Biology subjects

Norman, K. A.

Publications and source records attributed to Norman, K. A..

17 recordsLinked to original sources

bioRxiv2018

Targeted memory reactivation during sleep elicits neural signals related to learning content

Reactivation of learning-related neural activity patterns is thought to drive memory stabilization. However, finding reliable, non-invasive, content-specific indicators of reactivation remains a central challenge. Here, we attempted to decode the content of reactivated memories in the electroencephalogram (EEG) during sleep. During encoding, human participants learned to associate spatial locations of visual objects with left- or right-hand movements, and each object was accompanied by an inherently related sound. During subsequent slow-wave sleep within an afternoon nap, we presented half of the sound cues that were associated (during wake) with left- and right-hand movements before bringing participants back for a final post-nap test. We trained a classifier on sleep EEG data (focusing on lateralized EEG features that discriminated left- vs. right-sided trials during wake) to predict learning content when we reactivated the memories during sleep. Discrimination performance was significantly above chance and predicted subsequent memory, supporting the idea that reactivation leads to memory stabilization. Moreover, these lateralized signals increased with post-cue spindle power, demonstrating that reactivation has a strong relationship with spindles. These results show that lateralized activity related to individual memories can be decoded from sleep EEG, providing an effective indicator of offline reactivation.

neuroscience↗

bioRxiv2018

Neurofeedback helps to reveal a relationship between context reinstatement and memory retrieval

Theories of mental context and memory posit that successful mental context reinstatement enables better retrieval of memories from the same context, at the expense of memories from other contexts. To test this hypothesis, we had participants study lists of words, interleaved with task-irrelevant images from one category (e.g., scenes). Following encoding, participants were cued to mentally reinstate the context associated with a particular list, by thinking about the images that had appeared between the words. We measured context reinstatement with fMRI, and related this to performance on a free recall test that followed immediately afterwards. To increase sensitivity, we used a closed-loop neurofeedback procedure, whereby higher levels of context reinstatement (measured neurally) elicited increased visibility of the images from the studied context onscreen. Our goal was to create a positive feedback loop that amplified small fluctuations in mental context reinstatement, making it easier to experimentally detect a relationship between context reinstatement and recall. As predicted, we found that higher levels of neural context reinstatement were associated with better recall of words from the reinstated context, and worse recall of words from a different context. In a second experiment, we assessed the role of neurofeedback in identifying this brain-behavior relationship by presenting context images again but manipulating whether their visibility depended on neural context reinstatement. When neurofeedback was removed, the relationship between context reinstatement and memory retrieval disappeared. Together, these findings demonstrate a clear effect of context reinstatement on memory recall and suggest that neurofeedback can be a useful tool for characterizing brain-behavior relationships.\n\nAbbreviated titleNeurofeedback context

neuroscience↗

bioRxiv2018

Reductions in Retrieval Competition Predict the Benefit of Repeated Testing

Repeated testing leads to improved long-term memory retention compared to repeated study, but the mechanism underlying this improvement remains controversial. In this work, we test the hypothesis that retrieval practice benefits subsequent recall by reducing competition from related memories. This hypothesis implies that the degree of reduction in competition between retrieval practice attempts should predict subsequent memory for practiced items. To test this prediction, we collected electroencephalography (EEG) data across two sessions. In the first session, participants practiced selectively retrieving exemplars from superordinate semantic categories (high competition), as well as retrieving the names of the superordinate categories from exemplars (low competition). In the second session, participants repeatedly studied and were tested on Swahili-English vocabulary. One week after session two, participants were again tested on the vocabulary. We trained a within-subject classifier on the data from session one to distinguish high and low competition states.We then used this classifier to measure competition across multiple retrieval practice attempts in the second session. The degree to which competition decreased for a given vocabulary word predicted whether that item was subsequently remembered in the third session. These results are consistent with the hypothesis that repeated testing improves retention by reducing competition.

