The Neural Basis of Involuntary Episodic Memories

Involuntary episodic memories are memories that come into consciousness without preceding retrieval effort. These memories are commonplace and are relevant to multiple mental disorders. However, they are vastly understudied. We use a novel paradigm to elicit involuntary memories in the laboratory so that we can study their neural basis. In session one, an encoding session, sounds are presented with picture pairs or alone. In session two, in the scanner, sounds-picture pairs and unpaired sounds are reencoded. Immediately following, participants are split into two groups: a voluntary and an involuntary group. Both groups perform a sound localization task in which they hear the sounds and indicate the side from which they are coming. The voluntary group additionally tries to remember the pictures that were paired with the sounds. Looking at neural activity, we find a main effect of condition (paired vs. unpaired sounds) showing similar activity in both groups for voluntary and involuntary memories in regions typically associated with retrieval. There is also a main effect of group (voluntary vs. involuntary) in the dorsolateral prefrontal cortex, a region typically associated with cognitive control. Turning to connectivity similarities and differences between groups again, there is a main effect of condition showing paired > unpaired sounds are associated with a recollection network. In addition, three group differences were found: (1) increased connectivity between the pulvinar nucleus of the thalamus and the recollection network for the voluntary group, (2) a higher association between the voluntary group and a network that includes regions typically found in frontoparietal and cingulo-opercular networks, and (3) shorter path length for about half of the nodes in these networks for the voluntary group. Finally, we use the same paradigm to compare involuntary memories in people with posttraumatic stress disorder (PTSD) to trauma-controls. This study also included the addition of emotional pictures. There were two main findings. (1) A similar pattern of activity was found for paired > unpaired sounds for both groups but this activity was delayed in the PTSD group. (2) A similar pattern of activity was found for high > low emotion stimuli but it occurred early in the PTSD group compared to the control group. Our results suggest that involuntary and voluntary memories share the same neural representation but that voluntary memories are associated with additional cognitive control processes. They also suggest that disorders associated with cognitive deficits, like PTSD, can affect the processing of involuntary memories.

Functional neuroimaging of autobiographical memory.

Functional neuroimaging studies of autobiographical memory have grown dramatically in recent years. These studies are important because they can investigate the neural correlates of processes that are difficult to study using laboratory stimuli, including: (i) complex constructive processes, (ii) recollective qualities of emotion and vividness, and (iii) remote memory retrieval. Constructing autobiographical memories involves search, monitoring and self-referential processes that are associated with activity in separable prefrontal regions. The contributions of emotion and vividness have been linked to the amygdala and visual cortex respectively. Finally, there is evidence that recent and remote autobiographical memories might activate the hippocampus equally, which has implications for memory-consolidation theories. The rapid development of innovative methods for eliciting personal memories in the scanner provides the opportunity to delve into the functional neuroanatomy of our personal past.

Effects of priming duration on retention over the first 1 1/2 years of life.

Exposing individuals to an isolated component (a prime) of a prior event alleviates its forgetting. Two experiments with 120 human infants between 3 and 18 months of age determined the minimum duration of a prime that can reactivate a forgotten memory and how long the reactivated memory persists. Infants learned an operant task, forgot it, were exposed to the prime, and later were tested for renewed retention. In Experiment 1, the minimum duration of an effective prime decreased logarithmically with age, but was always longer than the duration of a mere glance. In Experiment 2, the reactivated memory was forgotten twice as fast after a minimum-duration prime as after a full-length one, irrespective of priming delay and infant age. These data reveal that the minimum effective prime duration psychophysically equates the accessibility of forgotten memories. We conclude that priming is perceptually based with effects that are organized on a ratio (log) scale.

Effects of task instruction on autobiographical memory specificity in young and older adults

Older adults tend to retrieve autobiographical information that is overly general (i.e., not restricted to a single event, termed the overgenerality effect) relative to young adults' specific memories. A vast majority of studies that have reported overgenerality effects explicitly instruct participants to retrieve specific memories, thereby requiring participants to maintain task goals, inhibit inappropriate responses, and control their memory search. Since these processes are impaired in healthy ageing, it is important to determine whether such task instructions influence the magnitude of the overgenerality effect in older adults. In the current study participants retrieved autobiographical memories during presentation of musical clips. Task instructions were manipulated to separate age-related differences in the specificity of underlying memory representations from age-related differences in following task instructions. Whereas young adults modulated memory specificity based on task demands, older adults did not. These findings suggest that reported rates of overgenerality in older adults' memories might include age-related differences in memory representation, as well as differences in task compliance. Such findings provide a better understanding of the underlying cognitive mechanisms involved in age-related changes in autobiographical memory and may also be valuable for future research examining effects of overgeneral memory on general well-being. © 2013 Taylor & Francis.

