Impaired emotional declarative memory following unilateral amygdala damage

Abstract

Case studies of patients with bilateral amygdala damage and functional imaging studies of normal individuals have demonstrated that the amygdala plays a critical role in encoding emotionally arousing stimuli into long-term declarative memory. However, several issues remain poorly understood: the separate roles of left and right amygdala, the time course over which the amygdala participates in memory consolidation, and the type of knowledge structures it helps consolidate. We investigated these questions in eight subjects with unilateral amygdala damage, using several different measures. For comparison, our main task used stimuli identical to those used previously to investigate emotional declarative memory in patients with bilateral amygdala damage. Contrasts with both brain-damaged and normal control groups showed that subjects with left amygdala damage were impaired in their memory for emotional stimuli, despite entirely normal memory for neutral stimuli (because of a number of caveats, the findings from subjects with right amygdala damage were less clear). Follow-up experiments suggested that the normal facilitation of memory for emotional stimuli may develop over an extended time course (>30 min), consistent with prior findings, and that the specific impairment we report may depend in part on the lexical nature of the task used (written questionnaire). We stress the complex and temporally extended nature of memory consolidation and suggest that the amygdala may influence specific components of this process.

Figure 1

Summary of subjects' neuroanatomy. Subjects' lesions from MR scans were coregistered onto the corresponding MR sections of a single, normal reference brain. The joint overlaps of lesions from multiple subjects were encoded by color (scale showing total subject N at bottom), and the MR sections of the normal brain with mapped lesions were then reconstructed in 3-D to obtain the whole brains shown in the figure (Frank et al. 1997). (Left) Left and right lateral views of the 3-D reconstructed brain with mapped lesions; (right) coronal sections through the middle and very anterior amygdala, corresponding to the planes indicated on the whole brains. Note that we follow the radiological convention of showing the right side of the brain on the left side of the coronal images.

Figure 2

Ratings of the stimuli. Shown are ratings of valence (9-point scale; 5 is neutral), arousal (9-point scale; 5 is neutral), perceived visual complexity (scale 0–3), and perceived unusualness (scale 0–3). In all cases, subjects rated their own personal reaction or judgment. Data are from normal controls, brain-damaged controls, left amygdala damage, and right amygdala damage, as indicated. The x-axis ranks the stimuli in the order that they were shown during the task (█) Normals; (●) BD control; (▴) L amygdala; (♦) R amygdala.

Figure 3

Memory performance on 24-hr delayed questionnaire. Proportion correct mean choices are shown for each subject group. Chance is at 0.25 (█) Normals; (●) BD control; (▴) L amygdala; (♦) R amygdala.

Figure 4

Memory performance on 24-hr delayed visual recognition. Proportion correct mean choices are shown for each subject group. Chance is at 0.25. Data from the two subjects with right amygdala damage are not shown for clarity (both recognized slide 7 correctly and showed the same overall pattern as the other subject groups). Although all subject groups performed comparably on this task, this finding is subject to ceiling effects and may not reveal more subtle impairments. (█) Normals; (●) BD control; (▴) L amygdala.

Figure 5

Memory performance on questionnaire after a 30-min delay. Data are from a separate group of nine normal controls and demonstrate that the enhanced memory for emotionally arousing material is a pattern that requires longer than 30 min to appear. For comparison, the data from normal subjects with the 24-hr delay are shown as well. (█) 24 hr; (●) 30 min.