Distinct neural systems underlying reduced emotional enhancement for positive and negative stimuli in early Alzheimer's disease (original) (raw)
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Frontiers in Aging Neuroscience, 2015
We studied the influence of emotions on autobiographical memory (AbM) in patients with Alzheimer's disease (AD), characteristically triggering atrophy in the hippocampus and the amygdala, two crucial structures sustaining memory and emotional processing. Our first aim was to analyze the influence of emotion on AbM in AD patients, on both the proportion and the specificity of emotional memories. Additionally, we sought to determine the relationship of emotional AbM to amygdalar-hippocampal volumes. Eighteen prodromal to mild AD patients and 18 age-matched healthy controls were included. We obtained 30 autobiographical memories per participant using the modified Crovitz test (MCT). Analyses were performed on global scores, rates and specificity scores of the emotional vs. neutral categories of memories. Amygdalar-hippocampal volumes were extracted from 3D T1-weighted MRI scans and tested for correlations with behavioral data. Overall, AD patients displayed a deficit in emotional AbMs as they elicited less emotional memories than the controls, however, the specificity of those memories was preserved. The deficit likely implied retrieval or storage as it was extended in time and without reminiscence bump effect. Global scores and rates of emotional memories, but not the specificity scores, were correlated to right amygdalar and hippocampal volumes, indicating that atrophy in these structures has a central role in the deficit observed. Conversely, emotional memories were more specific than neutral memories in both groups, reflecting an enhancement effect of emotion that could be supported by other brain regions that are spared during the early stages of the disease.
BMC Psychiatry, 2013
Background: Relative to intentional memory encoding, which quickly declines in Mild Cognitive Impairment (MCI) and Alzheimer's disease (AD), incidental memory for emotional stimuli appears to deteriorate more slowly. We hypothesised that tests of incidental emotional memory may inform on different aspects of cognitive decline in MCI and AD. Methods: Patients with MCI, AD and Healthy Controls (HC) were asked to attend to emotional pictures (i.e., positive and neutral) sequentially presented during an fMRI session. Attention was monitored behaviourally. A surprise postscan recognition test was then administered. Results: The groups remained attentive within the scanner. The post-scan recognition pattern was in the form of (HC = MCI) > AD, with only the former group showing a clear benefit from emotional pictures. fMRI analysis of incidental encoding demonstrated clusters of activation in para-hippocampal regions and in the hippocampus in HC and MCI patients but not in AD patients. The pattern of activation observed in MCI patients tended to be greater than that found in HC.
Effects of normal aging and Alzheimer's disease on emotional memory
Emotion, 2002
Recall is typically better for emotional than for neutral stimuli. This enhancement is believed to rely on limbic regions. Memory is also better for neutral stimuli embedded in an emotional context. The neural substrate supporting this effect has not been thoroughly investigated but may include frontal lobe, as well as limbic circuits. Alzheimer's disease (AD) results in atrophy of limbic structures, whereas normal aging relatively spares limbic regions but affects prefrontal areas. The authors hypothesized that AD would reduce all enhancement effects, whereas aging would disproportionately affect enhancement based on emotional context. The results confirmed the authors' hypotheses: Young and older adults, but not AD patients, showed better memory for emotional versus neutral pictures and words. Older adults and AD patients showed no benefit from emotional context, whereas young adults remembered more items embedded in an emotional versus neutral context. Declarative memory for emotional stimuli (positive and negative) is typically better than memory for neu
Neuroimage, 2003
Considerable evidence from both animal and human subject research supports the hypothesis that the amygdala, when activated by emotional arousal, modulates memory storage processes in other brain regions. By this hypothesis, changes in the functional interactions of the amygdala with other brain regions during emotional conditions should underlie, at least in part, enhanced memory for emotional material. Here we examined the influence of the human amygdala on other brain regions under emotional and nonemotional learning conditions using structural equation modeling (SEqM). Eleven male subjects received two PET scans for regional cerebral glucose metabolism-one scan while viewing a series of emotionally provocative (negative) film clips and a second scan while viewing a series of more emotionally neutral film clips. Enhanced activity in the right amygdala was related to enhanced memory for the emotional films. To identify potential candidate voxels for SEqM, the functional connectivity of the maximally activated voxel within the right amygdala was investigated using partial least squares. A subset of regions identified by this analysis showing differences functional connectivity with the amygdala between the emotional versus neutral film conditions were then submitted to SEqM, which revealed significantly increased amygdala influences on the ipsilateral parahippocampal gyrus and ventrolateral prefrontal cortex during the emotional relative to the neutral film viewing condition. These findings support the view that increased influences from the amygdala, presumably reflecting its memorymodulation function, occur during emotionally arousing learning situations.