Neural networks supporting autobiographical memory retrieval in posttraumatic stress disorder.

Posttraumatic stress disorder (PTSD) affects the functional recruitment and connectivity between neural regions during autobiographical memory (AM) retrieval that overlap with default and control networks. Whether such univariate changes relate to potential differences in the contributions of the large-scale neural networks supporting cognition in PTSD is unknown. In the present functional MRI study, we employed independent-component analysis to examine the influence of the engagement of neural networks during the recall of personal memories in a PTSD group (15 participants) as compared to non-trauma-exposed healthy controls (14 participants). We found that the PTSD group recruited similar neural networks when compared to the controls during AM recall, including default-network subsystems and control networks, but group differences emerged in the spatial and temporal characteristics of these networks. First, we found spatial differences in the contributions of the anterior and posterior midline across the networks, and of the amygdala in particular, for the medial temporal subsystem of the default network. Second, we found temporal differences within the medial prefrontal subsystem of the default network, with less temporal coupling of this network during AM retrieval in PTSD relative to controls. These findings suggest that the spatial and temporal characteristics of the default and control networks potentially differ in a PTSD group versus healthy controls and contribute to altered recall of personal memory.

Effects of task instruction on autobiographical memory specificity in young and older adults.

Older adults tend to retrieve autobiographical information that is overly general (i.e., not restricted to a single event, termed the overgenerality effect) relative to young adults' specific memories. A vast majority of studies that have reported overgenerality effects explicitly instruct participants to retrieve specific memories, thereby requiring participants to maintain task goals, inhibit inappropriate responses, and control their memory search. Since these processes are impaired in healthy ageing, it is important to determine whether such task instructions influence the magnitude of the overgenerality effect in older adults. In the current study participants retrieved autobiographical memories during presentation of musical clips. Task instructions were manipulated to separate age-related differences in the specificity of underlying memory representations from age-related differences in following task instructions. Whereas young adults modulated memory specificity based on task demands, older adults did not. These findings suggest that reported rates of overgenerality in older adults' memories might include age-related differences in memory representation, as well as differences in task compliance. Such findings provide a better understanding of the underlying cognitive mechanisms involved in age-related changes in autobiographical memory and may also be valuable for future research examining effects of overgeneral memory on general well-being.

Age-related effects on the neural correlates of autobiographical memory retrieval.

Older adults recall less episodically rich autobiographical memories (AM), however, the neural basis of this effect is not clear. Using functional MRI, we examined the effects of age during search and elaboration phases of AM retrieval. Our results suggest that the age-related attenuation in the episodic richness of AMs is associated with difficulty in the strategic retrieval processes underlying recovery of information during elaboration. First, age effects on AM activity were more pronounced during elaboration than search, with older adults showing less sustained recruitment of the hippocampus and ventrolateral prefrontal cortex (VLPFC) for less episodically rich AMs. Second, there was an age-related reduction in the modulation of top-down coupling of the VLPFC on the hippocampus for episodically rich AMs. In sum, the present study shows that changes in the sustained response and coupling of the hippocampus and prefrontal cortex (PFC) underlie age-related reductions in episodic richness of the personal past.

The reminiscence bump in the temporal distribution of the best football players of all time: Pelé, Cruijff or Maradona?

The reminiscence bump is the tendency to recall more autobiographical memories from adolescence and early adulthood than from adjacent lifetime periods. In this online study, the robustness of the reminiscence bump was examined by looking at participants' judgements about the quality of football players. Dutch participants (N = 619) were asked who they thought the five best players of all time were. The participants could select the names from a list or enter the names when their favourite players were not on the list. Johan Cruijff, Pelé, and Diego Maradona were the three most often mentioned players. Participants frequently named football players who reached the midpoint of their career when the participants were adolescents (mode = 17). The results indicate that the reminiscence bump can also be identified outside the autobiographical memory domain.

Autobiographical memory for stressful events: the role of autobiographical memory in posttraumatic stress disorder.

To provide the three-way comparisons needed to test existing theories, we compared (1) most-stressful memories to other memories and (2) involuntary to voluntary memories (3) in 75 community dwelling adults with and 42 without a current diagnosis of posttraumatic stress disorder (PTSD). Each rated their three most-stressful, three most-positive, seven most-important and 15 word-cued autobiographical memories, and completed tests of personality and mood. Involuntary memories were then recorded and rated as they occurred for 2 weeks. Standard mechanisms of cognition and affect applied to extreme events accounted for the properties of stressful memories. Involuntary memories had greater emotional intensity than voluntary memories, but were not more frequently related to traumatic events. The emotional intensity, rehearsal, and centrality to the life story of both voluntary and involuntary memories, rather than incoherence of voluntary traumatic memories and enhanced availability of involuntary traumatic memories, were the properties of autobiographical memories associated with PTSD.

