Biology subjects

Kahn, A. E.

Publications and source records attributed to Kahn, A. E..

12 recordsLinked to original sources

bioRxiv2026

Meta-learning is expressed through altered prefrontal cortical dynamics

Learning where and when rewards like food and water are available is essential for survival1,2. In the simplest cases where resource availability is stable, animals can learn reward contingencies by integrating outcomes across repeated samples of each possible action. In more natural settings, however, reward availability is governed by structured higher-order rules such as depletion and repletion over time. To adapt flexibly to such changing environments, optimal choices require meta-learning wherein animals learn how to learn from external feedback, ultimately enabling them to infer the underlying reward structure from abstract, generalizable rules rather than relying solely on recent outcomes3,4. The existence of meta-learning in animal behavior is well established3-8, yet the neural circuits and computations that implement it remain poorly understood9-11. Here we investigated meta-learning using a spatial foraging task in which rats acquired a depletion-repletion rule that regulated reward availability, and carried out longitudinal, high-density recordings from the medial prefrontal cortex (mPFC). We show that meta-learning engages specific, systematic changes in mPFC neural dynamics that embed the learned rule and thereby alter how the network learns action values from reward outcomes. These dynamics are based on mixed coding of task structure and value in individual mPFC neurons. At the population level, this coding organizes into low-dimensional dynamical motifs that generalize across task conditions. As meta-learning progresses, these motifs are reshaped to instantiate both rule-guided inference of future states before outcome delivery and rule-based value updating during the outcome period. These results indicate that meta-learning sculpts pre-existing prefrontal dynamics to support the acquisition of new, generalizable reward-learning strategies.

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bioRxiv2024

Trial-by-trial learning of successor representations in human behavior

Decisions in humans and other organisms depend, in part, on learning and using models that capture the statistical structure of the world, including the long-run expected outcomes of our actions. One prominent approach to forecasting such long-run outcomes is the successor representation (SR), which predicts future states aggregated over multiple timesteps. Although much behavioral and neural evidence suggests that people and animals use such a representation, it remains unknown how they acquire it. It has frequently been assumed to be learned by temporal difference bootstrapping (SR-TD(0)), but this assumption has largely not been empirically tested or compared to alternatives including eligibility traces (SR-TD({lambda} > 0)). Here we address this gap by leveraging trial-by-trial reaction times in graph sequence learning tasks, which are favorable for studying learning dynamics because the long horizons in these studies differentiate the transient update dynamics of different learning rules. We examined the behavior of SR-TD({lambda}) on a probabilistic graph learning task alongside a number of alternatives, and found that behavior was best explained by a hybrid model which learned via SR-TD({lambda}) alongside an additional predictive model of recency. The relatively large{lambda} we estimate indicates a predominant role of eligibility trace mechanisms over the bootstrap-based chaining typically assumed. Our results provide insight into how humans learn predictive representations, and demonstrate that people simultaneously learn the SR alongside lower-order predictions. Author SummaryOur ability to plan intelligently requires predicting the state of the world multiple steps into the future. Enumerating future outcomes step-by-step, however, is slow and costly. Instead, research has shown that people rely on simplified models of the world that skip across multiple steps at once. How do we construct these simplified models? One promising idea is the successor representation (SR), which predicts future events via a simple and neurally plausible computation. The SR has been shown to explain a range of behavioral phenomena, but these studies have not identified which among many learning rules the brain uses to build the SR. Plausible mechanisms for learning associations over delays (called bootstrapping and eligibility traces) both converge to identical simplified world models, and thus existing studies on the SR, which focus on well trained behavior, are unable to distinguish between them. Here, we answer this question by examining behavior on a graph learning task, where stimulus-by-stimulus reaction times have been shown to reflect predictions over long temporal horizons. Through both model fitting and model-agnostic comparisons, we find that behavior is best explained by a learning rule heavily dependent on eligibility traces, in contrast to previous work which generally assumed an (untested) bootstrapping update rule.

