Hemispheric asymmetry for affective stimulus processing in healthy subjects--a fMRI study

Abstract

Background: While hemispheric specialization of language processing is well established, lateralization of emotion processing is still under debate. Several conflicting hypotheses have been proposed, including right hemisphere hypothesis, valence asymmetry hypothesis and region-specific lateralization hypothesis. However, experimental evidence for these hypotheses remains inconclusive, partly because direct comparisons between hemispheres are scarce.

Methods: The present fMRI study systematically investigated functional lateralization during affective stimulus processing in 36 healthy participants. We normalized our functional data on a symmetrical template to avoid confounding effects of anatomical asymmetries. Direct comparison of BOLD responses between hemispheres was accomplished taking two approaches: a hypothesis-driven region of interest analysis focusing on brain areas most frequently reported in earlier neuroimaging studies of emotion; and an exploratory whole volume analysis contrasting non-flipped with flipped functional data using paired t-test.

Results: The region of interest analysis revealed lateralization towards the left in the medial prefrontal cortex (BA 10) during positive stimulus processing; while negative stimulus processing was lateralized towards the right in the dorsolateral prefrontal cortex (BA 9 & 46) and towards the left in the amygdala and uncus. The whole brain analysis yielded similar results and, in addition, revealed lateralization towards the right in the premotor cortex (BA 6) and the temporo-occipital junction (BA 19 & 37) during positive stimulus processing; while negative stimulus processing showed lateralization towards the right in the temporo-parietal junction (BA 37,39,42) and towards the left in the middle temporal gyrus (BA 21).

Conclusion: Our data suggests region-specific functional lateralization of emotion processing. Findings show valence asymmetry for prefrontal cortical areas and left-lateralized negative stimulus processing in subcortical areas, in particular, amygdala and uncus.

Figure 1. Lateralization during positive and negative picture viewing. ROI analysis.

Lateralization of BOLD responses in regions of interest. The bars represent hemispheric differences of contrasts of parameter estimates (red: ‘positive > neutral’; blue: ‘negative > neutral’) extracted from the respective ROI (mean values for the respective ROI, averaged across the 36 participants). Bars extending to the left indicate lateralization towards the left (left > right), and bars extending to the right indicate lateralization towards the right (right > left). *p<0.05; (*) p<0.1 on tests of laterality within valence condition (positive or negative), or between positive and negative valence conditions if marked by brackets. Lat PFC, dorsolateral prefrontal cortex; mPFC, medial prefrontal cortex; acc, anterior cingulate cortex; oc, occipital cortex.

Figure 2. Lateralization during positive picture viewing.

Whole volume analysis. Brain areas showing lateralization (‘left > right’, ‘right > left’) during positive (versus neutral) picture viewing (‘pos > neu’); SPM whole volume analysis (paired t-test) comparing non-flipped with flipped functional data. Because data represent comparisons between left and right hemispheres, sections views display half of the brain only: ‚Left > right’ indicates clusters showing significantly larger activation in the left compared to the right hemisphere. ‚Right > left’ indicates clusters showing significantly larger activation in the right compared to the left hemisphere. Clusters are projected on a symmetrical MNI template. P<0.001 uncorrected, cluster size k≥5, t = t-value. Bars represent contrasts of parameter estimates for ‘positive > neutral picture viewing’ (‘positive’) and ‘negative > neutral picture viewing’ (‘negative’). Values were extracted from peak voxels presented in Table 1 for the right and the left hemisphere averaged across the 36 participants.

Figure 3. Lateralization during negative picture viewing. Whole volume analysis.

Brain areas showing lateralization (‘left > right’, ‘right > left’) during negative (versus neutral) picture viewing (‘pos > neu’); SPM whole volume analysis (paired t-test) comparing non-flipped with flipped functional data. Because data represent comparisons between left and right hemispheres, sections views display half of the brain only: ‚Left > right’ indicates clusters showing significantly larger activation in the left compared to the right hemisphere. ‚Right > left’ indicates clusters showing significantly larger activation in the right compared to the left hemisphere. Clusters are projected on a symmetrical MNI template. P<0.001 uncorrected, cluster size k≥5, t = t-value. Bars represent contrasts of parameter estimates for ‘positive > neutral picture viewing’ (‘positive’) and ‘negative > neutral picture viewing’ (‘negative’). Values were extracted from peak voxels presented in Table 2 for the right and the left hemisphere averaged across the 36 participants.

Figure 4. Lateralization during negative versus positive picture viewing. Whole volume analysis.

Brain areas showing lateralization (‘right > left’) during negative versus positive picture viewing (‘neg >pos’); SPM whole volume analysis (paired t-test) comparing non-flipped (right-sided) with flipped (left-sided) functional data. Because data represent comparisons between left and right hemispheres, sections views display half of the brain only: ‚Right > left’ indicates clusters showing significantly larger activation in the right compared to the left hemisphere. The reverse contrast (‘left > right’) revealed no significant effect. Clusters are projected on a symmetrical MNI template. P<0.001 uncorrected, cluster size k≥5, t = t-value. Bars represent contrasts of parameter estimates for ‘positive > neutral picture viewing’ (‘positive’) and ‘negative > neutral picture viewing’ (‘negative’). Values were extracted from peak voxels presented in Table 3 for the right and the left hemisphere averaged across the 36 participants.