Left Amygdala Regulates the Cerebral Reading Network During Fast Emotion Word Processing

Abstract

Emotion words constitute a special class of verbal stimuli which can quickly activate the limbic system outside the left-hemisphere language network. Such fast response to emotion words may arise independently of the left occipitotemporal area involved in visual word-form analysis and rely on a distinct amygdala-dependent emotion circuit involved in fearful face processing. Using a hemifield priming paradigm with fMRI, we explored how the left and right amygdala systems interact with the reading network during emotion word processing. On each trial, participants viewed a centrally presented target which was preceded by a masked prime flashed either to the left or right visual field. Primes and targets, each denoting negative or positive nouns, could be either affectively congruent or incongruent with each other. We observed that affective congruency produced parallel changes in neural priming between the left frontal and parietotemporal regions and the bilateral amygdala. However, we also found that the left, but not right, amygdala exhibited significant change in functional connectivity with the neural components of reading as a function of affective congruency. Collectively, these results suggest that emotion words activate the bilateral amygdala during early stages of emotion word processing, whereas only the left amygdala exerts a long-distance regulatory influence over the reading network via its strong within-hemisphere connectivity.

Keywords: affective priming; amygdala; emotion words; functional connectivity; reading; repetition suppression and enhancement.

Figure 1

Behavioral paradigm. Each trial consisted of a masked prime flashed to LVF or RVF and a visible target displayed on the center of the screen. Primes and targets, each representing either positive or negative nouns, could be either congruent or incongruent with each other in emotional valence. Participants determined whether visible targets represented concrete objects or abstract concepts.

Figure 2

Behavioral results. Median reaction times (SEM) during the concrete/abstract judgment task as a function of prime valence (positive and negative) and prime hemifield (LVF and RVF). Participants responded faster to congruent (C) targets than to incongruent (IC) targets when masked primes were positive in valence. In contrast, participants responded faster to incongruent targets than to congruent targets when masked primes were negative in valance. This reversal of priming directions was observed on both LVF and RVF trials and confirmed by a robust cross-over interaction between the effects of valence and affective priming (see section “Results”).

Figure 3

Brain regions showing cross-over interaction between valence and affective priming. For each region, percent signal change relative to the baseline is plotted against the valence (positive and negative) and prime hemifield (LVF and RVF). The whole-brain SPM analysis identified three left hemisphere regions showing significant changes in priming directions associated with the reversal of behavioral priming. That is, the left IFG, ACC, PPC, and OTC showed repetition enhancement associated with inhibitory priming (i.e., to negative primes) and repetition suppression associated with facilitatory priming (i.e., to positive primes), respectively.

Figure 4

Effects of affective priming in the left and right amygdala ROIs. The left and right amygdala ROIs showed the similar patterns of cross-over interaction between valence and affective priming as those observed in the whole-brain SPM (see Figure 3). The magnitude of this valence × priming interaction did not differ between LVF and RVF, either for the left amygdala or for the right amygdala. Thus, negative and positive primes each showed the same trend of repetition enhancement and repetition suppression as the cerebral reading network, irrespective of the prime hemifield.

Figure 5

Functional connectivity with the amygdala in the left-hemisphere network involved in fast emotion word processing. Box plots for each region show the magnitude of group-level inter-regional connectivity with the left and right amygdala ROIs. The four cortical regions identified in the whole-brain SPM (see Figure 3) are surface-rendered on the normalized brain using MRIcron (https://www.nitrc.org/projects/mricron). Significant functional coupling was observed only between the left IFG and the left amygdala (shaded in gray, see section “Results”). Moreover, while all the four regions showed the same trend of greater connectivity with the left amygdala than with the right amygdala, this left-vs.-right difference in amygdala connectivity was significant only for the left IFG (^*p = 0.04).