutral) among 30 youths. Eleven of the youths had a history of caregiver deprivation and emotional neglect. Attention states (i.e., attention to anger, fear, or physical attributes, or passive viewing) were systematically manipulated. Relative to comparison youths, youths with a history of caregiver deprivation and emotional neglect showed significantly greater left amygdala and left anterior hippocampus activation during the processing of threatening information. To our knowledge, these findings are the first to demonstrate altered medial temporal lobe function during the processing of threat cues in youths with a history of caregiver deprivation and emotional neglect.

[1]  P. Sinha,et al.  Effects of early experience on children's recognition of facial displays of emotion. , 2002, Developmental psychology.

[2]  Gustavo Turecki,et al.  Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse , 2009, Nature Neuroscience.

[3]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[4]  Stephan Heckers,et al.  Sustained activation of the hippocampus in response to fearful faces in schizophrenia , 2005, Biological Psychiatry.

[5]  R. Kahn,et al.  Lateralization of amygdala activation: a systematic review of functional neuroimaging studies , 2004, Brain Research Reviews.

[6]  S. Pollak Experience‐Dependent Affective Learning and Risk for Psychopathology in Children , 2003, Annals of the New York Academy of Sciences.

[7]  William D S Killgore,et al.  Sex-specific developmental changes in amygdala responses to affective faces , 2001, Neuroreport.

[8]  S. Lupien,et al.  The effects of stress and stress hormones on human cognition: Implications for the field of brain and cognition , 2007, Brain and Cognition.

[9]  R. Davidson Well-being and affective style: neural substrates and biobehavioural correlates. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  Jeffrey A Lieberman,et al.  Neuropsychological correlates of hippocampal volumes in patients experiencing a first episode of schizophrenia. , 2002, The American journal of psychiatry.

[11]  D. Pine Developmental psychobiology and response to threats: relevance to trauma in children and adolescents , 2003, Biological Psychiatry.

[12]  R. Cabeza,et al.  Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events , 2004, Neuron.

[13]  Lisa A. Thomas,et al.  Biologic findings of post-traumatic stress disorder and child maltreatment , 2003, Current psychiatry reports.

[14]  S. Pollak,et al.  Selective attention to facial emotion in physically abused children. , 2003, Journal of abnormal psychology.

[15]  D. Pine,et al.  Trauma in children and adolescents: risk and treatment of psychiatric sequelae , 2002, Biological Psychiatry.

[16]  M. Ernst,et al.  Altered amygdala and hippocampus function in adolescents with hypercortisolemia: A functional magnetic resonance imaging study of Cushing syndrome , 2008, Development and Psychopathology.

[17]  Carrie L. Masten,et al.  Recognition of facial emotions among maltreated children with high rates of post-traumatic stress disorder. , 2008, Child abuse & neglect.

[18]  Martin H. Teicher,et al.  Developmental neurobiology of childhood stress and trauma. , 2002, The Psychiatric clinics of North America.

[19]  M. Gunnar,et al.  International adoption of institutionally reared children: Research and policy , 2000, Development and Psychopathology.

[20]  M. Kovacs The Children's Depression, Inventory (CDI). , 1985, Psychopharmacology bulletin.

[21]  M. D’Esposito,et al.  Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. , 1997, NeuroImage.

[22]  S. Southwick,et al.  MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. , 2003, The American journal of psychiatry.

[23]  Emma Colvert,et al.  Early adolescent outcomes for institutionally-deprived and non-deprived adoptees. I: disinhibited attachment. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[24]  Jong-Min Lee,et al.  Integration of cross-modal emotional information in the human brain: An fMRI study , 2010, Cortex.

[25]  Miou Zhou,et al.  Developmental Changes in NMDA Neurotoxicity Reflect Developmental Changes in Subunit Composition of NMDA Receptors , 2006, The Journal of Neuroscience.

[26]  N. Halfon,et al.  Health status of children in foster care. The experience of the Center for the Vulnerable Child. , 1995, Archives of pediatrics & adolescent medicine.

[27]  D. Pine,et al.  The risk for early-adulthood anxiety and depressive disorders in adolescents with anxiety and depressive disorders. , 1998, Archives of general psychiatry.

[28]  S. Southwick,et al.  Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. , 1999, The American journal of psychiatry.

[29]  Christian Büchel,et al.  Detecting fearful and neutral faces: BOLD latency differences in amygdala–hippocampal junction , 2006, NeuroImage.

[30]  Monique Ernst,et al.  Developmental differences in neuronal engagement during implicit encoding of emotional faces: an event-related fMRI study. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[31]  M. Winick,et al.  Early malnutrition and "late" adoption: a study of their effects on the development of Korean orphans adopted into American families. , 1977, The American journal of clinical nutrition.

