Biology subjects

Kuhl, B. A.

Publications and source records attributed to Kuhl, B. A..

15 recordsLinked to original sources

bioRxiv2025

Hippocampal transformations occur along dimensions of memory interference

The role of the hippocampus in resolving memory interference has been greatly elucidated by considering the relationship between the similarity of visual stimuli (input) and corresponding similarity of hippocampal activity patterns (output). However, these input-output functions can take surprisingly different forms. Here, we reconcile seemingly conflicting findings by considering the possibility that the hippocampus prioritizes different dimensions of visual similarity across different stages of learning. First, we generated a set of natural scene images from two visual categories and rigorously characterized visual similarity using a wide array of methods: neural networks, artificial intelligence models, and human perceptual and memory decisions. We then identified two orthogonal dimensions of visual similarity that each predicted memory interference, but that did so at distinct stages of learning. Using high-resolution fMRI, we then tested for dimension-specific input-output functions within the hippocampus. Within CA3 and dentate gyrus (CA3/DG), we show that dimensions of visual similarity were inverted (repulsion) at stages of learning when they contributed to memory interference. In contrast, CA3/DG preserved similarity when dimensions did not contribute to interference. These findings reveal that hippocampal representations of visually-similar stimuli are highly dynamic and critically depend on the dimensions of similarity that currently contribute to memory interference.

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bioRxiv2025

Hippocampal-guided reconstruction of an event's prior temporal context

Leading theories of episodic memory argue that when events from the past are remembered, temporally-adjacent events are also reinstated ( temporal context reinstatement). However, direct evidence for temporal context reinstatement is surprisingly limited. Here, we tested for temporal context reinstatement in a human fMRI continuous recognition memory experiment in which natural scene images were repeatedly encountered. For the original encounter with each scene, we defined its temporal context as the visual content of temporally-adjacent scenes. Using voxelwise encoding models, we tested whether fMRI activity patterns evoked when a scene was re-encountered carried information about the original encounters temporal context. Indeed, we found robust temporal context reinstatement within high-level visual cortex (lateral occipitotemporal cortex; LOTC), despite the fact that reinstated content was entirely incidental to task demands. However, temporal context reinstatement only occurred when stimuli were successfully recognized, indicating that reinstatement was behaviorally-relevant, even if incidental. Finally, the strength of temporal context reinstatement in LOTC was predicted by the similarity of hippocampal activity patterns across encounters, demonstrating distinct, but complimentary, roles for the hippocampus and neocortex in reinstating temporal context information.

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bioRxiv2024

Repulsion of CA3 / dentate gyrus representations is driven by distinct internal beliefs in the face of ambiguous sensory input

Recent human neuroimaging studies of episodic memory have revealed a counterintuitive phenomenon in the hippocampus: when events are highly similar, corresponding hippocampal activity patterns are sometimes less correlated than activity patterns associated with unrelated events. This phenomenon--repulsion--is not accounted for by most theories of the hippocampus, and the conditions that trigger repulsion remain poorly understood. Here, we used a spatial route-learning task and high-resolution fMRI in humans to test whether hippocampal repulsion is fundamentally driven by internal beliefs about the environment. By precisely measuring participants internal beliefs and actively manipulating them, we show that repulsion selectively occurred in hippocampal subfields CA3 and dentate gyrus when visual input was ambiguous--or even identical--but internal beliefs were distinct. These findings firmly establish conditions that elicit repulsion and have broad relevance to theories of hippocampal function and to the fields of human episodic memory and rodent spatial navigation.

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bioRxiv2024

Temporal asymmetry of neural representations predicts memory decisions

A stimulus can be familiar for multiple reasons. It might have been recently encountered, or is similar to recent experience, or is similar to typical experience. Understanding how the brain translates these sources of similarity into memory decisions is a fundamental, but challenging goal. Here, using fMRI, we computed neural similarity between a current stimulus and events from different temporal windows in the past and future (from seconds to days). We show that trial-by-trial memory decisions (is this stimulus old?) were predicted by the difference in similarity to past vs. future events (temporal asymmetry). This relationship was (i) evident in lateral parietal and occipitotemporal cortices, (ii) strongest when considering events from the recent past (minutes ago), and (iii) most pronounced when veridical (true) memories were weak. These findings suggest a new perspective in which the brain supports memory decisions by comparing what actually occurred to what is likely to occur.