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bioRxiv2024

Hippocampal representations of alternative possibilities are flexibly generated to meet cognitive demands

The cognitive ability to go beyond the present to consider alternative possibilities, including potential futures and counterfactual pasts, can support adaptive decision making. Complex and changing real-world environments, however, have many possible alternatives. Whether and how the brain can select among them to represent alternatives that meet current cognitive needs remains unknown. We therefore examined neural representations of alternative spatial locations in the rat hippocampus during navigation in a complex patch foraging environment with changing reward probabilities. We found representations of multiple alternatives along paths ahead and behind the animal, including in distant alternative patches. Critically, these representations were modulated in distinct patterns across successive trials: alternative paths were represented proportionate to their evolving relative value and predicted subsequent decisions, whereas distant alternatives were prevalent during value updating. These results demonstrate that the brain modulates the generation of alternative possibilities in patterns that meet changing cognitive needs for adaptive behavior.

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bioRxiv2024

Time-resolved functional connectivity during visuomotor graph learning

1Humans naturally attend to patterns that emerge in our perceptual environments, building mental models that allow future experiences to be processed more effectively and efficiently. Perceptual events and statistical relations can be represented as nodes and edges in a graph. Recent work in graph learning has shown that human behavior is sensitive to graph topology, but little is known about how that topology might elicit distinct neural responses during learning. Here, we address this knowledge gap by applying time-resolved network analyses to fMRI data collected during a visuomotor graph learning task. We assess neural signatures of learning on two types of structures: modular and non-modular lattice graphs. We find that task performance is supported by a highly flexible visual system, relatively stable brain-wide community structure, cohesiveness within the dorsal attention, limbic, default mode, and subcortical systems, and an increasing degree of integration between the visual and ventral attention systems. Additionally, we find that the time-resolved connectivity of the limbic, default mode, temporoparietal, and subcortical systems is associated with enhanced performance on modular graphs but not on lattice-like graphs. These findings provide evidence for the differential processing of statistical patterns with distinct underlying graph topologies. Our work highlights the similarities between the neural correlates of graph learning and those of statistical learning.

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bioRxiv2023

Humans rationally balance mental simulation and temporally-abstract heuristics

How do people model the worlds dynamics to guide mental simulation and evaluate choices? One prominent approach, the Successor Representation (SR), takes advantage of temporal abstraction of future states: by aggregating trajectory predictions over multiple timesteps, the brain can avoid the costs of iterative, multi-step mental simulation. Human behavior broadly shows signatures of such temporal abstraction, but finer-grained characterization of individuals strategies and their dynamic adjustment remains an open question. We developed a novel task to measure SR usage during dynamic, trial-by-trial learning. Using this approach, we find that participants exhibit a mix of SR and model-based learning strategies that varies across individuals. Further, by dynamically manipulating the task contingencies within-subject to favor or disfavor temporal abstraction, we observe evidence of resource-rational reliance on the SR, which decreases when future states are less predictable. Our work adds to a growing body of research showing that the brain arbitrates between approximate decision strategies. The current study extends these ideas from simple habits into usage of more sophisticated approximate predictive models, and demonstrates that individuals dynamically adapt these in response to the predictability of their environment.

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bioRxiv2023

Network structure influences the strength of learned neural representations

Human experience is built upon sequences of discrete events. From those sequences, humans build impressively accurate models of their world. This process has been referred to as graph learning, a form of structure learning in which the mental model encodes the graph of event-to-event transition probabilities [1], [2], typically in medial temporal cortex [3]-[6]. Recent evidence suggests that some network structures are easier to learn than others [7]-[9], but the neural properties of this effect remain unknown. Here we use fMRI to show that the network structure of a temporal sequence of stimuli influences the fidelity with which those stimuli are represented in the brain. Healthy adult human participants learned a set of stimulus-motor associations following one of two graph structures. The design of our experiment allowed us to separate regional sensitivity to the structural, stimulus, and motor response components of the task. As expected, whereas the motor response could be decoded from neural representations in postcentral gyrus, the shape of the stimulus could be decoded from lateral occipital cortex. The structure of the graph impacted the nature of neural representations: when the graph was modular as opposed to lattice-like, BOLD representations in visual areas better predicted trial identity in a held-out run and displayed higher intrinsic dimensionality. Our results demonstrate that even over relatively short timescales, graph structure determines the fidelity of event representations as well as the dimensionality of the space in which those representations are encoded. More broadly, our study shows that network context influences the strength of learned neural representations, motivating future work in the design, optimization, and adaptation of network contexts for distinct types of learning over different timescales.

