The neurophysiological bases of emotion: An fMRI study of the affective circumplex using emotion-denoting words

Abstract

Objective: We aimed to study the neural processing of emotion-denoting words based on a circumplex model of affect, which posits that all emotions can be described as a linear combination of two neurophysiological dimensions, valence and arousal. Based on the circumplex model, we predicted a linear relationship between neural activity and incremental changes in these two affective dimensions.

Methods: Using functional magnetic resonance imaging, we assessed in 10 subjects the correlations of BOLD (blood oxygen level dependent) signal with ratings of valence and arousal during the presentation of emotion-denoting words.

Results: Valence ratings correlated positively with neural activity in the left insular cortex and inversely with neural activity in the right dorsolateral prefrontal and precuneus cortices. The absolute value of valence ratings (reflecting the positive and negative extremes of valence) correlated positively with neural activity in the left dorsolateral and medial prefrontal cortex (PFC), dorsal anterior cingulate cortex, posterior cingulate cortex, and right dorsal PFC, and inversely with neural activity in the left medial temporal cortex and right amygdala. Arousal ratings and neural activity correlated positively in the left parahippocampus and dorsal anterior cingulate cortex, and inversely in the left dorsolateral PFC and dorsal cerebellum.

Conclusion: We found evidence for two neural networks subserving the affective dimensions of valence and arousal. These findings clarify inconsistencies from prior imaging studies of affect by suggesting that two underlying neurophysiological systems, valence and arousal, may subserve the processing of affective stimuli, consistent with the circumplex model of affect.

Figures

Figure 1

A schematic representation of the affective circumplex. The horizontal axis represents valence and the vertical axis represents arousal. Circles are drawn around each emotion to indicate that the affective states are ambiguous, overlapping categories.

Figure 2

Each trial was divided into three distinct temporal components: (1) participants were shown a single emotion‐denoting word; (2) participants were shown a 9 × 9 grid displaying the dimensions of valence and arousal as visual analog scales on the x‐ and y‐axes, respectively, ranging in values from −4 to +4; (3) participants gazed at a cross‐hair at the center of an otherwise blank screen. The duration of Component 1 was 18 s. The combined duration of Components 2 and 3 was 20 s. The 9 × 9 grid was presented on screen until the subject made a selection or until a maximum time of 20 s had elapsed. Once the participant made the selection, the fixation screen was displayed for the remainder of the 20 s (i.e. the duration of Component 3 = 20 s − the duration of Component 2).

Figure 3

Valence unadjusted and Arousal unadjusted index voxel‐wise correlations of subjects' affective ratings and BOLD signal. Valence extremes index correlations of the absolute value of subjects' valence ratings and BOLD signal. Positive correlations are coded in red to yellow, and inverse correlations are coded in green to purple. The effective P‐value for the conjoint requirement of a statistical threshold and cluster filter across all voxels was < 0.05 [Forman et al., 1995]. A: Activity in the left anterior insula cortex (AIN) correlated with valence ratings. Inverse correlations in the right dorsolateral prefrontal cortex (DLPFC) and the right precuneus gyrus (PC) indicate that activity in these regions decreased with progressively more positive ratings of valence (or increased with more negative valence ratings) B: Activity in the left parahippocampal gyrus (PHG) and the bilateral anterior cingulate cortex (ACC) correlated with arousal ratings. The inverse correlations in left dorsolateral prefrontal cortex (DLPFC) and the dorsal cerebellum (DC) indicate that activity decreased with progressively more positive ratings of arousal (or increased with more negative ratings). C: Activity in the left dorsolateral prefrontal cortex (DLPFC), bilateral medial prefrontal cortex (MPFC), bilateral anterior cingulate cortex (ACC), and bilateral posterior cingulate cortex (PCC) correlated with extremes of valence ratings. Inverse correlation in the right amygdala (AMG) indicates that activity decreased with progressively more extreme ratings of valence.

Figure 4

Unit change in BOLD signal per unit change in affective rating. BOLD signal intensity and affective ratings are represented on the vertical and horizontal axes, respectively. A: Valence ratings correlated positively with activity in the left anterior insula and inversely with activity in right dorsolateral prefrontal cortex (DLPFC). B: Arousal ratings correlated positively with activity in the dorsal anterior cingulate and inversely with activity in the left DLPFC. C: Valence extremely correlated positively with activity in the left medial prefrontal cortex (MPFC) and inversely with activity in the right amygdala. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]