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bioRxiv2024

Benefits of spaced learning are predicted by re-encoding of past experience in ventromedial prefrontal cortex

More than a century of research shows that spaced learning improves long-term memory. Yet, there remains debate concerning why. A major limitation to resolving theoretical debates is the lack of evidence for how neural representations change as a function of spacing. Here, leveraging a massive-scale 7T human fMRI dataset, we tracked neural representations and behavioral expressions of memory as participants viewed thousands of natural scene images that repeated at lags ranging from seconds to many months. We show that spaced learning increases the similarity of human ventromedial prefrontal cortex representations across stimulus encounters and, critically, these increases parallel and predict the behavioral benefits of spacing. Additionally, we show that these spacing benefits critically depend on remembering and, in turn, re-encoding past experience. Collectively, our findings provide fundamental insight into how spaced learning influences neural representations and why spacing is beneficial.

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bioRxiv2023

Mapping multidimensional content representations to neural and behavioral expressions of episodic memory

Human neuroimaging studies have shown that the contents of episodic memories are represented in distributed patterns of neural activity. However, these studies have mostly been limited to decoding simple, unidimensional properties of stimuli. Semantic encoding models, in contrast, offer a means for characterizing the rich, multidimensional information that comprises episodic memories. Here, we extensively sampled four human fMRI subjects to build semantic encoding models and then applied these models to reconstruct content from natural scene images as they were viewed and recalled from memory. First, we found that multidimensional semantic information was successfully reconstructed from activity patterns across visual and lateral parietal cortices, both when viewing scenes and when recalling them from memory. Second, whereas visual cortical reconstructions were much more accurate when images were viewed versus recalled from memory, lateral parietal reconstructions were comparably accurate across visual perception and memory. Third, by applying natural language processing methods to verbal recall data, we showed that fMRI-based reconstructions reliably matched subjects verbal descriptions of their memories. In fact, reconstructions from ventral temporal cortex more closely matched subjects own verbal recall than other subjects verbal recall of the same images. Fourth, encoding models reliably transferred across subjects: memories were successfully reconstructed using encoding models trained on data from entirely independent subjects. Together, these findings provide evidence for successful reconstructions of multidimensional and idiosyncratic memory representations and highlight the differential sensitivity of visual cortical and lateral parietal regions to information derived from the external visual environment versus internally-generated memories.

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bioRxiv2022

Adding meaning to memories: How parietal cortex combines semantic content with episodic experience

Neuroimaging studies of human memory have consistently found that univariate responses in parietal cortex track episodic experience with stimuli (whether stimuli are old or new). More recently, pattern-based fMRI studies have shown that parietal cortex also carries information about the semantic content of remembered experiences. However, it is not well understood how memory-based and content-based signals are integrated within parietal cortex. Here, we used voxel-wise encoding models and a recognition memory task to predict the fMRI activity patterns evoked by complex natural scene images based on (a) the episodic history and (b) the semantic content of each image. Models were generated and compared across distinct subregions of parietal cortex and for occipitotemporal cortex. We show that parietal and occipitotemporal regions each encode memory and content information, but they differ in how they combine this information. Among parietal subregions, angular gyrus was characterized by robust and overlapping effects of memory and content. Moreover, subject-specific semantic tuning functions revealed that successful recognition shifted the amplitude of tuning functions in angular gyrus but did not change the selectivity of tuning. In other words, effects of memory and content were additive in angular gyrus. This pattern of data contrasted with occipitotemporal cortex where memory and content effects were interactive: memory effects were preferentially expressed by voxels tuned to the content of a remembered image. Collectively, these findings provide unique insight into how parietal cortex combines information about episodic memory and semantic content.

