Amygdala activity related to enhanced memory for pleasant and aversive stimuli.

Pleasant or aversive events are better remembered than neutral events. Emotional enhancement of episodic memory has been linked to the amygdala in animal and neuropsychological studies. Using positron emission tomography, we show that bilateral amygdala activity during memory encoding is correlated with enhanced episodic recognition memory for both pleasant and aversive visual stimuli relative to neutral stimuli, and that this relationship is specific to emotional stimuli. Furthermore, data suggest that the amygdala enhances episodic memory in part through modulation of hippocampal activity. The human amygdala seems to modulate the strength of conscious memory for events according to emotional importance, regardless of whether the emotion is pleasant or aversive.

Normal recognition of emotional similarity between facial expressions following bilateral amygdala damage.

Bilateral damage to the amygdala in humans has been previously linked to two deficits in recognizing emotion in facial expressions: recognition of individual basic emotions, especially fear, and recognition of similarity among emotional expressions. Although several studies have examined recognition of individual emotions following amygdala damage, only one subject has been examined on recognition of similarity. To assess the extent to which deficits in recognizing similarity among facial expressions might be a general consequence of amygdala damage, we examined this ability in two subjects with complete bilateral amygdala damage. Both subjects had previously demonstrated entirely normal recognition of individual facial emotions. Here we report that these two patients also are intact in their ability to recognize similarity between emotional expressions. These results indicate that, like the recognition of individual basic emotions in facial expressions, the recognition of similarity among emotional expressions does not have an absolute dependence on the amygdala.

Intact perceptual memory in the absence of conscious memory.

Declarative memory enables conscious recollection of the past and has been proposed to be distinct from priming, a perceptual form of memory that operates nonconsciously and improves the ability to detect or identify recently presented stimuli. Yet, it has been difficult to obtain unambiguous evidence for the independence of declarative memory and priming. The authors report the first demonstration, using matched tests, of fully intact perceptual memory (priming) in a profoundly amnesic patient (E.P.), despite at-chance recognition memory. The priming and recognition tests included tests that were matched with respect to test materials, length of the study and test lists, and the kind of cues available at test. Priming appears to reflect neural changes within perceptual processing systems that occur before information reaches the brain systems that transform visual perception into conscious visual memory.

On the acquisition of new declarative knowledge in amnesia.

In 2 experiments, the acquisition of new declarative knowledge was examined in amnesic patients and in 7 groups of controls, with a study-only procedure that delayed testing until the conclusion of training. The study-only procedure was compared with a standard procedure in which study and test trials alternated (study-test). The amnesic patients acquired new factual (declarative) knowledge at an abnormally slow rate, learning more with the study-only procedure than with the study-test procedure. Controls exhibited the opposite pattern. The advantage of the study-only procedure for amnesic patients was related to the presence of frontal lobe dysfunction. The 2 groups exhibited a similar ability to use their knowledge flexibly, suggesting that the information acquired by amnesic patients was based on their residual capacity for declarative memory. In addition, the capacity for factual learning in amnesia was proportional to the capacity to recollect specific events in the learning session.

When amnesic patients perform well on recognition memory tests.

Extended exposure to study material can markedly improve subsequent recognition memory performance in amnesic patients, even the densely amnesic patient H.M. To understand this phenomenon, the severely amnesic patient E.P., 3 other amnesic patients, and controls studied pictorial material and then were given either a yes-no (Experiment 1) or a 2-alternative, forced-choice (Experiment 2) recognition test. The amnesic patients and controls benefited substantially from extended exposure, but patient E.P. consistently performed at chance. Furthermore, confidence ratings corresponded to recognition accuracy. The results do not support the idea that the benefit of extended study time is due to some kind of familiarity process made available through nondeclarative memory. It is likely that amnesic patients benefit from extended study time to the extent that they have residual capacity for declarative memory.

Emotional perception and memory in amnesia.

