Enhanced Visual Cortical Activation for Emotional Stimuli is Preserved in Patients with Unilateral Amygdala Resection

Abstract

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 role of the basolateral amygdala in the perception of faces in natural contexts

“…This suggests that the fusiform gyrus remains functional, but that AMG-mediated contextual regulation is disrupted. In line with our results, a recent study reported no differences in ventral stream activity between participants with unilateral amygdala damage and healthy controls during the processing of emotional images [42].…”

“…Several findings already suggest that damage to this structure would impact the processing in the dorsal stream more than the ventral stream during contextual emotional face perception. No consistent effect of damage to the AMG, including the BLA, on activity in ventral regions has been reported [15,42]. Against this background, we expected that damage to BLA would modify activity in the dorsal stream.…”

Asymmetrical effects of unilateral right or left amygdala damage on auditory cortical processing of vocal emotions

“…Distant effects of amygdala damage have also been observed for visual stimuli in cats (19) and for auditory stimuli in rats (8). However, other results have challenged this view, with some studies reporting no impairment in recognition (20)(21)(22)(23)(24)(25) or changes in cortical processing for emotional stimuli in patients with amygdala lesions (26). Notably, Edmiston et al (26) observed normal visual increases in response to emotional scenes for patients with unilateral amygdala resection, arguing against a direct role for the amygdala in modulating activity in sensory cortical areas.…”

“…However, other results have challenged this view, with some studies reporting no impairment in recognition (20)(21)(22)(23)(24)(25) or changes in cortical processing for emotional stimuli in patients with amygdala lesions (26). Notably, Edmiston et al (26) observed normal visual increases in response to emotional scenes for patients with unilateral amygdala resection, arguing against a direct role for the amygdala in modulating activity in sensory cortical areas. However, in that study (26), such increases could be related to attentional effects driven by greater interest or complexity of emotional scenes (27,28).…”

“…Notably, Edmiston et al (26) observed normal visual increases in response to emotional scenes for patients with unilateral amygdala resection, arguing against a direct role for the amygdala in modulating activity in sensory cortical areas. However, in that study (26), such increases could be related to attentional effects driven by greater interest or complexity of emotional scenes (27,28).…”