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bioRxiv2022

Measuring brain critical dynamics to inform Brain-Computer Interfaces

Large-scale interactions among multiple brain regions manifest as bursts of activations called neuronal avalanches, which reconfigure according to the task at hand and, hence, might constitute natural candidates to design brain-computer interfaces (BCI). To test this hypothesis, we used source-reconstructed magneto/electroencephalography, during resting state and a motor imagery task performed within a BCI protocol. To track the probability that an avalanche would spread across any two regions we built an avalanche transition matrix (ATM) and demonstrated that the edges whose transition probabilities significantly differed between conditions hinged selectively on premotor regions in all subjects. Furthermore, we showed that the topology of the ATMs allows task-decoding above the current gold standard. Hence, our results suggest that Neuronal Avalanches might capture interpretable differences between tasks that can be used to inform brain-computer interfaces.

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bioRxiv2021

Neurophysiological evidence for cognitive map formation during sequence learning

Humans deftly parse statistics from sequences. Some theories posit that humans learn these statistics by forming cognitive maps, or underlying representations of the latent space which links items in the sequence. Here, an item in the sequence is a node, and the probability of transitioning between two items is an edge. Sequences can then be generated from walks through the latent space, with different spaces giving rise to different sequence statistics. Individual or group differences in sequence learning can be modeled by changing the time scale over which estimates of transition probabilities are built, or in other words, by changing the amount of temporal discounting. Latent space models with temporal discounting bear a resemblance to models of navigation through Euclidean spaces. However, few explicit links have been made between predictions from Euclidean spatial navigation and neural activity during human sequence learning. Here, we use a combination of behavioral modeling and intracranial encephalography (iEEG) recordings to investigate how neural activity might support the formation of space-like cognitive maps through temporal discounting during sequence learning. Specifically, we acquire human reaction times from a sequential reaction time task, to which we fit a model that formulates the amount of temporal discounting as a single free parameter. From the parameter, we calculate each individuals estimate of the latent space. We find that neural activity reflects these estimates mostly in the temporal lobe, including areas involved in spatial navigation. Similar to spatial navigation, we find that low dimensional representations of neural activity allow for easy separation of important features, such as modules, in the latent space. Lastly, we take advantage of the high temporal resolution of iEEG data to determine the time scale on which latent spaces are learned. We find that learning typically happens within the first 500 trials, and is modulated by the underlying latent space and the amount of temporal discounting characteristic of each participant. Ultimately, this work provides important links between behavioral models of sequence learning and neural activity during the same behavior, and contextualizes these results within a broader framework of domain general cognitive maps.

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bioRxiv2021

Alprazolam modulates persistence energy during emotion processing in first-degree relatives of individuals with schizophrenia: a network control study

Schizophrenia is marked by deficits in facial affect processing associated with abnormalities in GABAergic circuitry, deficits also found in first-degree relatives. Facial affect processing involves a distributed network of brain regions including limbic regions like amygdala and visual processing areas like fusiform cortex. Pharmacological modulation of GABAergic circuitry using benzodiazepines like alprazolam can be useful for studying this facial affect processing network and associated GABAergic abnormalities in schizophrenia. Here, we use pharmacological modulation and computational modeling to study the contribution of GABAergic abnormalities toward emotion processing deficits in schizophrenia. Specifically, we apply principles from network control theory to model persistence energy - the control energy required to maintain brain activation states - during emotion identification and recall tasks, with and without administration of alprazolam, in a sample of first-degree relatives and healthy controls. Here, persistence energy quantifies the magnitude of theoretical external inputs during the task. We find that alprazolam increases persistence energy in relatives but not in controls during threatening face processing, suggesting a compensatory mechanism given the relative absence of behavioral abnormalities in this sample of unaffected relatives. Further, we demonstrate that regions in the fusiform and occipital cortices are important for facilitating state transitions during facial affect processing. Finally, we uncover spatial relationships (i) between regional variation in differential control energy (alprazolam versus placebo) and (ii) both serotonin and dopamine neurotransmitter systems, indicating that alprazolam may exert its effects by altering neuromodulatory systems. Together, these findings reveal differences in emotion-processing circuitry associated with genetic vulnerability to schizophrenia.

