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Doeller, C. F.

Publications and source records attributed to Doeller, C. F..

At least 19 recordsLinked to original sources

Sequential Sampling as a Computational Principle of Episodic Memory

Visual perception unfolds through sequential eye movements, yet computational models of episodic memory typically assume that event representations already exist. Here, we propose that sequential gaze sampling does not simply supply memory with visual information, but contributes to the construction and organisation of episodic representations. We introduce a computational model in which successive fixations are integrated into an evolving internal representation, subsequently stored in associative memory and later retrieved through partial reinstatement of the original sampling trajectory. Within to-be-remembered elements, successive samples support progressive individuation; between elements, more frequent transitions strengthen relational binding. As sampling proceeds, internal representations become progressively lower-dimensional while retaining information about where samples were taken and when they occurred in the sequence. Sampling history also remains embedded in the resulting representation: changing the order of otherwise identical samples alters both the representation itself and element-specific retrieval. At retrieval, reinstating more of the original sampling trajectory improves access to specific elements, while competition is strongest when memories share both semantic category and sampling history. Finally, an exploratory generative readout shows that regions sampled during encoding are reconstructed more faithfully than unsampled regions. Together, these findings suggest that sequential sampling provides a candidate computational process through which episodic representations are constructed, shaping their subsequent storage and retrieval.

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Neural Dissociation of Cognitive Maps and Graphs in the Human Brain

Cognitive maps and graphs offer two distinct ways of organizing knowledge: maps arrange items within a spatial layout, whereas graphs thread them together through experiential transitions. However, spatial proximity and experiential contiguity are typically correlated, and content represented in one format can often be transformed into the other, making their neural representations difficult to disentangle. Here, we orthogonally manipulated Euclidean distance, indexing spatial proximity, and shortest-path distance, indexing experiential contiguity, within the same learned environment. Using fMRI and whole-brain searchlight representational similarity analysis, we identified dissociable representations of these two formats in the human brain. Euclidean distance was represented in the intraparietal sulcus, whereas shortest-path distance was represented in the hippocampal/parahippocampal region and in cortical areas that overlapped substantially with scene-selective regions. ROI analyses further supported the specificity of these representations across regions. Together, these findings provide neural evidence for a dissociation between cognitive maps and cognitive graphs.

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A computational model of the two dentate gyrus blades

The Dentate Gyrus (DG) is a key part of the hippocampus, and damage to the DG produces a wide range of pathologies, including overgeneralization of contexts, affective dysregulation (Anacker et al., 2018), and epileptogenic effects (Sloviter, 1994). The canonical model of the DG focuses on pattern separation for subsequent memory storage in the hippocampal subfield CA3. Experimental results challenge the singular focus on pattern separation and extend the function of the DG to the precise binding of objects and events to space, and the integration of information across episodes. Recent studies suggest that pattern separation and integration preferentially rely on distinct DG blades, with the suprapyramidal and infrapyramidal blades biased toward separation and integration, respectively. Here, we propose the first computational model that accounts for this distinction: an exemplar-based k-WTA architecture in the suprapyramidal DG (DGSUP) supports pattern separation and episode-specific representations, whereas an architecture with gradual heterosynaptic plasticity in the infrapyramidal DG (DGINF) supports integration of patterns across episodes. Both coding regimes are tested with two datasets: MNIST and neurally plausible entorhinal cortex inputs, thus suggesting some domain generality. Using the entorhinal cortex inputs, the two blades form place fields that either remap or maintain a stable code, consistent with experimental results. Novel inputs, including novel digit classes and novel spatial episodes, are incorporated through a neurogenesis-inspired turnover and recruitment mechanism. The two processing streams allow for a comparison of ongoing experience with the generalized expectations formed through integration across episodes. This yields prediction errors that can drive the storage of poorly predicted memories and the forgetting of well-predicted memories. The differential processing across the DG could thus aid in the iterative construction of spatial cognitive maps that encode location-dependent expectations, while at the same time preserving individual episodic memory traces. These functions are accomplished with biologically plausible learning regimes and widen the scope of DG computation beyond its well-established role in pattern separation.

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Non-invasive tracking of ripple-like activity during human sleep using MEG

Hippocampal ripples are considered a key mechanism of sleep-dependent memory consolidation. In humans, however, their direct investigation has relied on invasive recordings from patients with epilepsy, because EEG provides limited access to fast activity from deep medial temporal structures. Here, we tested whether source-resolved magnetoencephalography can reveal physiologically meaningful ripple-like activity during NREM sleep in healthy humans. These events showed hallmarks expected of sleep ripples: they were most prominent in medial temporal regions and embedded within slow oscillation (SO)-spindle dynamics, occurring preferentially during SO up-states and spindle centers. To test mnemonic relevance, we combined sleep MEG with targeted memory reactivation, in which learning cues were replayed during sleep. TMR improved memory performance, and later remembered cues preferentially recruited medial temporal ripple-like events alongside cortical spindles. Ripple-like events also coincided with enhanced item-specific reactivation during successful TMR. Together, these findings establish MEG as a non-invasive window onto hippocampo-cortical memory dynamics during sleep.