Neural Correlates of Emotional Memories: A Review of Evidence from Brain Imaging Studies
PSYCHOLOGIA, 2012
What are the neural markers of encoding and retrieving emotional events with increased efficacy? In recent years, this question has captured the attention of cognitive neuroscientists who fervently engaged in addressing it using a multitude of approaches. The present review discusses evidence from brain imaging studies investigating the neural correlates of the memory-enhancing effect of emotion in healthy human participants. The available evidence points to two main mechanisms: one direct involving the medial temporal lobe (MTL), and the other indirect involving the prefrontal cortex (PFC), among other brain regions. Recent studies also showed that these mechanisms are sensitive to aspects relevant to social interactions, as well as to personality-, sex-and age-related differences. Overall, this evidence provides insights into the brain mechanisms that make emotional memories special, and points to possible alterations that could lead to negative affective biases in encoding and remembering emotional memories observed in affective disorders.
Effects of Alzheimer disease on memory for verbal emotional information
Neuropsychologia, 2004
In healthy young and older adults, emotional information is often better remembered than neutral information. It is an open question, however, whether emotional memory enhancement is blunted or preserved in Alzheimer disease (AD). Prior studies of emotional memory in AD have included small samples of patients. In addition, studies that failed to find an enhancement effect in AD used stimuli lacking semantic coherence (e.g. lists of unrelated words, some that were emotional and others that were neutral). To circumvent these limitations, the present study examined a large number of AD patients (N = 80) and investigated whether AD patients would show better memory for a verbal description of an emotional event as compared to a neutral one. AD patients were equivalent to young and older control participants in rating the emotional descriptions for valence and arousal. Unlike the control groups, however, memory in AD patients did not benefit from the emotional narratives. We conclude that AD disrupts memory enhancement for at least some types of verbal emotional information.
Memories for emotional autobiographical events following unilateral damage to medial temporal lobe
Brain, 2006
Abnormalities of both memory and emotion have been reported in patients with unilateral damage to the anteromedial temporal lobe, probably reflecting the functions of the amygdala and hippocampus in these processes. Emotion and memory are also known to interact: emotional experiences often leave remarkably durable autobiographical memories. To explore this interaction, and to extend prior studies to the domain of autobiographical memory, we investigated the recollection of real-life emotional events in patients with unilateral damage to the anteromedial temporal lobe. Twenty-three patients who had undergone unilateral temporal lobectomy for the treatment of epilepsy (12 left, 11 right) and 20 healthy comparison participants completed an emotional autobiographical memory test. Participants were asked to recollect their five most emotional memories from any time in their lives and then they completed a word-cued autobiographical memory task. Participants dated each memory and gave ratings on scales of pleasantness, intensity, significance, novelty, vividness and frequency of rehearsal. Left temporal lobectomy (LTL) and healthy comparison groups generated similar numbers of pleasant and unpleasant memories, whereas the right temporal lobectomy (RTL) group produced significantly fewer memories of unpleasant events (P < 0.01). When memories were further categorized according to pleasantness and intensity, the RTL group produced significantly fewer unpleasant/high intensity memories than the other groups (P < 0.01). All groups reported more memories from between the ages of 10 and 30 (the so-called autobiographical memory 'bump'). The results demonstrate a positive bias in the recollection of autobiographical memory following right-sided anteromedial temporal damage. This finding is consistent with the notion that the right, but not the left, anteromedial temporal lobe is involved in the retrieval of negatively valenced, high-intensity memories.