Increased amygdala activation is related to heart rate during emotion processing in adolescent subjects

Emotions have been conceptualized as representations of bodily responses to a stimulus that critically involves the autonomic nervous system (ANS). An association between amygdala activation and ANS activity has been shown in adults. However, to date, no studies have demonstrated this association in adolescents. Examining the interaction between the ANS and amygdala in healthy adolescents may provide information about age-related changes in the association between amygdala activation and ANS measures. Therefore, the aim of this study was to examine the relationship between amygdala activation and heart rate in normal adolescents. Eighteen 12- to 17-year old adolescents participated. Heart rate data was collected during functional magnetic resonance imaging while subjects performed a facial expression matching task that reliably activates the amygdala. Adolescents showed significant amygdala activation for all facial expressions relative to the shape-matching, control task. Moreover, the degree of activation in the right amygdala for Fearful faces was significantly correlated with heart rate (Spearman's rho=0.55, p=0.018, two-tailed). This study shows that amygdala activity is related to heart rate in healthy adolescents. Thus, similar to adults, adolescents show a coupling between processing emotional events and adjusting the ANS accordingly. Furthermore, this study confirms previous adolescent studies showing amygdala activation to Fearful, Angry, and Happy faces. Finally, the results of the present study lay the foundation for future research to investigate whether adolescents with mood or anxiety disorders show an altered coupling between processing emotionally salient events and ANS activity.

[1]  Eric Vermetten,et al.  Hippocampal and amygdalar volumes in dissociative identity disorder. , 2006, The American journal of psychiatry.

[2]  J. Stainer,et al.  The Emotions , 1922, Nature.

[3]  W. James.  Discussion: The physical basis of emotion. , 1894 .

[4]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[5]  Isabel Gauthier,et al.  fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism , 2005, Neuropsychologia.

[6]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[7]  Stephan Eliez,et al.  Amygdalar activation associated with positive and negative facial expressions , 2002, Neuroreport.

[8]  Joseph E LeDoux.  Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[9]  M. Mintun,et al.  Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study , 2001, Biological Psychiatry.

[10]  Justin S. Feinstein,et al.  Dose-dependent decrease of activation in bilateral amygdala and insula by lorazepam during emotion processing. , 2005, Archives of general psychiatry.

[11]  Justin S. Feinstein,et al.  Lorazepam dose-dependently decreases risk-taking related activation in limbic areas , 2006, Psychopharmacology.

[12]  G. Breithardt,et al.  Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. , 1996 .

[13]  Philipp Sterzer,et al.  Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder , 2005, Biological Psychiatry.

[14]  Michael G. Hardin,et al.  Triadic model of the neurobiology of motivated behavior in adolescence , 2005, Psychological Medicine.

[15]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[16]  R. Harper,et al.  Cardiac and respiratory correlations with unit discharge in human amygdala and hippocampus. , 1989, Electroencephalography and clinical neurophysiology.

[17]  Andrzej Urbanik,et al.  Central control of heart rate changes during visual affective processing as revealed by fMRI. , 2003, Acta neurobiologiae experimentalis.

[18]  W. Grodd,et al.  Differential amygdala activation in schizophrenia during sadness , 1998, Schizophrenia Research.

[19]  Jenifer Juranek,et al.  Association Between Amygdala Volume and Anxiety Level: Magnetic Resonance Imaging (MRI) Study in Autistic Children , 2006, Journal of child neurology.

[20]  W. James.  The Physical Basis of Emotion. , 1994 .

[21]  R. Harper,et al.  Cardiac and Respiratory Correlations with Unit Discharge in Epileptic Human Temporal Lobe , 1990, Epilepsia.

[22]  R Bandler,et al.  Lateralized and widespread brain activation during transient blood pressure elevation revealed by magnetic resonance imaging , 2000, The Journal of comparative neurology.

[23]  Deborah A. Yurgelun-Todd,et al.  Amygdala and hippocampus volumes in pediatric major depression , 2005, Biological Psychiatry.

[24]  B. J. Casey,et al.  Amygdala response to fearful faces in anxious and depressed children. , 2001, Archives of general psychiatry.

[25]  Hugo D. Critchley,et al.  Activity in the human brain predicting differential heart rate responses to emotional facial expressions , 2005, NeuroImage.

[26]  A. Porta,et al.  Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt. , 1994, Circulation.

[27]  S. Rauch,et al.  Amygdala, Medial Prefrontal Cortex, and Hippocampal Function in PTSD , 2006, Annals of the New York Academy of Sciences.

[28]  Andrew H. Kemp,et al.  Distinct amygdala–autonomic arousal profiles in response to fear signals in healthy males and females , 2005, NeuroImage.

[29]  R. J Dolan,et al.  Activity in ventromedial prefrontal cortex covaries with sympathetic skin conductance level: a physiological account of a “default mode” of brain function , 2004, NeuroImage.

[30]  V. Somers,et al.  Heart Rate Variability: , 2003, Journal of cardiovascular electrophysiology.

[31]  B. Hurwitz,et al.  Decomposition of heart rate variability by adaptive filtering for estimation of cardiac vagal tone , 1991, Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society Volume 13: 1991.

[32]  E. Leibenluft,et al.  Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[34]  K. Jan,et al.  Decomposition of heart rate variability by adaptive filtering for estimation of cardiac vagal tone , 1991 .

[35]  E. Courchesne,et al.  Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. , 2001, Brain : a journal of neurology.

[36]  V. Menon,et al.  Amygdalar activation associated with happy facial expressions in adolescents: a 3-T functional MRI study. , 2003, Journal of the American Academy of Child and Adolescent Psychiatry.

[37]  William D S Killgore,et al.  fMRI during affect discrimination in bipolar affective disorder. , 2000, Bipolar disorders.

[38]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[39]  A. Malliani,et al.  Heart rate variability. Standards of measurement, physiological interpretation, and clinical use , 1996 .

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

[41]  C. A. Swenne,et al.  Heart rate and heart rate variability as indexes of sympathovagal balance. , 1994, The American journal of physiology.

[42]  D. Shaffer,et al.  NIMH Diagnostic Interview Schedule for Children Version IV (NIMH DISC-IV): description, differences from previous versions, and reliability of some common diagnoses. , 2000, Journal of the American Academy of Child and Adolescent Psychiatry.

[43]  J Lee,et al.  REGIONAL BRAIN ACTIVATION IN HUMANS DURING RESPIRATORY AND BLOOD PRESSURE CHALLENGES , 1998, Clinical and experimental pharmacology & physiology.

[44]  M. Egan,et al.  Serotonin Transporter Genetic Variation and the Response of the Human Amygdala , 2002, Science.