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Functional neural signatures of navigation impairment in early Alzheimer's Disease

Spatial navigation is impaired early in Alzheimers disease (AD), but the neural computations affected by AD pathology remain unclear. We combined virtual-reality navigation with fMRI in aged controls, preclinical AD, and early AD participants, relating navigation activity to cerebrospinal fluid biomarkers and genetic risk. Early AD was associated with dissociable alterations: amyloid-{beta}-linked hippocampal hyperactivity during memory-demanding navigation, tau-linked reductions in hexadirectional modulation near the entorhinal cortex, and altered object-centered representations in posterior cingulate and entorhinal-adjacent regions. Object-centered changes related to how participants encoded and retrieved target locations. Hippocampal hyperactivity was the earliest, most robust effect and the only functional measure distinguishing preclinical individuals from controls. These findings connect AD biomarkers to distinct spatial computations in humans and reveal navigation-based functional signatures of neural dysfunction before overt dementia.

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Hexadirectional modulation of EEG gamma band activity

The medial temporal lobe (MTL) houses specialised cell types supporting spatial representation in the human brain. Among these are grid cells that encode the location of the navigator, displaying a geometrically structured anchoring to the environment. While macroscopic grid-cell-like coding in humans is typically investigated using functional magnetic resonance imaging or invasive electrophysiological methods in clinical populations, we demonstrate the feasibility of using non-invasive scalp electroencephalography (EEG) to capture the characteristic six-fold modulation of high-frequency activity source-localised to the MTL. We found hexadirectional modulations of the low- and high-gamma band activity by movement direction in virtual reality. Furthermore, individual preference to use an allocentric reference frame was linked to higher hexadirectional modulation in the low gamma band and encoding a location along the putative grid axes of high gamma band predicted faster retrieval of the remembered location. The use of scalp EEG to capture grid-cell-like activity and its functional relevance sets the foundation for investigating the MTL activity in richer experimental contexts.

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Adaptive sequential eye-movement sampling and replay under different task demands

Human cognition is capacity-limited, requiring strategies to actively structure information. Eye movements offer a natural mechanism for sequential sampling, but whether such sequences organize mnemonic representations is unknown. We developed a working-memory task where color-frequency pairings created a consistent latent ordinal structure to optimally reduce memory load. Across two experiments, gaze patterns spontaneously aligned with this structure. Participants sampled items following this sequence during encoding and covertly replayed them during maintenance. Critically, the expression of this structure depended on cognitive demand. In a 3-item task, high performers showed robust sequential sampling during encoding, whereas lower performers compensated with replay-like revisitation during maintenance. Under higher demand (4 items), encoding-based organization was disrupted, and structured replay emerged primarily during maintenance to support memory. These findings show that eye movements do more than reflect memory; they actively organize it, revealing a flexible, behavioral analogue to neural replay when encoding resources are strained.

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Visual working memory representations of naturalistic images in early visual cortex are not sensory-like

For a long time, working memory was considered to reflect sustained activity in prefrontal and parietal areas. This has been challenged by the "sensory recruitment model" according to which sensory areas are involved in maintaining working memory representations. The main support for this comes from the finding that working memory contents can be decoded from early sensory areas during memory delay periods. However, the availability of stimulus-related information in sensory regions does not reveal whether this information is encoded in a sensory format, i.e. in the same way as sensory stimuli. Alternatively, working memory contents could be encoded in independent formats or even potentially undergo dynamic changes throughout the delay. Here, we test this question directly by requiring participants to briefly memorise naturalistic object-scenes. We directly compared the way early visual regions encoded the contents during perception and working memory maintenance. As in previous studies, we found robust stimulus-related information in early visual cortex throughout the delay. However, despite continuously robust information, the encoding of memory contents in the later delay period did not occur in the same format as during pure perception. Thus, despite the fact that sensory areas have working-memory-related information, the format of this information is not strictly sensory-like throughout the delay.

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Neural replay is connected to latent cause inference and supports fast generalization

Dynamic environments require generalizing knowledge through two computational mechanisms: Inferring clusters of equivalent observations and propagating reward expectations within a cluster. While neural replay has been linked to both, past work has not studied these processes simultaneously, leaving their relative importance for replay unclear. We used fMRI and computational modeling to investigate latent cause inference and replay in 52 participants during a value-based task with shared rewards across bandits. Participants learned this structure and achieved one-shot generalization after reversals, consistent with a latent cause inference process. fMRI during predecision pauses revealed backwards replay of shared-reward bandits in the visual cortex and medial temporal lobe. Trial-wise fluctuations in visual replay strength and content were better explained by value updates than by structure learning. Conversely, abstract reward structure representations were localized specifically to the MTL. These results demonstrate that on-task replay serves reward propagation within learned latent structures to facilitate fast generalization.

