Decoding individual episodic memory traces in the human hippocampus.
ABSTRACT: In recent years, multivariate pattern analyses have been performed on functional magnetic resonance imaging (fMRI) data, permitting prediction of mental states from local patterns of blood oxygen-level-dependent (BOLD) signal across voxels. We previously demonstrated that it is possible to predict the position of individuals in a virtual-reality environment from the pattern of activity across voxels in the hippocampus. Although this shows that spatial memories can be decoded, substantially more challenging, and arguably only possible to investigate in humans, is whether it is feasible to predict which complex everyday experience, or episodic memory, a person is recalling. Here we document for the first time that traces of individual rich episodic memories are detectable and distinguishable solely from the pattern of fMRI BOLD signals across voxels in the human hippocampus. In so doing, we uncovered a possible functional topography in the hippocampus, with preferential episodic processing by some hippocampal regions over others. Moreover, our results imply that the neuronal traces of episodic memories are stable (and thus predictable) even over many re-activations. Finally, our data provide further evidence for functional differentiation within the medial temporal lobe, in that we show the hippocampus contains significantly more episodic information than adjacent structures.
Project description:The role of the hippocampus in declarative memory consolidation is a matter of intense debate. We investigated the neural substrates of memory retrieval for recent and remote information using functional magnetic resonance imaging (fMRI). 18 young, healthy participants learned a series of pictures. Then, during two fMRI recognition sessions, 3 days and 3 months later, they had to determine whether they recognized or not each picture using the "Remember/Know" procedure. Presentation of the same learned images at both delays allowed us to track the evolution of memories and distinguish consistently episodic memories from those that were initially episodic and then became familiar or semantic over time and were retrieved without any contextual detail. Hippocampal activation decreased over time for initially episodic, later semantic memories, but remained stable for consistently episodic ones, at least in its posterior part. For both types of memories, neocortical activations were observed at both delays, notably in the ventromedial prefrontal and anterior cingulate cortices. These activations may reflect a gradual reorganization of memory traces within neural networks. Our data indicate maintenance and strengthening of hippocampal and cortico-cortical connections in the consolidation and retrieval of episodic memories over time, in line with the Multiple Trace theory (Nadel and Moscovitch, 1997). At variance, memories becoming semantic over time consolidate through strengthening of cortico-cortical connections and progressive disengagement of the hippocampus.
Project description:Experiences unfold over time, but little is known about the mechanisms that support the formation of coherent episodic memories for temporally extended events. Recent work in animals has provided evidence for signals in hippocampus that could link events across temporal gaps; however, it is unknown whether and how such signals might be related to later memory for temporal information in humans. We measured patterns of fMRI BOLD activity as people encoded items that were separated in time and manipulated the presence of shared or distinct context across items. We found that hippocampal pattern similarity in the BOLD response across trials predicted later temporal memory decisions when context changed. By contrast, pattern similarity in lateral occipital cortex was related to memory only when context remained stable. These data provide evidence in humans that representational stability in hippocampus across time may be a mechanism for temporal memory organization.
Project description:Structured knowledge is thought to form, in part, through the extraction and representation of regularities across overlapping experiences. However, little is known about how consolidation processes may transform novel episodic memories to reflect such regularities. In a multi-day fMRI study, participants encoded trial-unique associations that shared features with other trials. Multi-variate pattern analyses were used to measure neural similarity across overlapping and non-overlapping memories during immediate and 1-week retrieval of these associations. We found that neural patterns in the hippocampus and medial prefrontal cortex represented the featural overlap across memories, but only after a week. Furthermore, after a week, the strength of a memory's unique episodic reinstatement during retrieval was inversely related to its representation of overlap, suggesting a trade-off between the integration of related memories and recovery of episodic details. These findings suggest that consolidation-related changes in neural representations support the gradual organization of discrete episodes into structured knowledge.
Project description:Selective retrieval of overlapping memories can generate competition. How does the brain adaptively resolve this competition? One possibility is that competing memories are inhibited; in support of this view, numerous studies have found that selective retrieval leads to forgetting of memories that are related to the just-retrieved memory. However, this retrieval-induced forgetting (RIF) effect can be eliminated or even reversed if participants are given opportunities to restudy the materials between retrieval attempts. Here, we outline an explanation for such a reversal, rooted in a neural network model of RIF that predicts representational differentiation when restudy is interleaved with selective retrieval. To test this hypothesis, we measured changes in pattern similarity of the BOLD fMRI signal elicited by related memories after undergoing interleaved competitive retrieval and restudy. Reduced pattern similarity within the hippocampus positively correlated with retrieval-induced facilitation of competing memories. This result is consistent with an adaptive differentiation process that allows individuals to learn to distinguish between once-confusable memories.
Project description:Although autobiographical memory and episodic simulations recruit similar core brain regions, episodic simulations engage additional neural recruitment in the frontoparietal control network due to greater demands on constructive processes. However, previous functional neuroimaging studies showing differences in remembering and episodic simulation have focused on veridical retrieval of past experiences, and thus have not fully considered how retrieving the past in different ways from how it was originally experienced may also place similar demands on constructive processes. Here we examined how alternative versions of the past are constructed when adopting different egocentric perspectives during autobiographical memory retrieval compared to simulating hypothetical events from the personal past that could have occurred, or episodic counterfactual thinking. Participants were asked to generate titles for specific autobiographical memories from the last five years, and then, during functional magnetic resonance (fMRI) scanning, were asked to repeatedly retrieve autobiographical memories or imagine counterfactual events cued by the titles. We used an fMRI adaptation paradigm in order to isolate neural regions that were sensitive to adopting alternative egocentric perspectives and counterfactual simulations of the personal past. The fMRI results revealed that voxels within left posterior inferior parietal and ventrolateral frontal cortices were sensitive to novel visual perspectives and counterfactual simulations. Our findings suggest that the neural regions supporting remembering become more similar to those underlying episodic simulation when we adopt alternative egocentric perspectives of the veridical past.
