Film excerpts shown to specifically elicit various affects lead to overlapping activation foci in a large set of symmetrical brain regions in males

Abstract

While the limbic system theory continues to be part of common scientific parlance, its validity has been questioned on multiple grounds. Nonetheless, the issue of whether or not there exists a set of brain areas preferentially dedicated to emotional processing remains central within affective neuroscience. Recently, a widespread neural reference space for emotion which includes limbic as well as other regions was characterized in a large meta-analysis. As methodologically heterogeneous studies go into such meta-analyses, showing in an individual study in which all parameters are kept constant, the involvement of overlapping areas for various emotion conditions in keeping with the neural reference space for emotion, would serve as valuable confirmatory evidence. Here, using fMRI, 20 young adult men were scanned while viewing validated neutral and effective emotion-eliciting short film excerpts shown to quickly and specifically elicit disgust, amusement, or sexual arousal. Each emotion-specific run included, in random order, multiple neutral and emotion condition blocks. A stringent conjunction analysis revealed a large overlap across emotion conditions that fit remarkably well with the neural reference space for emotion. This overlap included symmetrical bilateral activation of the medial prefrontal cortex, the anterior cingulate, the temporo-occipital junction, the basal ganglia, the brainstem, the amygdala, the hippocampus, the thalamus, the subthalamic nucleus, the posterior hypothalamus, the cerebellum, as well as the frontal operculum extending towards the anterior insula. This study clearly confirms for the visual modality, that processing emotional stimuli leads to widespread increases in activation that cluster within relatively confined areas, regardless of valence.

Figure 1. Sagittal and coronal slices across the main areas of supra-threshold areas of activation for the ‘Amusement condition minus Neutral’, ‘Disgust condition minus Neutral’, and ‘Sexual arousal condition minus Neutral’ contrasts.

Note the similarities between contrasts. All contrasts clearly show involvement of medial prefrontal cortex, supplementary motor area, hypothalamus, thalamus, amygdala, ventral insula, and cerebellum.

Figure 2. Three-dimensional rendered images of areas of supra-threshold areas of activation for the same contrasts as Figure 1.

Here again, there similarities are obvious between contrasts. All contrasts clearly show involvement of the frontal operculum, dorsolateral prefrontal cortex, premotor and motor cortices, temporo-occipital regions, and cerebellum.

Figure 3. Areas of significant BOLD signal changes for the ‘amusement minus neutral’, ‘disgust minus neutral’, and ‘sexual arousal minus neutral’ conjunction null analysis conducted at the second level.

Accompanying sagittal, coronal and horizontal slices through most ROIs are provided. BOLD signal changes for these slices are coregistered on top of normalized brain sections from the Montreal Neurological Institute (MNI) stereotaxic space template. Coordinates (x, y, and z) are given in mm and refer to locations in MNI stereotaxic space. Height threshold is set to p = 0.001, uncorrected. The neurological convention has been chosen for orientation of coronal sections in all figures i.e., left is left and right is right. A: Medial prefrontal cortex, frontal operculum encroaching on anterior insula, thalamus, lateral occipital gyrus B: Medial prefrontal cortex, anterior cingulate, thalamus, brainstem, cerebellum C: Supplementary motor area, thalamus, amygdala D: Temporo-occipital junction, cerebellum.

Figure 4. Three-dimensional rendered images of areas of significant activation for the same contrast as Figure 3.

Note the involvement of the frontal operculum, temporo-occipital regions, cerebellum, and lateral temporal, premotor as well as motor cortices.

Figure 5. Sagittal, coronal, and/or axial slices across the main areas of supra-threshold activated areas for the ‘Amusement condition-specific’, ‘Disgust condition-specific’, and ‘Sexual arousal condition-specific’ contrasts.

Slices were selected so as to show most involved areas. Amusement-specific temporal, medial occipital and precuneus areas are shown on top. Disgust condition-specific periaqueductal, posterior pons, left amygdala, left hypothalamus, and cerebellar areas are shown in the middle and Sexual arousal-condition-specific medial prefrontal, posterior cingulate, cerebellar, and precuneus regions are shown at the bottom.

Figure 6. Three-dimensional rendered images of supra-threshold of activated areas for the same contrasts as Figure 5.

Temporal cortical involvement is shown to be specific here to the Amusement condition, lateral occipital and fusiform areas to the Disgust condition, and superior parietal and posterior inferior temporal areas to the Sexual arousal condition.