Emotionally arousing pictures induce increased activation of visual pathways relative to emotionally neutral images. A predominant model for the preferential processing and attention to emotional stimuli posits that the amygdala modulates sensory pathways through its projections to visual cortices. However, recent behavioral studies have found intact perceptual facilitation of emotional stimuli in individuals with amygdala damage. To determine the importance of the amygdala to modulations in visual processing, we used functional magnetic resonance imaging to examine visual cortical blood oxygenation level-dependent (BOLD) signal in response to emotionally salient and neutral images in a sample of human patients with unilateral medial temporal lobe resection that included the amygdala. Adults with right (n ϭ 13) or left (n ϭ 5) medial temporal lobe resections were compared with demographically matched healthy control participants (n ϭ 16). In the control participants, both aversive and erotic images produced robust BOLD signal increases in bilateral primary and secondary visual cortices relative to neutral images. Similarly, all patients with amygdala resections showed enhanced visual cortical activations to erotic images both ipsilateral and contralateral to the lesion site. All but one of the amygdala resection patients showed similar enhancements to aversive stimuli and there were no significant group differences in visual cortex BOLD responses in patients compared with controls for either aversive or erotic images. Our results indicate that neither the right nor left amygdala is necessary for the heightened visual cortex BOLD responses observed during emotional stimulus presentation. These data challenge an amygdalo-centric model of emotional modulation and suggest that non-amygdalar processes contribute to the emotional modulation of sensory pathways.
The importance of cues signaling reward, threat or danger would suggest that they receive processing privileges in the neural systems underlying perception and attention. Previous research has documented enhanced processing of motivationally salient cues, and has pointed to the amygdala as a candidate neural structure underlying the enhancements. In the current study, we examined whether the amygdala was necessary for this emotional modulation of attention to occur. Patients with unilateral amygdala lesions and matched controls completed an emotional attentional blink task in which emotional distractors impair the perception of subsequent targets. Emotional images proved more distracting across all participant groups, including those with right or left amygdala lesions. These data argue against a central role for the amygdala in mediating all types of attentional capture by emotional stimuli.
Previous research has indicated that the amygdala is a critical neural substrate of the emotional modulation of attention. However, a recent case-study suggests that the amygdala may not be essential for all types of emotion-attention interactions. In order to test this hypothesis, we assessed the visual-search performance of patients with unilateral amygdala lesions, matched controls, and medication-matched epilepsy patients with intact amygdalae. All participants completed a visualsearch task consisting of trials in which (1) an emotional target was embedded amongst neutral distractors, (2) a neutral target was embedded amongst emotional distractors, or (3) a neutral target was embedded amongst neutral distractors. All participant groups, including those with amygdala lesions, detected emotional targets more efficiently than neutral targets. These data indicate that the amygdala is not necessary for emotion-guided visual search and suggest that other mechanisms beyond the amygdala help guide attention toward threatening stimuli.
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