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bioRxiv2022

Perception and Memory Retrieval States are Reflected in Distributed Patterns of Background Functional Connectivity

The same visual input can serve as the target of perception or as a trigger for memory retrieval depending on whether cognitive processing is externally oriented (perception) or internally oriented (memory retrieval). While numerous human neuroimaging studies have characterized how visual stimuli are differentially processed during perception versus memory retrieval, perception and memory retrieval may also be associated with distinct neural states that are independent of stimulus-evoked neural activity. Here, we combined human fMRI with full correlation matrix analysis (FCMA) to reveal potential differences in "background" functional connectivity across perception and memory retrieval states. We found that perception and retrieval states could be discriminated with high accuracy based on patterns of connectivity across (1) the control network, (2) the default mode network (DMN), and (3) retrosplenial cortex (RSC). In particular, clusters in the control network increased connectivity with each other during the perception state, whereas clusters in the DMN were more strongly coupled during the retrieval state. Interestingly, RSC switched its coupling between networks as the cognitive state shifted from retrieval to perception. Finally, we show that background connectivity 1) was fully independent from stimulus-related variance in the signal and, further, 2) captured distinct aspects of cognitive states compared to traditional classification of stimulus-evoked responses. Together, our results reveal that perception and memory retrieval are associated with sustained cognitive states that manifest as distinct patterns of connectivity among large-scale brain networks.

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bioRxiv2022

Re-expression of CA1 and entorhinal activity patterns preserves temporal context memory at long timescales

Converging, cross-species evidence indicates that memory for time is supported by hippocampal area CA1 and entorhinal cortex. However, limited evidence characterizes how these regions preserve temporal memories over long timescales (e.g., months). At long timescales, memoranda may be encountered in multiple temporal contexts, potentially creating interference. Here, using 7T fMRI, we measured CA1 and entorhinal activity patterns as human participants viewed thousands of natural scene images distributed, and repeated, across many months. We show that memory for an images original temporal context was predicted by the degree to which CA1/entorhinal activity patterns from the first encounter with an image were re-expressed during re-encounters occurring minutes to months later. Critically, temporal memory signals were dissociable from predictors of recognition confidence, which were carried by distinct medial temporal lobe expressions. These findings suggest that CA1 and entorhinal cortex preserve temporal memories across long timescales by coding for and reinstating temporal context information.

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bioRxiv2021

Abrupt remapping in human CA3/dentate gyrus signals resolution of memory interference

Remapping refers to a decorrelation of hippocampal representations of similar spatial environments. While it has been speculated that remapping may contribute to the resolution of episodic memory interference in humans, direct evidence is surprisingly limited. Here, we tested this idea using high-resolution, pattern-based fMRI analyses. We show that activity patterns in human CA3/dentate gyrus exhibit an abrupt, temporally-specific decorrelation of highly similar memory representations that is precisely coupled with behavioral expressions of successful learning. Strikingly, the magnitude of this learning-related decorrelation was predicted by the amount of pattern overlap during initial stages of learning, with greater initial overlap leading to stronger decorrelation. Finally, we show that remapped activity patterns carry relatively more information about learned episodic associations compared to competing associations, further validating the learning-related significance of remapping. Collectively, these findings establish a critical link between hippocampal remapping and episodic memory interference and provide novel insight into why remapping occurs.

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bioRxiv2020

Adaptive repulsion of long-term memory representations is triggered by event similarity

We tested whether similarity between events triggers an adaptive repulsion of long-term memories. Subjects completed an associative learning task in which objects were paired with faces. Critically, the objects consisted of pairs that were identical except for their color values, which were parametrically varied in order to manipulate interference. Performance on associative memory tests confirmed that color similarity robustly influenced interference. Separate tests of color memory showed that high similarity triggered a repulsion of long-term memories, wherein remembered colors were biased away from colors of competing objects. This repulsion effect was replicated across three experiments. In a fourth experiment, the repulsion effect was fully eliminated when task demands promoted integration, instead of discrimination, of similar memories. Finally, we show that repulsion of color memory was highly adaptive: greater repulsion was associated with less memory interference. These findings reveal that similarity between events triggers adaptive distortions in how events are remembered. SUPPLEMENTARY INFORMATIONThree supplementary figures are included.