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Inference over hidden contexts shapes the geometry of conceptual knowledge for flexible behaviour

Flexible decision-making in uncertain environments requires inferring latent task states and prioritising behaviourally relevant information. We tested the hypothesis that this process is associated with systematic changes in attention and neural representational structure. Human participants performed a serial reversal learning task that required identifying which stimulus dimension(s) were currently relevant. Behaviourally, participants rapidly adapted to context switches, and a hidden-state inference model best explained these adaptations, outperforming multiple reinforcement-learning variants in predicting both choices and inferred contexts. Oculomotor behaviour provided converging evidence for selective attention, with gaze increasingly concentrated on relevant features, tracking trial-by-trial belief updates, and transiently broadening following high prediction errors. Guided by these results, we used magnetoencephalography to examine how latent-state inference was reflected in neural activity. Neural representations encoded the currently inferred context and were modulated by recent prediction errors, with larger prediction errors associated with weaker context representations on subsequent trials. Representational analyses further revealed that successful performance was associated with a systematic reorganisation of neural geometry, characterised by selective amplification of task-relevant representational distances and increased separation of behaviourally relevant stimulus values. Together, our findings demonstrate that latent-state inference, attention, and neural representational geometry are tightly coordinated during flexible decision-making, providing a systems-level account of how behaviourally relevant information is selectively prioritised and represented to support adaptive behaviour.

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Foraging in conceptual spaces: hippocampal oscillatory dynamics underlying searching for concepts in memory

How does the brain access stored knowledge? It has been proposed that conceptual search engages neurocognitive processes similar to foraging in physical space. We tested this idea using intracranial EEG in patients performing a verbal fluency task, where they spontaneously explored their own knowledge of the world, sampling words from semantic memory. We found that hippocampal theta power increased during conceptual search and scaled with the semantic distance between successive words, paralleling dynamics observed in spatial navigation. Critically, people transitioned between conceptual clusters, resembling transitions between resource patches in foraging behavior. These shifts were marked by enhanced theta-gamma coupling, both within the hippocampus and between the hippocampus and lateral temporal cortex, a key hub of the semantic network. These findings support a mechanistic account of memory search grounded in navigation and foraging principles, suggesting that the hippocampus orchestrates local computations and long-range interactions to enable flexible retrieval of conceptual knowledge.

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Impact of Task Similarity and Training Regimes on Cognitive Transfer and Interference

Learning depends not only on the content of what we learn, but also on how we learn and on how experiences are structured over time. To investigate how task similarity and training regime interact during learning, we trained participants on spatial and conceptual learning tasks that shared either similar or distinct underlying structures, using either interleaved or blocked regimes. Interleaving the two tasks hindered performance when their structures were similar, compared to when they were different. In contrast, blocked training produced the opposite effect: it improved performance and facilitated transfer across similar tasks. This effect, however, emerged only when participants first learned the conceptual task, followed by the spatial task, suggesting an asymmetric interaction between task order and structural similarity. We also replicated our results using a neural network model, providing converging evidence for the computational principles governing the interplay between training regime and structural similarity in multi-task learning.

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Efficient coding in working memory is adapted to the structure of the environment

Working memory (WM) relies on efficient coding strategies to overcome its limited capacity, yet how the brain adaptively organizes WM representations to maximize coding efficiency based on environmental structure remains largely unknown. In our study, participants remembered a sequence of gratings defined in a two-dimensional feature space where we manipulated directional consistency, revealing enhanced performance for structured (consistent direction) vs non-strutured (non-consistent direction) contexts, particularly for individuals with lower WM capacity. Magnetoencephalography analyses uncovered dissociable neural bases: consistent sequences engaged anterior temporal and medial frontal cortices for abstract directional representations during maintenance, while inconsistent sequences preferentially reactivated item-specific representations in parietal regions. These neural patterns predicted behavioral performance, establishing a neural efficiency principle wherein the brain adaptively switches between relational and item-based coding strategies, mitigating WM constraints. These findings advance our understanding of how structures shape WM organization, offering insights into cognitive flexibility and neural resource allocation in complex environments.