[32]  Ellen Leibenluft,et al.  A Developmental Examination of Amygdala Response to Facial Expressions , 2008, Journal of Cognitive Neuroscience.

[33]  M. Smucker,et al.  Normative and reliability data for the children's depression inventory , 1986, Journal of abnormal child psychology.

[34]  Sandra M. Neer,et al.  The Screen for Child Anxiety Related Emotional Disorders (SCARED): scale construction and psychometric characteristics. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[35]  J. Dunn,et al.  The development of adopted children after institutional care: a follow-up study. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[36]  Robert M. Sapolsky,et al.  Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent , 1990, Brain Research.

[37]  S. Southwick,et al.  Neural correlates of declarative memory for emotionally valenced words in women with posttraumatic stress disorder related to early childhood sexual abuse , 2003, Biological Psychiatry.

[38]  P. Mason,et al.  International Adoption: A Health and Developmental Prospective , 2005, Seminars in speech and language.

[39]  Chet D. Johnson,et al.  Developmental Issues for Young Children in Foster Care , 2000 .

[40]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[41]  Christopher S. Monk,et al.  Increased Amygdala Activity During Successful Memory Encoding in Adolescent Major Depressive Disorder: An fMRI Study , 2006, Biological Psychiatry.

[42]  M. D’Esposito,et al.  Empirical Analyses of BOLD fMRI Statistics , 1997, NeuroImage.

[43]  A. Reiss,et al.  Stress Predicts Brain Changes in Children: A Pilot Longitudinal Study on Youth Stress, Posttraumatic Stress Disorder, and the Hippocampus , 2007, Pediatrics.

[44]  A. Winsler,et al.  Child Neglect: Developmental Consequences, Intervention, and Policy Implications , 2006 .

[45]  I. Litt,et al.  Adolescents' self-assessment of sexual maturation. , 1980, Pediatrics.

[46]  M. Ernst,et al.  Amygdala function in adolescents with congenital adrenal hyperplasia: A model for the study of early steroid abnormalities , 2007, Neuropsychologia.

[47]  M. Rutter,et al.  Developmental catch-up, and deficit, following adoption after severe global early privation. English and Romanian Adoptees (ERA) Study Team. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[48]  J. Seok,et al.  Neural correlates of affective processing in response to sad and angry facial stimuli in patients with major depressive disorder , 2008, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[49]  Monique Ernst,et al.  Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. , 2007, Archives of general psychiatry.

[50]  Monique Ernst,et al.  Ventrolateral prefrontal cortex activation and attentional bias in response to angry faces in adolescents with generalized anxiety disorder. , 2006, The American journal of psychiatry.

[51]  P. Fisher,et al.  Developmental, Cognitive, and Neuropsychological Functioning in Preschool-aged Foster Children: Associations with Prior Maltreatment and Placement History , 2005, Journal of developmental and behavioral pediatrics : JDBP.

[52]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[53]  P. Fisher,et al.  Emotion understanding and theory of mind among maltreated children in foster care: Evidence of deficits , 2005, Development and Psychopathology.

[54]  R. Harris,et al.  Malnutrition and environmental enrichment by early adoption , 1975, Science.

[55]  Michael G. Hardin,et al.  Attention alters neural responses to evocative faces in behaviorally inhibited adolescents , 2007, NeuroImage.

[56]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[57]  Christian Grillon,et al.  Positron emission tomographic imaging of neural correlates of a fear acquisition and extinction paradigm in women with childhood sexual-abuse-related post-traumatic stress disorder , 2004, Psychological Medicine.

[58]  M. K. Gordon,et al.  Foster Children’s Diurnal Production of Cortisol: An Exploratory Study , 2006, Child maltreatment.

[59]  P. McGuire,et al.  Laterality effect on emotional faces processing: ALE meta-analysis of evidence , 2009, Neuroscience Letters.

[60]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[61]  Dependent Care Developmental Issues for Young Children in Foster Care , 2000, Pediatrics.

[62]  S. Nickman,et al.  Children in adoptive families: overview and update. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[63]  P. Fisher,et al.  Interventions for foster parents: Implications for developmental theory , 2002, Development and Psychopathology.

[64]  Monique Ernst,et al.  Attention bias to threat in maltreated children: implications for vulnerability to stress-related psychopathology. , 2005, The American journal of psychiatry.

[65]  Mairead C. Dolan,et al.  Psychopathy and Functional Magnetic Resonance Imaging Blood Oxygenation Level-Dependent Responses to Emotional Faces in Violent Patients with Schizophrenia , 2009, Biological Psychiatry.