Project description:Neocortical-hippocampal interactions support new episodic (event) memories, but there is conflicting evidence about the dependence of remote episodic memories on the hippocampus. In line with systems consolidation and computational theories of episodic memory, evidence from model organisms suggests that the cornu ammonis 3 (CA3) hippocampal subfield supports recent, but not remote, episodic retrieval. In this study, we demonstrated that recent and remote memories were susceptible to a loss of episodic detail in human participants with focal bilateral damage to CA3. Graph theoretic analyses of 7.0-Tesla resting-state fMRI data revealed that CA3 damage disrupted functional integration across the medial temporal lobe (MTL) subsystem of the default network. The loss of functional integration in MTL subsystem regions was predictive of autobiographical episodic retrieval performance. We conclude that human CA3 is necessary for the retrieval of episodic memories long after their initial acquisition and functional integration of the default network is important for autobiographical episodic memory performance.
Project description:The hippocampus has long been implicated in supporting autobiographical memories, but little is known about how they are instantiated in hippocampal subfields. Using high-resolution functional magnetic resonance imaging (fMRI) combined with multivoxel pattern analysis we found that it was possible to detect representations of specific autobiographical memories in individual hippocampal subfields. Moreover, while subfields in the anterior hippocampus contained information about both recent (2 weeks old) and remote (10 years old) autobiographical memories, posterior CA3 and DG only contained information about the remote memories. Thus, the hippocampal subfields are differentially involved in the representation of recent and remote autobiographical memories during vivid recall.
Project description:At ultra-high field, fMRI voxels can span the sub-millimeter range, allowing the recording of blood oxygenation level dependent (BOLD) responses at the level of fundamental units of neural computation, such as cortical columns and layers. This sub-millimeter resolution, however, is only nominal in nature as a number of factors limit the spatial acuity of functional voxels. Multivoxel Pattern Analysis (MVPA) may provide a means to detect information at finer spatial scales that may otherwise not be visible at the single voxel level due to limitations in sensitivity and specificity. Here, we evaluate the spatial scale of stimuli specific BOLD responses in multivoxel patterns exploited by linear Support Vector Machine, Linear Discriminant Analysis and Naïve Bayesian classifiers across cortical depths in V1. To this end, we artificially misaligned the testing relative to the training portion of the data in increasing spatial steps, then investigated the breakdown of the classifiers' performances. A one voxel shift led to a significant decrease in decoding accuracy (p?<?0.05) across all cortical depths, indicating that stimulus specific responses in a multivoxel pattern of BOLD activity exploited by multivariate decoders can be as precise as the nominal resolution of single voxels (here 0.8?mm isotropic). Our results further indicate that large draining vessels, prominently residing in proximity of the pial surface, do not, in this case, hinder the ability of MVPA to exploit fine scale patterns of BOLD signals. We argue that tailored analytical approaches can help overcoming limitations in high-resolution fMRI and permit studying the mesoscale organization of the human brain with higher sensitivities.
Project description:Our experiences often overlap with each other, yet we are able to selectively recall individual memories to guide decisions and future actions. The neural mechanisms that support such precise memory recall remain unclear. Here, using ultra-high field 7T MRI we reveal two distinct mechanisms that protect memories from interference. The first mechanism involves the hippocampus, where the blood-oxygen-level-dependent (BOLD) signal predicts behavioral measures of memory interference, and representations of context-dependent memories are pattern separated according to their relational overlap. The second mechanism involves neocortical inhibition. When we reduce the concentration of neocortical GABA using trans-cranial direct current stimulation (tDCS), neocortical memory interference increases in proportion to the reduction in GABA, which in turn predicts behavioral performance. These findings suggest that memory interference is mediated by both the hippocampus and neocortex, where the hippocampus separates overlapping but context-dependent memories using relational information, and neocortical inhibition prevents unwanted co-activation between overlapping memories.
Project description:Functional MRI (fMRI) studies investigating the neural basis of episodic memory recall, and the related task of thinking about plausible personal future events, have revealed a consistent network of associated brain regions. Surprisingly little, however, is understood about the contributions individual brain areas make to the overall recollective experience. To examine this, we used a novel fMRI paradigm in which subjects had to imagine fictitious experiences. In contrast to future thinking, this results in experiences that are not explicitly temporal in nature or as reliant on self-processing. By using previously imagined fictitious experiences as a comparison for episodic memories, we identified the neural basis of a key process engaged in common, namely scene construction, involving the generation, maintenance and visualization of complex spatial contexts. This was associated with activations in a distributed network, including hippocampus, parahippocampal gyrus, and retrosplenial cortex. Importantly, we disambiguated these common effects from episodic memory-specific responses in anterior medial prefrontal cortex, posterior cingulate cortex and precuneus. These latter regions may support self-schema and familiarity processes, and contribute to the brain's ability to distinguish real from imaginary memories. We conclude that scene construction constitutes a common process underlying episodic memory and imagination of fictitious experiences, and suggest it may partially account for the similar brain networks implicated in navigation, episodic future thinking, and the default mode. We suggest that additional brain regions are co-opted into this core network in a task-specific manner to support functions such as episodic memory that may have additional requirements.