INVITED COMMENTARY
Emotional Memory Functions of the Human Amygdala Kevin S. LaBar, PhD
Address Center for Cognitive Neuroscience, Duke University, Box 90999, Durham, NC 27708-0999, USA. E-mail:
[email protected] Current Neurology and Neuroscience Reports 2003, 3:363–364 Current Science Inc. ISSN 1528–4042 Copyright © 2003 by Current Science Inc.
Introduction Recent developments in behavioral neurology and cognitive neuroscience have sparked a renewed interest in understanding the functions of the human amygdala, an enigmatic temporal lobe region historically linked to motivated behaviors. Significant advances have been made in understanding its role in emotional learning and memory through a combination of neuropsychologic, functional neuroimaging, and intracranial recording studies. The evidence to date indicates that the amygdala is important for aspects of both implicit (unconscious or nondeclarative) and explicit (conscious or declarative) forms of memory. In the implicit domain, the amygdala is critical for learning conditioned emotional associations but not for the acquisition of preferences. In the explicit domain, it contributes to multiple stages of memory processing, but only for events that have high emotional salience. These effects can be understood within the framework of a two-factor model of emotional memory in which arousal and valence dimensions of affective space have dissociable impacts on memory performance and amygdala function.
Implicit Emotional Memory Pavlovian fear-conditioning paradigms have provided a useful starting point for investigating emotional memory in the implicit domain. Neurologic patients with damage to the amygdala have difficulty acquiring conditioned fear responses to visual or auditory cues paired with aversive noises or tactile stimulation. Such emotional learning deficits are present despite intact autonomic response generation to noxious stimuli and intact declarative memory about the stimulus contingencies during the task. Amnesic patients without amygdala damage show the converse effect; they cannot state the stimulus relationships but nonetheless show intact conditioned fear responses on simple tasks. Collectively, these observations support a
double dissociation between the role of the hippocampus and amygdala relative to declarative knowledge and physiologic indices of fear acquisition. Neuroimaging studies of the amygdala in healthy subjects have confirmed the patient results, even when fear conditioning proceeds subconsciously by perceptual masking. Amygdala activation to conditioned fear stimuli emerges within a few training trials, similar to its temporal profile in electrophysiologic recordings from rats. Amygdala processing during associative learning thus signals rapid detection of changes in the emotional salience of sensory stimuli that can occur outside of awareness. In contrast, amygdala-lesioned patients typically demonstrate intact acquisition of preferences. Preference formation has been studied using both mere exposure and social judgment tests. In a mere exposure task, preference judgments for novel neutral stimuli increase as a function of repeated exposure to the items. In a social preference task, preference judgments are evaluated following repeated exposure to real or fictitious characters who exhibit positive or negative personality traits. Mere exposure effects and acquired social preferences are generally preserved even when concomitant hippocampal damage renders the patient amnesic to the learning episode. One feature that discriminates fear conditioning from preference formation is the degree of arousal elicited by the tasks. Whereas conditioning tasks establish mnemonic associations to highly arousing events of biologic importance, preference tests involve exposure to stimuli that are affectively valent (or neutral) but low in arousal. Typical preference formation tests may be insufficiently arousing to engage an amygdala-dependent memory system. In fact, temporal lobectomy patients fail to acquire preferences to neutral stimuli that are conditionally paired with salient, primary reward cues. An analogous dissociation between the amygdala's sensitivity to influences of arousal versus valence is further described with respect to explicit memory in the following text.