Remembering from any angle: the flexibility of visual perspective during retrieval.

When recalling autobiographical memories, individuals often experience visual images associated with the event. These images can be constructed from two different perspectives: first person, in which the event is visualized from the viewpoint experienced at encoding, or third person, in which the event is visualized from an external vantage point. Using a novel technique to measure visual perspective, we examined where the external vantage point is situated in third-person images. Individuals in two studies were asked to recall either 10 or 15 events from their lives and describe the perspectives they experienced. Wide variation in spatial locations was observed within third-person perspectives, with the location of these perspectives relating to the event being recalled. Results suggest remembering from an external viewpoint may be more common than previous studies have demonstrated.

The temporal distribution of autobiographical memory: changes in reliving and vividness over the life span do not explain the reminiscence bump.

When autobiographical memories are elicited with word cues, personal events from middle childhood to early adulthood are overrepresented compared to events from other periods. It is, however, unclear whether these memories are also associated with greater recollection. In this online study, we examined whether autobiographical memories from adolescence and early adulthood are recollected more than memories from other lifetime periods. Participants rated personal events that were elicited with cue words on reliving or vividness. Consistent with previous studies, most memories came from the period in which the participants were between 6 and 20 years old. The memories from this period were not relived more or recalled more vividly than memories from other lifetime periods, suggesting that they do not involve more recollection. Recent events had higher levels of reliving and vividness than remote events, and older adults reported a stronger recollective experience than younger adults.

A memory-based model of posttraumatic stress disorder: evaluating basic assumptions underlying the PTSD diagnosis.

In the mnemonic model of posttraumatic stress disorder (PTSD), the current memory of a negative event, not the event itself, determines symptoms. The model is an alternative to the current event-based etiology of PTSD represented in the Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; American Psychiatric Association, 2000). The model accounts for important and reliable findings that are often inconsistent with the current diagnostic view and that have been neglected by theoretical accounts of the disorder, including the following observations. The diagnosis needs objective information about the trauma and peritraumatic emotions but uses retrospective memory reports that can have substantial biases. Negative events and emotions that do not satisfy the current diagnostic criteria for a trauma can be followed by symptoms that would otherwise qualify for PTSD. Predisposing factors that affect the current memory have large effects on symptoms. The inability-to-recall-an-important-aspect-of-the-trauma symptom does not correlate with other symptoms. Loss or enhancement of the trauma memory affects PTSD symptoms in predictable ways. Special mechanisms that apply only to traumatic memories are not needed, increasing parsimony and the knowledge that can be applied to understanding PTSD.

Memory and coping with stress: the relationship between cognitive-emotional distinctiveness, memory valence, and distress.

Cognitive-emotional distinctiveness (CED), the extent to which an individual separates emotions from an event in the cognitive representation of the event, was explored in four studies. CED was measured using a modified multidimensional scaling procedure. The first study found that lower levels of CED in memories of the September 11 terrorist attacks predicted greater frequency of intrusive thoughts about the attacks. The second study revealed that CED levels are higher in negative events, in comparison to positive events and that low CED levels in emotionally intense negative events are associated with a pattern of greater event-related distress. The third study replicated the findings from the previous study when examining CED levels in participants' memories of the 2004 Presidential election. The fourth study revealed that low CED in emotionally intense negative events is associated with worse mental health. We argue that CED is an adaptive and healthy coping feature of stressful memories.

The spatiotemporal dynamics of autobiographical memory: neural correlates of recall, emotional intensity, and reliving.

We sought to map the time course of autobiographical memory retrieval, including brain regions that mediate phenomenological experiences of reliving and emotional intensity. Participants recalled personal memories to auditory word cues during event-related functional magnetic resonance imaging (fMRI). Participants pressed a button when a memory was accessed, maintained and elaborated the memory, and then gave subjective ratings of emotion and reliving. A novel fMRI approach based on timing differences capitalized on the protracted reconstructive process of autobiographical memory to segregate brain areas contributing to initial access and later elaboration and maintenance of episodic memories. The initial period engaged hippocampal, retrosplenial, and medial and right prefrontal activity, whereas the later period recruited visual, precuneus, and left prefrontal activity. Emotional intensity ratings were correlated with activity in several regions, including the amygdala and the hippocampus during the initial period. Reliving ratings were correlated with activity in visual cortex and ventromedial and inferior prefrontal regions during the later period. Frontopolar cortex was the only brain region sensitive to emotional intensity across both periods. Results were confirmed by time-locked averages of the fMRI signal. The findings indicate dynamic recruitment of emotion-, memory-, and sensory-related brain regions during remembering and their dissociable contributions to phenomenological features of the memories.