Using Movies to Probe the Neurobiology of Anxiety

What can movies tell us about the anxious brain? In our recent papers, we explore how anxiety shapes with brain and cardiac dynamics during movie-watching.

A well characterized amygdala-prefrontal circuit is thought to be crucial for threat vigilance during anxiety. However, studies to date have primarily investigated this using static stimuli (i.e. faces) presented without context. Consequently, the relationship between this circuit and anxiety in relatively more dynamic, naturalistic contexts remains poorly understood. Extending study of this circuitry to more naturalistic stimuli offers the opportunity to validate these findings in more ecologically-rich settings and observe how this circuit may be modulated as a function of dynamic, contextual features. We have now investigated this using naturalistic ‘movie fMRI’ data from the Naturalistic Neuroimaging Database (N=86), Human Connectome Project (N=178), and CamCAN (N=630) datasets. Firstly, we report a relationship between trait anxiety and stimulus-dependent activations in the Naturalistic Neuroimaging Database. Specifically, self-reported anxiety was associated with decreased activation to words in the primary auditory cortex and increased activation to faces in the superior parietal lobe. 

Whole-brain results (p <.001, cluster-corrected) demonstrating activations to faces and spoken words and how these activations correlate with self-reported anxiety (red = positive; blue = negative values).

Static connectivity analyses (which treat brain connectivity as time-invariant) of the Naturalistic Neuroimaging Database and Human Connectome Project failed to demonstrate any relationship between amygdala-prefrontal connectivity and anxiety during movie-watching. However, dynamic analyses (which treat brain connectivity as relatively time-varying) of the CamCAN database revealed trait anxiety to have a variable association with amygdala-prefrontal connectivity dependent on the degree of suspense during the movie. Specifically, we observed effects in the inverse direction to what we predicted: anxiety was associated with increases in right amygdala-prefrontal connectivity primarily during low suspense scenes (r = -.14, p = .04; figure 2). Additionally, a planned exploratory analysis suggested a measure of threat-relevant attentional bias was also sensitive to these effects (r = -.24, p = .001). We offer three potential interpretations of these findings: 1) high anxiety individuals may chronically engage threat circuitry irrespective of suspenseful scenes in a movie; 2) high anxiety individuals anticipate suspenseful scenes quicker, engaging threat circuitry at earlier time points; and/or 3) high anxiety individuals are slower to disengage threat circuitry following suspenseful scenes.

Scatterplots demonstrating a negative correlation (with 95% Confidence Intervals) between TR-wise suspense ratings and anxiety-relevant increases in right amygdala-dorsomedial prefrontal connectivity. Left: hospital anxiety and depression scale anxiety scores. Right: affective bias (drift rate from drift-diffusion models of fearful face responding). 

Timeseries of canonical suspense ratings (orange line), suspenseful events (orange rectangles; marked using amplitude-based peak detection), average right amygdala-dmPFC dynamic connectivity, and the correlation between anxiety and dynamic connectivity at each TR (smoothed). Shading denotes 95% confidence intervals. 

There is also evidence to suggest anxiety impacts the degree of communication between the brain and the autonomic nervous system. Using a suspenseful movie-watching paradigm (n=29-), we demonstrated that anxiety was associated with reduced coherence between heart rate and: amygdala-dorsomedial prefrontal dynamic connectivity; amygdala-subgenual anterior cingulate dynamic connectivity; precuneus activity; vmPFC activity; and bilateral putamen activity. Taken together, we provide preliminary evidence for altered neural-autonomic coherence as a function of anxiogenic movie-watching.

Effect (Cohen’s D) of suspenseful vs non-suspenseful movie-watching on brain-heart coherence. Coherence measures in each condition were defined as the Fisher transformed bivariate correlation between 6s-lagged HR against fMRI measures.  The diagonal of the matrix represents change in activation-based coherence. Cells below the diagonal represents change in dynamic connectivity-based coherence. Blue cells refer to a reduction in coherence between heart rate and brain responses during suspenseful movie-watching relative to non-suspenseful movie-watching, while red cells refer to an increase. There were no significant changes in the coherence between activation and heart rate. Dynamic connectivity between the right amygdala and both the dmPFC and sgACC was associated with reduced coherence with heart rate during the anxiogenic movie. ** p < .0009 (Bonferroni-corrected threshold), * p < .05 (uncorrected). 

Violin plots detailing coherence (Fisher-transformed correlation coefficients) between amygdala-prefrontal dynamic connectivity and heart rate as participants watched non-suspenseful and suspenseful movie clips. This illustrates that coherence was significantly positive during the non-suspenseful condition and was reduced during the suspenseful condition (to negative coherence for amygdala-dmPFC and to non-significant coherence for amygdala-sgACC). * p < .05.