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bioRxiv2019

Spatial perception and memory have distinct activation profiles in human visual cortex

Reactivation of earlier perceptual activity is thought to underlie long-term memory recall. Despite evidence for this view, it is unknown whether mnemonic activity exhibits the same tuning properties as feedforward perceptual activity. Here, we leveraged population receptive field models to parameterize fMRI activity in human visual cortex during spatial memory retrieval. Though retinotopic organization was present during both perception and memory, large systematic differences in tuning were also evident. Notably, whereas there was a three-fold decline in spatial precision from early to late visual areas during perception, this property was entirely abolished during memory retrieval. This difference could not be explained by reduced signal-to-noise or poor performance on memory trials. Instead, by simulating top-down activity in a network model of cortex, we demonstrate that this property is well-explained by the hierarchical structure of the visual system. Our results provide insight into the computational constraints governing memory reactivation in sensory cortex.

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bioRxiv2018

Parietal representations of stimulus features are amplified during memory retrieval and flexibly aligned with top-down goals

In studies of human episodic memory, the phenomenon of reactivation has traditionally been observed in regions of occipitotemporal cortex (OTC) involved in sensory experience. However, reactivation also occurs in lateral parietal cortex (LPC), and recent evidence indicates that reactivation of stimulus-specific information may be stronger in LPC than in OTC. These observations raise a number of questions about the nature of memory representations in LPC and their relation to representations in OTC. Here, we report two fMRI experiments that quantify stimulus feature information (color and object category) within LPC and OTC, separately during perception and memory retrieval, in male and female human subjects. Across both experiments, we show a clear dissociation between OTC and LPC: while feature information in OTC is relatively stronger during perception than memory, feature information in LPC is relatively stronger during memory than perception. Thus, while OTC and LPC represent common stimulus features, they preferentially represent this information during different stages. We show that this transformation of feature information across regions co-occurs with stimulus-level reinstatement within LPC and high-level OTC. In Experiment 2, we consider whether feature information in LPC during memory retrieval is flexibly and dynamically shaped by top-down goals. Indeed, we find that dorsal LPC preferentially represents retrieved feature information that addresses current goals. In contrast, ventral LPC represents retrieved features independent of current goals. Collectively, these findings provide insight into the nature and significance of mnemonic representations in LPC and constitute an important bridge between putative mnemonic and control functions of parietal cortex.

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bioRxiv2017

Decomposing parietal memory reactivation to predict consequences of remembering

Memory retrieval can strengthen, but also distort memories. Parietal cortex is a candidate region involved in retrieval-induced memory changes as it reflects retrieval success and represents retrieved content. Here, we conducted an fMRI experiment to test whether different forms of parietal reactivation predict distinct consequences of retrieval. Subjects studied associations between words and pictures of faces, scenes, or objects, and then repeatedly retrieved half of the pictures, reporting the vividness of the retrieved pictures ( retrieval practice). On the following day, subjects completed a recognition memory test for individual pictures. Critically, the test included lures highly similar to studied pictures. Behaviorally, retrieval practice increased both hit and false alarm rates to similar lures, confirming a causal influence of retrieval on subsequent memory. Using pattern similarity analyses, we measured two different levels of reactivation during retrieval practice: generic category-level reactivation and idiosyncratic item-level reactivation. Vivid remembering during retrieval practice was associated with stronger category- and item-level reactivation in parietal cortex. However, these measures differentially predicted subsequent recognition memory performance: whereas higher category-level reactivation tended to predict false alarms to lures, item-level reactivation predicted correct rejections. These findings indicate that parietal reactivation can be decomposed to tease apart distinct consequences of memory retrieval.

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bioRxiv2017

Overlap among spatial memories triggers divergence of hippocampal representations

Across the domains of spatial navigation and episodic memory, the hippocampus is thought to play a critical role in disambiguating (pattern separating) representations of overlapping events. However, the mechanisms underlying hippocampal pattern separation are not fully understood. Here, using a naturalistic route-learning paradigm and spatiotemporal pattern analysis of human fMRI data, we found that hippocampal representations of overlapping routes gradually diverged with learning to the point that they became less similar than representations of non-overlapping events. This representational reversal of the objective route similarity (a) was selective to the hippocampus, (b) only occurred for the specific route segments that were shared across routes, and (c) was predicted by the degree to which individual hippocampal voxels were initially shared across route representations. These findings indicate that event overlap triggers a repulsion of hippocampal representations--a finding that provides critical mechanistic insight into how and why hippocampal representations become separated.

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