neuroscience↗

bioRxiv2018

Representation of real-world event schemas during narrative perception

Understanding movies and stories requires maintaining a high-level situation model that abstracts away from perceptual details to describe the location, characters, actions, and causal relationships of the currently unfolding event. These models are built not only from information present in the current narrative, but also from prior knowledge about schematic event scripts, which describe typical event sequences encountered throughout a lifetime. We analyzed fMRI data from 44 human subjects presented with sixteen three-minute stories, consisting of four schematic events drawn from two different scripts (eating at a restaurant or going through the airport). Aside from this shared script structure, the stories varied widely in terms of their characters and storylines, and were presented in two highly dissimilar formats (audiovisual clips or spoken narration). One group was presented with the stories in an intact temporal sequence, while a separate control group was presented with the same events in scrambled order. Regions including the posterior medial cortex, medial prefrontal cortex (mPFC), and superior frontal gyrus exhibited schematic event patterns that generalized across stories, subjects, and modalities. Patterns in mPFC were also sensitive to overall script structure, with temporally scrambled events evoking weaker schematic representations. Using a Hidden Markov Model, patterns in these regions can predict the script (restaurant vs. airport) of unlabeled data with high accuracy, and can be used to temporally align multiple stories with a shared script. These results extend work on the perception of controlled, artificial schemas in human and animal experiments to naturalistic perception of complex narrative stimuli.\n\nSignificance StatementIn almost all situations we encounter in our daily lives, we are able to draw on our schematic knowledge about what typically happens in the world to better perceive and mentally represent our ongoing experiences. In contrast to previous studies that investigated schematic cognition using simple, artificial associations, we measured brain activity from subjects watching movies and listening to stories depicting restaurant or airport experiences. Our results reveal a network of brain regions that is sensitive to the shared temporal structure of these naturalistic situations. These regions abstract away from the particular details of each story, activating a representation of the general type of situation being perceived.

neuroscience↗

bioRxiv2017

Sleep spindle refractoriness segregates periods of memory reactivation

The stability of long-term memories is enhanced by reactivation during sleep. Correlative evidence has linked memory reactivation with thalamocortical sleep spindles, although their functional role is poorly understood. Our initial study replicated this correlation but also demonstrated a novel rhythmicity to spindles, such that spindles are less likely to occur immediately following other spindles. We leveraged this rhythmicity to test the role of spindles in memory by using real-time spindle tracking to present cues inside versus outside the presumptive refractory period; as predicted, cues presented in the refractory period led to better memory. Our findings reveal a previously undescribed neural mechanism whereby spindles segment sleep into two distinct substates: prime opportunities for reactivation and gaps that segregate reactivation events.\n\nOne Sentence SummaryThe characteristic timing of sleep spindles regulates when memories can be reactivated during sleep.

neuroscience↗

bioRxiv2017

Offline Replay Supports Planning: fMRI Evidence from Reward Revaluation

Making decisions in sequentially structured tasks requires integrating distally acquired information. The extensive computational cost of such integration challenges planning methods that integrate online, at decision time. Furthermore, it remains unclear whether \"offline\" integration during replay supports planning, and if so which memories should be replayed. Inspired by machine learning, we propose that (a) offline replay of trajectories facilitates integrating representations that guide decisions, and (b) unsigned prediction errors (uncertainty) trigger such integrative replay. We designed a 2-step revaluation task for fMRI, whereby participants needed to integrate changes in rewards with past knowledge to optimally replan decisions. As predicted, we found that (a) multi-voxel pattern evidence for off-task replay predicts subsequent replanning; (b) neural sensitivity to uncertainty predicts subsequent replay and replanning; (c) off-task hippocampus and anterior cingulate activity increase when revaluation is required. These findings elucidate how the brain leverages offline mechanisms in planning and goal-directed behavior under uncertainty.

neuroscience↗

bioRxiv2017

Perceptual decisions result from the continuous accumulation of memory and sensory evidence

Expectations can inform fast, accurate decisions. But what informs expectations? Here we test the hypothesis that expectations are set by dynamic inference from memory. Participants performed a cue-guided perceptual decision task with independently-varying memory and sensory evidence. Cues established expectations by reminding participants of past stimulus-stimulus pairings, which predicted the likely target in a subsequent noisy image stream. Participants responses used both memory and sensory information, in accordance to their relative reliability. Formal model comparison showed that the sensory inference was best explained when its parameters were set dynamically at each trial by evidence sampled from memory. Supporting this model, neural pattern analysis revealed that responses to the probe were modulated by the specific content and fidelity of memory reinstatement that occurred before the probe appeared. Together, these results suggest that perceptual decisions arise from the continuous sampling of memory and sensory evidence.

