Memory retrieval is thought to involve the reactivation of encoding processes. Previous fMRI work has indicated that reactivation processes are modulated by the residual effects of the prior emotional encoding context; different spatial patterns emerge during retrieval of memories previously associated with negative compared with positive or neutral context. Other research suggests that event-related potential (ERP) indicators of memory retrieval processes, like the left parietal old/new effect, can also be modulated by emotional context, but the spatial distribution and temporal dynamics of these effects are unclear. In the current study, we examined “when” emotion affects recognition memory and whether that timing reflects processes that come before and may guide successful retrieval or postrecollection recovery of emotional episodic detail. While recording EEG, participants ( n = 25) viewed neutral words paired with negative, positive, or neutral pictures during encoding, followed by a recognition test for the words. Analyses focused on ERPs during the recognition test. In line with prior ERP studies, we found an early positive-going parietally distributed effect starting around 200 msec after retrieval-cue onset. This effect emerged for words that had been encoded in an emotional compared with neutral context (no valence differences), before the general old/new effect. This emotion-dependent effect occurred in an early time window, suggesting that emotion-related reactivation is a precursor to successful recognition.

Most studies using a recognition memory paradigm examine the neural processes that support the ability to consciously recognize past events. However, there can also be nonconscious influences from the prior study episode that reflect repetition suppression effects—a reduction in the magnitude of activity for repeated presentations of stimuli—that are revealed by comparing neural activity associated with forgotten items to correctly rejected novel items. The present fMRI study examined the effect of emotional valence (positive vs. negative) on repetition suppression effects. Using a standard recognition memory task, 24 participants viewed line drawings of previously studied negative, positive, and neutral photos intermixed with novel line drawings. For each item, participants made an old–new recognition judgment and a sure–unsure confidence rating. Collapsed across valence, repetition suppression effects were found in ventral occipital-temporal cortex and frontal regions. Activity levels in the majority of these regions were not modulated by valence. However, repetition enhancement of the amygdala and ventral occipital-temporal cortex functional connectivity reflected nonconscious memory for negative items. In this study, valence had little effect on activation patterns but had a larger effect on functional connectivity patterns that were markers of nonconscious memory. Beyond memory and emotion, these findings are relevant to other cognitive and social neuroscientists that utilize fMRI repetition effects to investigate perception, attention, social cognition, and other forms of learning and memory.

Successful retrieval of an event includes an initial search phase in which the information is accessed and a subsequent elaboration phase in which an individual expands on event details. Traditionally, functional neuroimaging studies examining episodic memory retrieval either have not made a distinction between these two phases or have focused on the initial search process. The current study used an extended retrieval trial to compare the neural correlates of search and elaboration and to examine the effects of emotion on each phase. Before scanning, participants encoded positive, negative, and neutral images paired with neutral titles. After a 30-min delay, participants engaged in a scanned recognition task in which they viewed the neutral titles and indicated whether the title had been presented with an image during the study phase. Retrieval was divided into an initial memory search and a subsequent 5-sec elaboration phase. The current study identified neural differences between the search and elaboration phases, with search being associated with widespread bilateral activations across the entire cortex and elaboration primarily being associated with increased activity in the medial pFC. The emotionality of the retrieval target was more influential during search relative to elaboration. However, valence influenced when the effect of emotion was greatest, with search engaging many more regions for positive events than negative ones, but elaboration engaging the dorsomedial pFC more for negative events than positive events.

We used fMRI to investigate the neural processes engaged as individuals down- and up-regulated the emotions associated with negative autobiographical memories (AMs) using cognitive reappraisal strategies. Our analyses examined neural activity during three separate phases, as participants (a) viewed a reappraisal instruction (i.e., Decrease, Increase, Maintain), (b) searched for an AM referenced by a self-generated cue, and (c) elaborated upon the details of the AM being held in mind. Decreasing emotional intensity primarily engaged activity in regions previously implicated in cognitive control (e.g., dorsal and ventral lateral pFC), emotion generation and processing (e.g., amygdala, insula), and visual imagery (e.g., precuneus) as participants searched for and retrieved events. In contrast, increasing emotional intensity engaged similar regions during the instruction phase (i.e., before a memory cue was presented) and again as individuals later elaborated upon the details of the events they had recalled. These findings confirm that reappraisal can modulate neural activity during the recall of personally relevant events, although the time course of this modulation appears to depend on whether individuals are attempting to down- or up-regulate their emotions.