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Re-enacting steps supports human path integration consistent with motor-corrected grid cell drift

Efficient navigation, especially in the absence of vision, requires path integration -- the continuous updating of spatial position from self-motion cues. However, path integration is prone to cumulative error, which can be amplified when body-derived information is inconsistent between encoding and retrieval paths. Drawing on evidence from sensorimotor reactivation during memory retrieval, we hypothesized that re-enacting encoding-related movement patterns could serve as a body-derived mechanism to counteract such errors. In a novel virtual reality task with motion tracking, participants learned unique, irregular step sequences linked to specific target distances during an encoding phase. They later reproduced these distances in complete darkness under three conditions: self-paced free retrieval, retrieval with encoding-congruent movements, and retrieval with encoding-incongruent, regular gait. During free retrieval, participants naturally re-enacted encoding-related movements associated with improved distance reproduction. As predicted, distance estimation was significantly more accurate during congruent retrieval than during incongruent retrieval. These behavioral findings are consistent with a neural network model in which retrieved encoding-related motor patterns correct path integration errors in grid cells. Together, these results provide converging behavioral and computational evidence that body-derived, encoding-related motor patterns can enhance distance estimation, possibly by filtering grid cell error accumulation, offering new insights into embodied mechanisms of path integration.

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Hippocampal ripples initiate cortical dimensionality expansion for memory retrieval

How are past experiences reconstructed from memory? Learning is thought to compress external inputs into low-dimensional hippocampal representations, later expanded into high-dimensional cortical activity during recall. Hippocampal ripples, brief high-frequency bursts linked to retrieval, may initiate this expansion. Analysing intracranial EEG data from patients with pharmaco-resistant epilepsy during an episodic memory task, we found that cortical dimensionality increased following ripple events during correct, but not incorrect, retrieval. This expansion correlated with faster reaction times and reinstatement of the target association. Crucially, hippocampal theta and cortical gamma phase-amplitude coupling emerged after ripples but before cortical expansion, suggesting a mechanism for ripple-driven communication. Ripple events also marked the separation of task-relevant variables in cortical state space, revealing how hippocampal output reshapes the geometry of memory representations to support successful recall.

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Egocentric body-axis-related and allocentric clover-like tuning of object vector representations supports human spatial cognition

Vector-based spatial coding has been demonstrated in rodents, yet its neural basis in humans and its contribution to navigation remain poorly understood. Using a novel spatial updating task, we show that egocentric directional signals peak when objects are located behind the navigator, while distance signals emerge only when objects are out of view, suggesting a mnemonic role for vision-independent spatial mapping. Allocentric signals form a clover-shaped, four-axis pattern aligned to visual features, with improved navigation accuracy along its axes. Parallel rodent recordings further show the clover pattern arises from averaged activity of allocentric vectorial neurons, suggesting conserved cross-species mechanisms. Together, our findings uncover vector-based representations in the human brain, potentially serving as a neural reference axis to anchor objects to internal maps and support navigation.

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Locomotion-dependent use of geometric and body cues in humans mapping 3D space

The ability to represent locations across multiple dimensions of space is a core function of cognitive maps. While the influence of boundary-dependent environmental geometry on spatial representations has been extensively studied in 2D spaces, less is known about the role of boundaries for volumetric spatial memory. Research in humans and other animals has demonstrated distinct processing of the vertical and horizontal spatial dimensions, likely related to species-specific modes of locomotion. Here, we investigate whether different locomotion modes, flying and walking, affect the use of vertical boundaries, leading to possibly distinct volumetric representations. In a Virtual Reality experiment, human participants memorized objects within a symmetric 3D enclosure, and then were asked to replace them in either the familiar or geometrically deformed environments. We found that the flying group exhibited lower vertical than horizontal spatial memory precision, whereas the walking group showed the opposite pattern, an effect related to using their body axis as a vertical "ruler". Within deformed environments, object replacements in the flying group followed the predictions from a 3D-extended boundary-vector-cell-like computational model of spatial mapping that treated all boundaries equally, whereas those in the walking condition favored a modified model that prioritized the ground boundary. Our findings suggest that gravity-related movement constraints promote different utilization of geometric and body-related cues, resulting in flexible representations of volumetric space.

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Representation of conceptual affordances in eye movements and the entorhinal cortex

Structural representations in the entorhinal cortex are a crucial feature of cognitive maps. However, a complete understanding of task structure often requires knowledge of the actions available at each state (analogous to the moves of different pieces on a chessboard). Moreover, action representations are key to several models of the hippocampal-entorhinal system. In this study, we tested whether the entorhinal cortex represents the actions that allow transitioning between states of a conceptual space. In particular, participants learned to transition between numerically-labelled states using different mathematical operations. Behaviourally, participants learned and generalised action information across states. Action information was also reflected in eye movements, indicating the active processing of the possible actions for a given state during the trials. Importantly, we found that neural pattern similarity in the right entorhinal cortex scaled with the similarity of action affordances across the states. This affordance representation was not explained by other properties of the task space such as link distance between the states or action magnitude. In sum, this study provides first evidence for the integration of action information into ocular and entorhinal representations of conceptual spaces, suggesting that these may not just store experiences, but provide information about how to explore knowledge.

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