[66]  Monique Ernst,et al.  A developmental examination of gender differences in brain engagement during evaluation of threat , 2004, Biological Psychiatry.

[67]  P. Ekman Pictures of Facial Affect , 1976 .

[68]  M Ashtari,et al.  Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. , 1999, Archives of general psychiatry.

[69]  J. Rawlins,et al.  Regional dissociations within the hippocampus—memory and anxiety , 2004, Neuroscience & Biobehavioral Reviews.

[70]  Matcheri S. Keshavan,et al.  Brain structures in pediatric maltreatment-related posttraumatic stress disorder: a sociodemographically matched study , 2002, Biological Psychiatry.

[71]  Jeonghun Ku,et al.  The neural mechanism of imagining facial affective expression , 2007, Brain Research.

[72]  D. Pine Research review: a neuroscience framework for pediatric anxiety disorders. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[73]  R. Adolphs Cognitive neuroscience: Cognitive neuroscience of human social behaviour , 2003, Nature Reviews Neuroscience.

[74]  E. McClure A meta-analytic review of sex differences in facial expression processing and their development in infants, children, and adolescents. , 2000, Psychological bulletin.

[75]  M. Rutter,et al.  Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. , 2004, Developmental psychology.

[76]  Anirvan S. Nandy,et al.  The Angry Brain: Neural Correlates of Anger, Angry Rumination, and Aggressive Personality , 2009, Journal of Cognitive Neuroscience.

[77]  M. Rutter,et al.  Normality and impairment following profound early institutional deprivation: a longitudinal follow-up into early adolescence. , 2007, Developmental psychology.

[78]  Otto Muzik,et al.  Local Brain Functional Activity Following Early Deprivation: A Study of Postinstitutionalized Romanian Orphans , 2001, NeuroImage.

[79]  Larry A. Tupler,et al.  Segmented Hippocampal Volume in Children and Adolescents with Posttraumatic Stress Disorder , 2006, Biological Psychiatry.

[80]  D. Cicchetti,et al.  Recognizing emotion in faces: developmental effects of child abuse and neglect. , 2000, Developmental psychology.

[81]  D. Stein,et al.  Functional Neuroimaging in Post-traumatic Stress Disorder , 2004 .

[82]  S. Pollak Early adversity and mechanisms of plasticity: Integrating affective neuroscience with developmental approaches to psychopathology , 2005, Development and Psychopathology.

[83]  S. Pollak,et al.  Emotion understanding in postinstitutionalized Eastern European children , 2004, Development and Psychopathology.

[84]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[85]  A. B. Hollingshead,et al.  Four factor index of social status , 1975 .

[86]  N. Ryan,et al.  Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[87]  P. Plotsky,et al.  Early adverse experience as a developmental risk factor for later psychopathology: Evidence from rodent and primate models , 2001, Development and Psychopathology.

[88]  J. Tanner,et al.  Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. , 1976, Archives of disease in childhood.

[89]  Dante Cicchetti,et al.  Child maltreatment. , 2005, Annual review of clinical psychology.

[90]  M. Sanchez,et al.  The impact of early adverse care on HPA axis development: Nonhuman primate models , 2006, Hormones and Behavior.

[91]  Ellen Leibenluft,et al.  Adolescent immaturity in attention-related brain engagement to emotional facial expressions , 2003, NeuroImage.

[92]  Monique Ernst,et al.  Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. , 2008, Archives of general psychiatry.

[93]  Thomas J. Eluvathingal,et al.  Abnormal Brain Connectivity in Children After Early Severe Socioemotional Deprivation: A Diffusion Tensor Imaging Study , 2006, Pediatrics.

[94]  Joseph E LeDoux Emotion Circuits in the Brain , 2000 .

[95]  K. Lee Crying patterns of Korean infants in institutions. , 2000, Child: care, health and development.

[96]  Amelia K. Searle,et al.  The mental health and wellbeing of children and adolescents in home‐based foster care , 2007, The Medical journal of Australia.

[97]  M. Meaney,et al.  Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. , 2001, Annual review of neuroscience.

[98]  Joan Kaufman,et al.  Effects of early adverse experiences on brain structure and function: clinical implications , 2000, Biological Psychiatry.

[99]  J. Armony,et al.  Amygdala response in patients with acute PTSD to masked and unmasked emotional facial expressions. , 2005, The American journal of psychiatry.

[100]  M. Rutter,et al.  Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees study pilot. , 2009, Journal of child psychology and psychiatry, and allied disciplines.

[101]  M. D. Bellis The psychobiology of neglect. , 2005 .