The authors examined whether perception of emotional stimuli is normal in amnesia and whether emotional arousal has the same enhancing effect on memory in amnesic patients as it has in healthy controls. Forty standardized color pictures were presented while participants rated each picture according to emotional intensity (arousal) and pleasantness (valence). An immediate free-recall test was given for the pictures, followed by a yes-no recognition test. Arousal and valence ratings were highly similar among the amnesic patients and controls. Emotional arousal (regardless of valence) enhanced both recall and recognition of the pictures, and this enhancement was proportional for amnesic patients and controls. Results suggest that emotional perception and the enhancing effect of emotional arousal on memory are intact in amnesia.

Memory enhancement for emotional stimuli is impaired in early Alzheimer's disease.

Emotional arousal is associated with enhanced memory in neurologically intact individuals, but it is unknown whether this effect is obtained in Alzheimer's disease (AD). The current study compared emotional memory and emotional reactions in patients with early AD and in older controls. Participants viewed emotionally arousing (both pleasant and unpleasant) and neutral photographs while cognitive and electrophysiological reactions were assessed. Memory was tested by free recall and recognition. Emotional reactions were normal in the AD group, but the emotional memory effect (enhanced memory for emotional vs. neutral stimuli) was impaired. Recall results indicated that this effect was normal for pleasant stimuli but abnormal for unpleasant stimuli. These results suggest that the neural basis for the emotional memory effect may be disrupted in AD. Findings are discussed in terms of the role of the amygdala in mediating emotional memory.

Level-of-processing effects in word-completion priming: a neuropsychological study.

Recent reviews (A.S. Brown & D.B. Mitchell, 1994; B. Challis & D.R. Brodbeck, 1992) concluded that level-of-processing (LOP) manipulations affect priming in perceptual tasks, contrary to earlier suggestions that such tasks are insensitive to LOP. In 3 experiments with amnesic patients and control subjects, the authors examined the effect of LOP manipulations on priming in word-stem and word-fragment completion and on recognition memory. Amnesic patients exhibited reduced or near-zero LOP effects in word-completion priming compared with control subjects. LOP affected recognition memory for both amnesic patients and control subjects, confirming that the LOP manipulation affected explicit memory. When the effect of explicit retrieval on control performance was reduced by using a low-level encoding task, priming was the same for amnesic patients and control subjects. The authors suggest that LOP effects in word-completion priming tasks reflect the influence of explicit retrieval, which can be used usefully by control subjects but much less so by amnesic patients.

Intact priming for novel perceptual representations in amnesia.

Recent studies have challenged the notion that priming for ostensibly novel stimuli such as pseudowords (REAB) reflects the creation of new representations. Priming for such stimuli could instead reflect the activation of familiar memory representations that are orthographically similar (READ) and/or the activation of subparts of stimuli (RE, EX, AR), which are familar because they occur commonly in English. We addressed this issue in three experiments that assessed perceptual identification priming and recognition memory for novel and familiar letter strings in amnesic patients and control subjects. Priming for words, pseudowords, and orthographically illegal nonwords was fully intact in the amnesic patients following a single exposure, whereas recognition memory was impaired for the same items. Thus, priming can occur for stimuli that are unlikely to have preexisting representations. Words and pseudowords exhibited twice as much priming as illegal nonwords, suggesting that activation may contribute to priming for words and wordlike stimuli. Additional results showed that priming for illegal nonwords resulted from the formation of new perceptual associations among the component letters of each nonword rather than the activation of individual letter representations. In summary, the results demonstrate that priming following a single exposure can depend on the creation of new perceptual representations and that such priming is independent of the brain structures essential for declarative memory.

Intact enhancement of declarative memory for emotional material in amnesia.

Emotional arousal has been demonstrated to enhance declarative memory (conscious recollection) in humans in both naturalistic and experimental studies. Here, we examined this effect in amnesia. Amnesic patients and controls viewed a slide presentation while listening to an accompanying emotionally arousing story. In both groups, recognition memory was enhanced for the emotionally arousing story elements. The magnitude of the enhancement was proportional for both amnesic patients and controls. Emotional reactions to the story were also equivalent. The results suggest that the enhancement of declarative memory associated with emotional arousal is intact in amnesia. Together with findings from patients with bilateral amygdala lesions, the results indicate that the amygdala is responsible for the enhancement effect.