After information is encoded into memory, it undergoes an off-line period of consolidation that may occur optimally during sleep. The consolidation process not only solidifies memories but also changes them in useful and adaptive ways. Here, we provide evidence for a shift in the neural structures used to retrieve emotional memories after a night of sleep compared to a day of wakefulness. Although the hippocampus was activated during successful retrieval of negative objects regardless of whether participants slept during a delay, sleep led to a shift from engagement of a diffuse memory retrieval network—including widespread activity in the lateral prefrontal and parietal cortices—to a more refined network of regions—including the amygdala and ventromedial pFC. Effective connectivity analyses revealed stronger connections among limbic regions after sleep versus wake. Although circadian effects may have contributed to these findings, our data strongly suggest that a night of sleep is sufficient to evoke qualitative changes in the emotional memory retrieval network.

Human behavioral studies demonstrate that healthy aging is often accompanied by increases in memory distortions or errors. Here we used event-related fMRI to examine the neural basis of age-related memory distortions. We used the memory conjunction error paradigm, a laboratory procedure known to elicit high levels of memory errors. For older adults, right parahippocampal gyrus showed significantly greater activity during false than during accurate retrieval. We observed no regions in which activity was greater during false than during accurate retrieval for young adults. Young adults, however, showed significantly greater activity than old adults during accurate retrieval in right hippocampus. By contrast, older adults demonstrated greater activity than young adults during accurate retrieval in right inferior and middle prefrontal cortex. These data are consistent with the notion that age-related memory conjunction errors arise from dysfunction of hippocampal system mechanisms, rather than impairments in frontally mediated monitoring processes.

Young and older adults are more likely to remember emotional information than neutral information. The present functional magnetic resonance imaging study examined the neural processes supporting young (ages 18–35) and older (ages 62–79) adults' successful encoding of positive, negative, and neutral objects (e.g., a sundae, a grenade, a canoe). The results revealed general preservation of the emotional memory network across the age groups. Both groups recruited the amygdala and the orbito-frontal cortex during the successful encoding of positive and negative information. Both ages also showed valence-specific recruitment: right fusiform activity was greatest during the successful encoding of negative information, whereas left prefrontal and temporal activity was greatest during the successful encoding of positive information. These valence-specific processes are consistent with behavioral evidence that negative information is processed with perceptual detail, whereas positive information is processed at a conceptual or schematic level. The only age differences in emotional memory emerged during the successful encoding of positive items: Older adults showed more activity in the medial prefrontal cortex and along the cingulate gyrus than young adults. Because these regions often are associated with self-referential processing, these results suggest that older adults' mnemonic boost for positive information may stem from an increased tendency to process this information in relation to themselves.

Some studies have suggested that emotion primarily increases memory for “gist,” and does not enhance memory for detail. There are, however, some instances in which negative objects (e.g., snake, grenade) are remembered with more visual detail than neutral objects (e.g., barometer, blender). In the present functional magnetic resonance imaging (fMRI) study, we examined the encoding processes that lead a person to remember the exact visual details of negative and neutral objects, and to remember which of two decisions were made about the objects (a size decision or an animacy decision). The enhancement in memory for a negative item's visual details appeared to result from enhanced visual processing: The right fusiform gyrus, a region known to be critical for processing exemplar-specific details, showed a greater extent and magnitude of activity during the successful encoding of negative objects. Activity in the right amygdala also corresponded with memory for visual detail, although it did not relate to memory for the task performed with the item. These data provide strong evidence that engagement of some amygdalar regions can correspond with enhanced memory for certain types of details, but does not ensure successful encoding of all contextual details.

According to the distinctiveness heuristic, subjects rely more on detailed recollections (and less on familiarity) when memory is tested for pictures relative to words, leading to reduced false recognition. If so, then neural regions that have been implicated in effortful postretrieval monitoring (e.g., dorsolateral prefrontal cortex) might be recruited less heavily when trying to remember pictures. We tested this prediction with the criterial recollection task. Subjects studied black words, paired with either the same word in red font or a corresponding colored picture. Red words were repeated at study to equate recognition hits for red words and pictures. During fMRI scanning, alternating red word memory tests and picture memory tests were given, using only white words as test stimuli (say “yes” only if you recollect a corresponding red word or picture, respectively). These tests were designed so that subjects had to rely on memory for the criterial information. Replicating prior behavioral work, we found enhanced rejection of lures on the picture test compared to the red word test, indicating that subjects had used a distinctiveness heuristic. Critically, dorsolateral prefrontal activity was reduced when rejecting familiar lures on the picture test, relative to the red word test. These findings indicate that reducing false recognition via the distinctiveness heuristic is not heavily dependent on frontally mediated postretrieval monitoring processes.