neuroscience↗

bioRxiv2017

Human hippocampal replay during rest prioritizes weakly-learned information and predicts memory performance

There is now extensive evidence that the hippocampus replays experiences during quiet rest periods, and that this replay benefits subsequent memory. A critical open question is how memories are prioritized for replay during these offline periods. We addressed this question in an experiment in which participants learned the features of 15 objects and then underwent fMRI scanning to track item-level replay in the hippocampus using pattern analysis during a rest period. Objects that were remembered less well were replayed more during the subsequent rest period, suggesting a prioritization process in which weaker memories--memories most vulnerable to forgetting--are selected for wake replay. Participants came back for a second session, either after a night of sleep or a day awake, and underwent another scanned rest period followed by a second memory test. In the second session, more hippocampal replay of a satellite during the rest period predicted better subsequent memory for that satellite. Only in the group with intervening sleep did rest replay predict improvement from the first to second session. Our results provide the first evidence that replay of individual memories occurs during rest in the human hippocampus and that this replay prioritizes weakly learned information, predicts subsequent memory performance, and relates to memory improvement across a delay with sleep.

neuroscience↗

bioRxiv2017

Refresh my memory: Episodic memory reinstatements intrude on working memory maintenance

A fundamental question in memory research is how different forms of memory interact. Previous research has shown that people rely on working memory (WM) in short-term recognition tasks; a common view is that episodic memory (EM) only influences performance on these tasks when WM maintenance is disrupted. However, retrieval of memories from EM has been widely observed during brief periods of quiescence, raising the possibility that EM retrievals during maintenance-critically, before a response can be prepared-might affect short-term recognition memory performance even in the absence of distraction. We hypothesized that this influence would be mediated by the lingering presence of reactivated EM content in WM. We obtained support for this hypothesis in three experiments, showing that delay-period EM reactivation introduces incidentally-associated information (context) into WM, and that these retrieved associations negatively impact subsequent recognition, leading to substitution errors (Experiment 1) and slowing of accurate responses (Experiment 2). fMRI pattern analysis showed that slowing is mediated by the content of EM reinstatement (Experiment 3). These results expose a previously hidden influence of EM on WM, raising new questions about the adaptive nature of their interaction.

animal behavior and cognition↗

bioRxiv2017

Sleep Benefits Memory For Semantic Category Structure While Preserving Exemplar-Specific Information

Semantic memory encompasses knowledge about both the properties that typify concepts (e.g. robins, like all birds, have wings) as well as the properties that individuate conceptually related items (e.g. robins, in particular, have red breasts). We investigate the impact of sleep on new semantic learning using a property inference task in which both kinds of information are initially acquired equally well. Participants learned about three categories of novel objects possessing some properties that were shared among category exemplars and others that were unique to an exemplar, with exposure frequency varying across categories. In Experiment 1, memory for shared properties improved and memory for unique properties was preserved across a night of sleep, while memory for both feature types declined over a day awake. In Experiment 2, memory for shared properties improved across a nap, but only for the lower-frequency category, suggesting a prioritization of weakly learned information early in a sleep period. The increase was significantly correlated with amount of REM, but was also observed in participants who did not enter REM, suggesting involvement of both sleep stages. The results provide the first evidence that sleep improves memory for the shared structure of object categories, while simultaneously preserving object-unique information.

neuroscience↗

bioRxiv2017

Neural Overlap In Item Representations Across Episodes Impairs Context Memory

We frequently encounter the same item in different contexts, and when that happens, memories of earlier encounters can get reactivated in the brain. Here we examined how these existing memories are changed as a result of such reactivation. We hypothesized that when an items initial and subsequent neural representations overlap, this allows the initial item to become associated with novel contextual information, interfering with later retrieval of the initial context. That is, we predicted a negative relationship between representational similarity across repeated experiences of an item and subsequent source memory for the initial context. We tested this hypothesis in an fMRI study, in which objects were presented multiple times during different tasks. We measured the similarity of the neural patterns in lateral occipital cortex that were elicited by the first and second presentations of objects, and related this neural overlap score to source memory in a subsequent test. Consistent with our hypothesis, greater item-specific pattern similarity was linked to worse source memory for the initial task. Our findings suggest that the influence of novel experiences on an existing context memory depends on how reliably a shared component (i.e., same item) is represented across these episodes.

