Increased amygdala and visual cortex activity and functional connectivity towards stimulus novelty is associated with state anxiety

Abstract

Novel stimuli often require a rapid reallocation of sensory processing resources to determine the significance of the event, and the appropriate behavioral response. Both the amygdala and the visual cortex are central elements of the neural circuitry responding to novelty, demonstrating increased activity to new as compared to highly familiarized stimuli. Further, these brain areas are intimately connected, and thus the amygdala may be a key region for directing sensory processing resources to novel events. Although knowledge regarding the neurocircuit of novelty detection is gradually increasing, we still lack a basic understanding of the conditions that are necessary and sufficient for novelty-specific responses in human amygdala and the visual cortices, and if these brain areas interact during detection of novelty. In the present study, we investigated the response of amygdala and the visual cortex to novelty, by comparing functional MRI activity between 1st and 2nd time presentation of a series of emotional faces in an event-related task. We observed a significant decrease in amygdala and visual cortex activity already after a single stimulus exposure. Interestingly, this decrease in responsiveness was less for subjects with a high score on state anxiety. Further, novel faces stimuli were associated with a relative increase in the functional coupling between the amygdala and the inferior occipital gyrus (BA 18). Thus, we suggest that amygdala is involved in fast sensory boosting that may be important for attention reallocation to novel events, and that the strength of this response depends on individual state anxiety.

Figure 1. Amygdala and visual cortex BOLD activation to stimulus novelty.

BOLD fMRI responses in the amygdala and visual cortex obtained for the contrast ”1^st presentation” >”2^nd presentation”. (A) Statistical parametric maps (SPM) demonstrating the responses in visual cortex for the given contrast. The image is thresholded at p = 0.005, k = 25 voxels for illustrative reasons. The colors refer to t-values as coded in the bar to the left of the image (B) Statistical parametric maps (SPM) demonstrating the responses in amygdala for the same contrast. The image is thresholded at p = 0.005, k = 25 voxels for illustrative reasons. (C) Beta values for the peak voxel in right amygdala (x = 24, y = −6, z = −14) and right inferior occipital gyrus (x = 34, y = −78, z = −12) for the conditions 1^st presentation and 2^nd presentation of the emotional faces.

Figure 2. Correlation between state anxiety scores and individual amygdala activation.

Negative correlation between the individual state anxiety scores and the activity in right amygdala. Subjects with a high score on state anxiety had less amygdala signal change between the 1^st time and the 2^nd time presentation of the emotional faces. (A) Statistical parametric map (SPM) showing the right amygdala cluster. The image is thresholded at p<0.005, 25 voxels extent threshold, for illustrative reasons. The colors refer to t-values as coded in the bar to the right of the image (B) Scatter-plot demonstrating the negative correlation.

Figure 3. BOLD activation by condition in right inferior occipital gyrus.

Beta values for the peak voxel in right inferior occipital gyrus (x = 34, y = −78, z = −12) for the conditions 1^st presentation, 2^nd presentation and other presentations of the emotional faces. The figure illustrates that the right inferior occipital gyrus BOLD fMRI response was significantly reduced in the 2^nd compared to the 1^st presentation. However, the BOLD response during the 2^nd presentation was significantly greater than the mean response from the remaining presentations of the faces.

Figure 4. Psychophysiological interaction analysis.

The results of the psychophysiological interaction analysis. (A) Statistical parametric map (SPM) showing regions in the visual cortex that showed condition-specific BOLD signal changes with right amygdala activity. The image is thresholded at p<0.005, 25 voxels extent threshold, for illustrative reasons. The colors refer to t-values as coded in the bar to the right of the image (B) Scatter plot with regression lines demonstrating the pattern of functional connectivity. The x-axis represents activity in the right amygdala (beta values) peak voxel and the y-axis represents activity in the right inferior occipital gyrus peak voxel (beta values).