Commentary: Distinct neural mechanisms for remembering when an event occurred (original) (raw)
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Temporal memory is shaped by encoding stability and intervening item reactivation
The Journal of neuroscience : the official journal of the Society for Neuroscience, 2014
Making sense of previous experience requires remembering the order in which events unfolded in time. Prior work has implicated the hippocampus and medial temporal lobe cortex in memory for temporal information associated with individual episodes. However, the processes involved in encoding and retrieving temporal information across extended sequences is relatively poorly understood. Here we used fMRI during the encoding and retrieval of extended sequences to test specific predictions about the type of information used to resolve temporal order and the role of the hippocampus in this process. Participants studied sequences of images of celebrity faces and common objects followed by a recency discrimination test. The main conditions of interest were pairs of items that had been presented with three intervening items, half of which included an intervening category shift. During encoding, hippocampal pattern similarity across intervening items was associated with subsequent successful o...
2017
We examined the neurobiological basis of temporal resetting, an aspect of temporal order memory, using a version of the delayed-match-to-multiple-samples task. While in an fMRI scanner, participants evaluated whether an item was novel, or whether it had appeared before or after a reset event that signified the start of a new block of trials. Participants responded "old" to items that were repeated within the current block, and "new" to both novel items and to items that had last appeared before the reset event (pseudonew items). Medial temporal, prefrontal and occipital regions responded to absolute novelty of the stimulus-they differentiated between novel items and previously seen items, but not between old and pseudonew items. Activation for pseudonew items in the frontopolar and parietal regions, in contrast, was intermediate between old and new items. The posterior cingulate cortex extending to precuneus was the only region that showed complete temporal resetting and its activation reflected whether an item was new or old according to the task instructions regardless of its familiarity. There was also a significant Condition (old/pseudonew)-by-Familiarity (second/third presentations) interaction effect on behavioral and neural measures. For pseudonew items, greater familiarity decreased response accuracy, increased response times, increased anterior cingulate cortex (ACC) activation and increased functional connectivity between the ACC and the left frontal pole. The reverse was observed for old items. Based on these results, we propose a theoretical framework in which temporal resetting relies on an episodic retrieval network that is modulated by cognitive control and conflict resolution.
Cortical Networks Involved in Memory for Temporal Order
Journal of cognitive neuroscience, 2017
We examined the neurobiological basis of temporal resetting, an aspect of temporal order memory, using a version of the delayed-match-to-multiple-sample task. While in an fMRI scanner, participants evaluated whether an item was novel or whether it had appeared before or after a reset event that signified the start of a new block of trials. Participants responded "old" to items that were repeated within the current block and "new" to both novel items and items that had last appeared before the reset event (pseudonew items). Medial-temporal, prefrontal, and occipital regions responded to absolute novelty of the stimulus-they differentiated between novel items and previously seen items, but not between old and pseudonew items. Activation for pseudonew items in the frontopolar and parietal regions, in contrast, was intermediate between old and new items. The posterior cingulate cortex extending to precuneus was the only region that showed complete temporal resetting,...
Journal of Neuroscience, 2011
Episodic memory involves remembering the incidental order of a series of events that comprise a specific experience. Current models of temporal organization in episodic memory have demonstrated that animals can make memory judgments about the order of serially presented events; however, in these protocols, the animals can judge items based on their relative recency. Thus, it remains unclear as to whether animals use the specific order of items in forming memories of distinct sequences. To resolve this important issue in memory representation, we presented mice repeatedly with two widely separated odor sequences and then tested their natural exploratory preference between pairs of odors selected from within or between sequences. Intact animals preferred to investigate odors that occurred earlier within each sequence, indicating they did remember the order of events within each distinct sequence. In contrast, intact animals did not discriminate between pairs of odors from different sequences. These findings indicate that preferences were not guided by relative recency, which would be expected to support graded discrimination between widely separated events. Furthermore, damage to either the hippocampus or the medial prefrontal cortex eliminated order preference within sequences. Despite the deficit in order memory, control recognition tests showed that normal mice and mice with hippocampal or medial prefrontal damage could correctly identify previously experienced odors compared with novel odors. These findings provide strong evidence that animals form representations of the order of events within specific experiences and that the hippocampus and prefrontal cortex are essential to order memory.
The hippocampus, prefrontal cortex, and perirhinal cortex are critical to incidental order memory
Behavioural Brain Research, 2019
Considerable research in rodents and humans indicates the hippocampus and prefrontal cortex are essential for remembering temporal relationships among stimuli, and accumulating evidence suggests the perirhinal cortex may also be involved. However, experimental parameters differ substantially across studies, which limits our ability to fully understand the fundamental contributions of these structures. In fact, previous studies vary in the type of temporal memory they emphasize (e.g., order, sequence, or separation in time), the stimuli and responses they use (e.g., trial-unique or repeated sequences, and incidental or rewarded behavior), and the degree to which they control for potential confounding factors (e.g., primary and recency effects or order memory deficits secondary to item memory impairments). To help integrate these findings, we developed a new paradigm testing incidental memory for trial-unique series of events, and concurrently assessed order and item memory in animals with damage to the hippocampus, prefrontal cortex, or perirhinal cortex. We found that this new approach led to robust order and item memory, and that hippocampal, prefrontal and perirhinal damage selectively impaired order memory. These findings suggest the hippocampus, prefrontal cortex and perirhinal cortex are part of a broad network of structures essential for incidentally learning the order of events in episodic memory.