Explicit Emotional Memory The anatomic proximity of the amygdala and the hippocampus makes it difficult to distinguish their contributions to explicit emotional memory in patients with organic syndromes or neurologic insults affecting the medial
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temporal lobe. Several rare case studies have now been reported of patients who present with amygdala damage without concomitant amnesia. The relative sparing of hippocampal function in these patients enables an assessment of explicit memory for emotional material without encountering floor effects in overall performance. Such cases help to determine the range of explicit emotional memories possible in the absence of intact amygdalae. Functional magnetic resonance imaging can also discriminate signal changes within these adjacent brain regions in healthy subjects. Finally, epileptic patients with implanted electrodes in the medial temporal lobe provide unique insight into the effects of amygdala stimulation on recall of emotional life events. Most patient studies have investigated explicit emotional memory by testing recognition and recall for words, pictures, or stories that vary in their emotional properties. Unlike healthy control patients, amygdalalesioned patients do not exhibit better recognition memory for details of emotionally arousing scenes or story segments relative to neutral ones. Because arousal and valence ratings of the pictures or narrative elements are normal, the deficit is not due to impaired affective evaluation of the material during encoding. This pattern of performance is usually interpreted as a failure of arousal-enhanced memory consolidation. To specifically implicate consolidation processes, memory must be assessed at various times after encoding to demonstrate that the impairment is magnified following a delay relative to immediate testing. In healthy subjects, forgetting rates for emotionally arousing words are slower than for neutral words. Forgetting rates in amygdala-lesioned patients, however, do not vary as a function of emotional content. This role of the amygdala has been confirmed in functional imaging studies where the degree of amygdala activation during encoding has been shown to predict subsequent memory for emotionally arousing, but not neutral, material. Amygdala-lesioned patients perform normally on other explicit emotional memory tests. On word list learning paradigms, they selectively remember positively and negatively valent words that are low in arousal relative to neutral words. They also remember neutral words encoded in affective sentence contexts better than those encoded in neutral sentence contexts. Memory performance on these tasks benefits from an organizational function of affective valence via semantic integration processes. In healthy subjects, the retention advantage for both affectively valent words and affective sentence contexts is eliminated when the neutral words or sentences are semantically categorized. Memory in amygdala-lesioned patients improves when they can utilize organizational semantic cues even when the material is highly arousing. For instance, they show good retention for the main ideas, but not the details, of emotionally arousing stories in free recall tests. Emotional memory facilitation by semantic integration is a relatively unexplored topic whose neuroanatomic correlates are unknown. Because the pre-
frontal cortex regulates strategic aspects of memory processing, organizational effects of affective valence may involve interactions between the frontal lobes and temporal neocortex where semantic representations are putatively stored. Based on these results, it is clear that additional amygdala-independent mechanisms contribute to explicit emotional memory formation in humans. The amygdala also participates in the retrieval stage of memory processing. Imaging studies have revealed amygdala activity during the recall of autobiographic memories, including the recall of traumatic episodes experienced by post-traumatic stress disorder patients. In addition, stimulation of the amygdala in epileptic patients with implanted electrodes for seizure monitoring elicits retrieval of salient personal memories that sometimes extend to the remote past. Stimulation-induced memory fragments always contain emotional content, although the emotion most often evoked from amygdalar sites is fear. In this line of research, however, it is important to disambiguate amygdala signals related to memory retrieval operations versus emotional perception, expression, or feeling states generated by the retrieval cues or electrical stimulation itself. Recent animal studies have also indicated that the amygdala is directly involved in reconsolidating emotional memory traces upon retrieval. In contrast, classic accounts of amygdala function have emphasized its modulation of memory consolidation occurring in other brain regions during a limited time window after encoding. With accumulating evidence, it appears that the rich qualities of emotional experiences engage multiple, interactive mechanisms in the amygdala and other brain regions to collectively ensure persistence in memory.
Conclusions Affective space is conceptually parsed according to two principal factors or underlying dimensions—arousal and valence. The aforementioned analysis supports a basic dissociation between the amygdala's contribution to arousal versus valence functions in memory. Whereas the amygdala mediates arousal effects during conditioned emotional learning and across various stages of explicit memory processing (eg, encoding, consolidation, and retrieval), preference formation and affective semantic integration occur outside the amygdaloid system. Unlike its sister structure, the hippocampus, the amygdala's role in memory cuts across the implicitexplicit dichotomy. Arousal systems are associated with survival functions, including defensive, reproductive, and maternal behaviors, which may account for the amygdala's participation in certain emotions over others. The scientific understanding of emotional memory will be further refined with improved neuroscientific methodologies and paradigm development. In particular, future studies should characterize the amygdala's participation in other forms of implicit memory and clarify the scope of its influence beyond basic emotions such as fear.