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bioRxiv2018

White Matter Network Architecture Guides Direct Electrical Stimulation Through Optimal State Transitions

Electrical brain stimulation is currently being investigated as a potential therapy for neurological disease. However, opportunities to optimize and personalize such therapies are challenged by the fact that the beneficial impact (and potential side effects) of focal stimulation on both neighboring and distant regions is not well understood. Here, we use network control theory to build a formal model of brain network function that makes explicit predictions about how stimulation spreads through the brains white matter network and influences large-scale dynamics. We test these predictions using combined electrocorticography (ECoG) and diffusion weighted imaging (DWI) data from patients with medically refractory epilepsy undergoing evaluation for resective surgery, and who volunteered to participate in an extensive stimulation regimen. We posit a specific model-based manner in which white matter tracts constrain stimulation, defining its capacity to drive the brain to new states, including states associated with successful memory encoding. In a first validation of our model, we find that the true pattern of white matter tracts can be used to more accurately predict the state transitions induced by direct electrical stimulation than the artificial patterns of a topological or spatial network null model. We then use a targeted optimal control framework to solve for the optimal energy required to drive the brain to a given state. We show that, intuitively, our model predicts larger energy requirements when starting from states that are farther away from a target memory state. We then suggest testable hypotheses about which structural properties will lead to efficient stimulation for improving memory based on energy requirements. We show that the strength and homogeneity of edges between controlled and uncontrolled nodes, as well as the persistent modal controllability of the stimulated region, predict energy requirements. Our work demonstrates that individual white matter architecture plays a vital role in guiding the dynamics of direct electrical stimulation, more generally offering empirical support for the utility of network control theoretic models of brain response to stimulation.

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bioRxiv2018

Predictive control of electrophysiological network architecture using direct, single-node neurostimulation in humans

Chronically implantable neurostimulation devices are becoming a clinically viable option for treating patients with neurological disease and psychiatric disorders. Neurostimulation offers the ability to probe and manipulate distributed networks of interacting brain areas in dysfunctional circuits. Here, we use tools from network control theory to examine the dynamic reconfiguration of functionally interacting neuronal ensembles during targeted neurostimulation of cortical and subcortical brain structures. By integrating multi-modal intracranial recordings and diffusion tensor imaging from patients with drug-resistant epilepsy, we test hypothesized structural and functional rules that predict altered patterns of synchronized local field potentials. We demonstrate the ability to predictably reconfigure functional interactions depending on stimulation strength and location. Stimulation of areas with structurally weak connections largely modulates the functional hubness of downstream areas and concurrently propels the brain towards more difficult-to-reach dynamical states. By using focal perturbations to bridge large-scale structure, function, and markers of behavior, our findings suggest that stimulation may be tuned to influence different scales of network interactions driving cognition.

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bioRxiv2017

Process reveals structure: How a network is traversed mediates expectations about its architecture

Network science has emerged as a powerful tool through which we can study the higher-order architectural properties of the world around us. How human learners exploit this information remains an essential question. Here, we focus on the temporal constraints that govern such a process. Participants viewed a continuous sequence of images generated by three distinct walks on a modular network. Walks varied along two critical dimensions: their predictability and the density with which they sampled from communities of images. Learners exposed to walks that richly sampled from each community exhibited a sharp increase in processing time upon entry into a new community. This effect was eliminated in a highly regular walk that sampled exhaustively from images in short, successive cycles (i.e., that increasingly minimized uncertainty about the nature of upcoming stimuli). These results demonstrate that temporal organization plays an essential role in how robustly knowledge of network architecture is acquired.

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