Dissecting medial temporal lobe contributions to item and associative memory formation
NeuroImage, 2009
A fundamental and intensively discussed question is whether medial temporal lobe (MTL) processes that lead to non-associative item memories differ in their anatomical substrate from processes underlying associative memory formation. Using event-related functional magnetic resonance imaging, we implemented a novel design to dissociate brain activity related to item and associative memory formation not only by subsequent memory performance and anatomy but also in time, because the two constituents of each pair to be memorized were presented sequentially with an intra-pair delay of several seconds. Furthermore, the design enabled us to reduce potential differences in memory strength between item and associative memory by increasing task difficulty in the item recognition memory test. Confidence ratings for correct item recognition for both constituents did not differ between trials in which only item memory was correct and trials in which item and associative memory were correct. Specific subsequent memory analyses for item and associative memory formation revealed brain activity that appears selectively related to item memory formation in the posterior inferior temporal, posterior parahippocampal, and perirhinal cortices. In contrast, hippocampal and inferior prefrontal activity predicted successful retrieval of newly formed inter-item associations. Our findings therefore suggest that different MTL subregions indeed play distinct roles in the formation of item memory and inter-item associative memory as expected by several dual process models of the MTL memory system.
A Specific Role of the Human Hippocampus in Recall of Temporal Sequences
Journal of Neuroscience, 2009
There is a growing interest in how temporal order of episodic memories is represented within the medial temporal lobe (MTL). Animal studies suggest that the hippocampal formation (HF) is critical for retrieving the temporal order of past experiences. However, human imaging studies that have tested recency discrimination between pairs of previously encoded items have generally failed to report HF activation. We hypothesized that recalling a naturalistic sequence of past events would be particularly sensitive to HF function, attributable to greater involvement of associative processes. To test this prediction, we let subjects watch a novel movie and later, during functional magnetic resonance imaging, asked them to rearrange and "replay" scenes from the movie in correct order. To identify areas specifically involved in retrieval of temporal order, we used a control condition where subjects logically inferred the order of scenes from the same movie. Extensive MTL activation was observed during sequence recall. Activation within the right HF was specifically related to retrieval of temporal order and correlated positively with accuracy of sequence recall. Also, the bilateral parahippocampal cortex responded to retrieval of temporal order, but the activation here was not related to performance. Our study is the first to unequivocally demonstrate that correct sequence recall depends on HF.
Lingering representations of stimuli influence recall organization
Neuropsychologia, 2017
Several prominent theories posit that information about recent experiences lingers in the brain and organizes memories for current experiences, by forming a temporal context that is linked to those memories at encoding. According to these theories, if the thoughts preceding an experience X resemble the thoughts preceding an experience Y, then X and Y should show an elevated probability of being recalled together. We tested this prediction by using multi-voxel pattern analysis (MVPA) of fMRI data to measure neural evidence for lingering processing of preceding stimuli. As predicted, memories encoded with similar lingering thoughts about the category of preceding stimuli were more likely to be recalled together. Our results demonstrate that the "fading embers" of previous stimuli help to organize recall, confirming a key prediction of computational models of episodic memory.
The Short and Long of It: Neural Correlates of Temporal-order Memory for Autobiographical Events
Journal of Cognitive Neuroscience, 2008
Previous functional neuroimaging studies of temporal-order memory have investigated memory for laboratory stimuli that are causally unrelated and poor in sensory detail. In contrast, the present functional MRI (fMRI) study investigated temporal-order memory for autobiographical events that were causally interconnected and rich in sensory detail. Participants took photographs at many campus locations over a period of several hours, and the following day they were scanned while making temporal-order judgments to pairs of photographs from different locations. By manipulating the temporal lag between the two locations in each trial, we compared the neural correlates associated with reconstruction processes, which we hypothesized depended on recollection and contribute mainly to short lags, and distance processes, which we hypothesized to depend on familiarity and contribute mainly to longer lags. Consistent with our hypotheses, parametric fMRI analyses linked shorter lags to activations in regions previously associated with recollection (left prefrontal, parahippocampal, precuneus, and visual cortices) and longer lags with regions previously associated with familiarity (right prefrontal cortex). The hemispheric asymmetry in prefrontal cortex activity fits very well with evidence and theories regarding the contributions of left vs. right prefrontal cortex to memory (recollection vs. familiarity processes) and cognition (systematic vs. heuristic processes). In sum, using a novel photo-paradigm this study provided the first evidence regarding the neural correlates of temporal-order for autobiographical events.
Brain activation in processing temporal sequence: an fMRI study
NeuroImage, 2004
Structured event complexes (SECs) are stored representations of sequential event knowledge, and represent sequences of activities that have been described elsewhere as scripts or schemas. Previous studies have shown that the prefrontal cortex is involved in temporal sequencing. The present study investigates the involvement of the prefrontal cortex in temporal order and membership judgments of script and category items by using functional magnetic resonance imaging. In this experiment, stimuli were either script events or category items. In experimental trials, subjects classified stimuli according to temporal order or membership category. Results show that the script order task and the chronological order task (relative to their respective memberships tasks) were associated with different patterns of PFC activation. Both order tasks activated the middle frontal gyrus bilaterally; however, script order tasks showed additional activation in right inferior frontal gyrus, and the chronological order tasks in left inferior frontal gyrus. These results suggest that while the middle frontal gyri are activated bilaterally in both script and chronological temporal ordering tasks, there are different, though largely overlapping, neural substrates for script and chronological representations during temporal ordering. Published by Elsevier Inc.