neuroscience↗

bioRxiv2017

Dissociable effects of surprising rewards on learning and memory

The extent to which rewards deviate from learned expectations is tracked by a signal known as a \"reward prediction error\", but it is unclear how this signal interacts with episodic memory. Here, we investigated whether learning in a high-risk environment, with frequent large prediction errors, gives rise to higher fidelity memory traces than learning in a low-risk environment. In Experiment 1, we showed that higher magnitude prediction errors, positive or negative, improved recognition memory for trial-unique items. Participants also increased their learning rate after large prediction errors. In addition, there was an overall higher learning rate in the low-risk environment. Although unsigned prediction errors enhanced memory and increased learning rate, we did not find a relationship between learning rate and memory, suggesting that these two effects were due to separate underlying mechanisms. In Experiment 2, we replicated these results with a longer task that posed stronger memory demands and allowed for more learning. We also showed improved source and sequence memory for high-risk items. In Experiment 3, we controlled for the difficulty of learning in the two risk environments, again replicating the previous results. Moreover, equating the range of prediction errors in the two risk environments revealed that learning in a high-risk context enhanced episodic memory above and beyond the effect of prediction errors to individual items. In summary, our results across three studies showed that (absolute) prediction error magnitude boosted both episodic memory and incremental learning, but the two effects were not correlated, suggesting distinct underlying systems.

animal behavior and cognition↗

bioRxiv2017

Parametrically scalable memory reactivation using multiple object tracking

Converging evidence supports the \"non-monotonic plasticity\" hypothesis that although complete retrieval may strengthen memories, partial retrieval weakens them. Yet, the classic experimental paradigms used to study effects of partial retrieval are not ideally suited to doing so, because they lack the parametric control needed to ensure that the memory is activated to the appropriate degree (i.e., that there is some retrieval, but not enough to cause memory strengthening). Here we present a novel procedure designed to accommodate this need. After participants learned a list of word-scene associates, they completed a cued mental visualization task that was combined with a multiple-object tracking (MOT) procedure, which we selected for its ability to interfere with mental visualization in a parametrically adjustable way (by varying the number of MOT targets). We also used fMRI data to successfully train an \"associative recall\" classifier for use in this task: this classifier revealed greater memory reactivation during trials in which associative memories were cued while participants tracked one, rather than five MOT targets. However, the classifier was insensitive to task difficulty when recall was not taking place, suggesting it had indeed tracked memory reactivation rather than task difficulty per se. Consistent with the classifier findings, participants' introspective ratings of visualization vividness were modulated by task difficulty. In addition, classifier output and slowing of responses in a post-reactivation memory test suggested that partial reactivation, induced by MOT, weakened memory. We argue that this procedure has desirable properties for future investigation of partial retrieval effects, e.g., in closed-loop experiments.

neuroscience↗

bioRxiv2017

A probabilistic approach to discovering dynamic full-brain functional connectivity patterns

Recent research shows that the covariance structure of functional magnetic resonance imaging (fMRI) data - commonly described as functional connectivity - can change as a function of the participants cognitive state (for review see [35]). Here we present a Bayesian hierarchical matrix factorization model, termed hierarchical topographic factor analysis (HTFA), for efficiently discovering full-brain networks in large multi-subject neuroimaging datasets. HTFA approximates each subjects network by first re-representing each brain image in terms of the activities of a set of localized nodes, and then computing the covariance of the activity time series of these nodes. The number of nodes, along with their locations, sizes, and activities (over time) are learned from the data. Because the number of nodes is typically substantially smaller than the number of fMRI voxels, HTFA can be orders of magnitude more efficient than traditional voxel-based functional connectivity approaches. In one case study, we show that HTFA recovers the known connectivity patterns underlying a collection of synthetic datasets. In a second case study, we illustrate how HTFA may be used to discover dynamic full-brain activity and connectivity patterns in real fMRI data, collected as participants listened to a story. In a third case study, we carried out a similar series of analyses on fMRI data collected as participants viewed an episode of a television show. In these latter case studies, we found that the HTFA-derived activity and connectivity patterns can be used to reliably decode which moments in the story or show the participants were experiencing. Further, we found that these two classes of patterns contained partially non-overlapping information, such that decoders trained on combinations of activity-based and dynamic connectivity-based features performed better than decoders trained on activity or connectivity patterns alone. We replicated this latter result with two additional (previously developed) methods for efficiently characterizing full-brain activity and connectivity patterns.

