Limbic dysregulation is associated with lowered heart rate variability and increased trait in healthy adults

Lilianne R. Mujica-Parodi, Mayuresh Korgaonkar, Bosky Ravindranath, Tsafrir Greenberg, Dardo Tomasi, Mark E. Wagshul, Babak Ardekani, David Guilfoyle, Shilpi Khan, Yuru Zhong, Ki Chon, Dolores Malaspina

Research output: Contribution to journalArticle

55 Citations (Scopus)

Abstract

Objectives: We tested whether dynamic interaction between limbic regions supports a control systems model of excitatory and inhibitory components of a negative feedback loop, and whether dysregulation of those dynamics might correlate with trait differences in anxiety and their cardiac characteristics among healthy adults. Experimental Design: Sixty-five subjects received fMRI scans while passively viewing angry, fearful, happy, and neutral facial stimuli. Subjects also completed a trait anxiety inventory, and were monitored using ambulatory wake ECG. The ECG data were analyzed for heart rate variability, a measure of autonomic regulation. The fMRI data were analyzed with respect to six limbic regions (bilateral amygdala, bilateral hippocampus, Brodmann Areas 9, 45) using limbic time-series cross-correlations, maximum BOLD amplitude, and BOLD amplitude at each point in the time-series. Principal Observations: Diminished coupling between limbic time-series in response to the neutral, fearful, and happy faces was associated with greater trait anxiety, greater sympathetic activation, and lowered heart rate variability. Individuals with greater levels of trait anxiety showed delayed activation of Brodmann Area 45 in response to the fearful and happy faces, and lowered Brodmann Area 45 activation with prolonged left amygdala activation in response to the neutral faces. Conclusions: The dynamics support limbic regulation as a control system, in which dysregulation, as assessed by diminished coupling between limbic time-series, is associated with increased trait anxiety and excitatory autonomic outputs. Trait-anxious individuals showed delayed inhibitory activation in response to overt-affect stimuli and diminished inhibitory activation with delayed extinction of excitatory activation in response to ambiguous-affect stimuli.

Original languageEnglish (US)
Pages (from-to)47-58
Number of pages12
JournalHuman Brain Mapping
Volume30
Issue number1
DOIs
StatePublished - Jan 2009
Externally publishedYes

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Anxiety
Heart Rate
Amygdala
Electrocardiography
Magnetic Resonance Imaging
Hippocampus
Research Design
Equipment and Supplies

Keywords

  • Amygdala
  • Anxiety
  • Autonomic
  • Cardiac
  • connectivity
  • Control systems
  • Dynamic
  • fMRI
  • Heart rate variability
  • Homeostasis
  • Limbic
  • Prefrontal cortex
  • Stress
  • Time-series

ASJC Scopus subject areas

  • Clinical Neurology
  • Anatomy
  • Neurology
  • Radiology Nuclear Medicine and imaging
  • Radiological and Ultrasound Technology

Cite this

Mujica-Parodi, L. R., Korgaonkar, M., Ravindranath, B., Greenberg, T., Tomasi, D., Wagshul, M. E., ... Malaspina, D. (2009). Limbic dysregulation is associated with lowered heart rate variability and increased trait in healthy adults. Human Brain Mapping, 30(1), 47-58. https://doi.org/10.1002/hbm.20483

Limbic dysregulation is associated with lowered heart rate variability and increased trait in healthy adults. / Mujica-Parodi, Lilianne R.; Korgaonkar, Mayuresh; Ravindranath, Bosky; Greenberg, Tsafrir; Tomasi, Dardo; Wagshul, Mark E.; Ardekani, Babak; Guilfoyle, David; Khan, Shilpi; Zhong, Yuru; Chon, Ki; Malaspina, Dolores.

In: Human Brain Mapping, Vol. 30, No. 1, 01.2009, p. 47-58.

Research output: Contribution to journalArticle

Mujica-Parodi, LR, Korgaonkar, M, Ravindranath, B, Greenberg, T, Tomasi, D, Wagshul, ME, Ardekani, B, Guilfoyle, D, Khan, S, Zhong, Y, Chon, K & Malaspina, D 2009, 'Limbic dysregulation is associated with lowered heart rate variability and increased trait in healthy adults', Human Brain Mapping, vol. 30, no. 1, pp. 47-58. https://doi.org/10.1002/hbm.20483
Mujica-Parodi, Lilianne R. ; Korgaonkar, Mayuresh ; Ravindranath, Bosky ; Greenberg, Tsafrir ; Tomasi, Dardo ; Wagshul, Mark E. ; Ardekani, Babak ; Guilfoyle, David ; Khan, Shilpi ; Zhong, Yuru ; Chon, Ki ; Malaspina, Dolores. / Limbic dysregulation is associated with lowered heart rate variability and increased trait in healthy adults. In: Human Brain Mapping. 2009 ; Vol. 30, No. 1. pp. 47-58.
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