neuroscience↗

bioRxiv2016

Neural differentiation of incorrectly predicted memories

When an item is predicted in a particular context but the prediction is violated, memory for that item is weakened (Kim et al., 2014). Here we explore what happens when such previously mispredicted items are later re-encountered. According to prior neural network simulations, this sequence of events - misprediction and subsequent restudy - should lead to differentiation of the item's neural representation from the previous context (on which the misprediction was based). Specifically, misprediction weakens connections in the representation to features shared with the previous context, and restudy allows new features to be incorporated into the representation that are not shared with the previous context. This cycle of misprediction and restudy should have the net effect of moving the item s neural representation away from the neural representation of the previous context. We tested this hypothesis using fMRI, by tracking changes in item-specific BOLD activity patterns in the hippocampus, a key structure for representing memories and generating predictions. In left CA2/3/DG, we found greater neural differentiation for items that were repeatedly mispredicted and restudied compared to items from a control condition that was identical except without misprediction. We also measured prediction strength in a trial-by-trial fashion and found that greater misprediction for an item led to more differentiation, further supporting our hypothesis. Thus, the consequences of prediction error go beyond memory weakening: If the mispredicted item is restudied, the brain adaptively differentiates its memory representation to improve the accuracy of subsequent predictions and to shield it from further weakening.\n\nSignificanceCompetition between overlapping memories leads to weakening of non-target memories over time, making it easier to access target memories. However, a non-target memory in one context might become a target memory in another context. How do such memories get re-strengthened without increasing competition again? Computational models suggest that the brain handles this by reducing neural connections to the previous context and adding connections to new features that were not part of the previous context. The result is neural differentiation away from the previous context. Here provide support for this theory, using fMRI to track neural representations of individual memories in the hippocampus and how they change based on learning.

neuroscience↗

bioRxiv2016

How we transmit memories to other brains: constructing shared neural representations via communication

It is striking that humans are able to encode and later verbally share their memories of an episode with listeners, who are in turn able to imagine (mentally construct) details of the episode which they have not personally experienced. However, it is unknown how strongly the neural patterns elicited by imagining specific episodes resemble the neural states elicited during the original encoding of those episodes. In the current study, using fMRI and a natural communication task, we traced how neural patterns associated with specific scenes depicted in a movie are encoded, verbally recalled, and then transferred to a group of naive listeners who construct the scenes of the movie in their imagination. By comparing neural patterns across the three conditions, we report, for the first time, that event-specific neural patterns are observed in the default mode network (DMN) and shared across the encoding, reinstatement (spoken recall), and new construction (imagination) of the same real-life episode. This study uncovers the intimate correspondences between memory encoding and imagination, and highlights the essential role that our common language plays in the process of transmitting ones experiences to other brains.

neuroscience↗

bioRxiv2016

Discovering event structure in continuous narrative perception and memory

SummaryDuring realistic, continuous perception, humans automatically segment experiences into discrete events. Using a novel model of neural event dynamics, we investigate how cortical structures generate event representations during continuous narratives, and how these events are stored and retrieved from long-term memory. Our data-driven approach enables identification of event boundaries and event correspondences across datasets without human-generated stimulus annotations, and reveals that different regions segment narratives at different timescales. We also provide the first direct evidence that narrative event boundaries in high-order areas (overlapping the default mode network) trigger encoding processes in the hippocampus, and that this encoding activity predicts pattern reinstatement during recall. Finally, we demonstrate that these areas represent abstract, multimodal situation models, and show anticipatory event reinstatement as subjects listen to a familiar narrative. Our results provide strong evidence that brain activity is naturally structured into semantically meaningful events, which are stored in and retrieved from long-term memory.

neuroscience↗