Biology subjects

Love, B. C.

Publications and source records attributed to Love, B. C..

18 recordsLinked to original sources

bioRxiv2024

Distinct hippocampal mechanisms support concept formation and updating

Learning systems must constantly decide whether to create new representations or update existing ones. For example, a child learning that a bat is a mammal and not a bird would be best served by creating a new representation, whereas updating may be best when encountering a second similar bat. Characterizing the neural dynamics that underlie these complementary memory operations requires identifying the exact moments when each operation occurs. We address this challenge by interrogating fMRI brain activation with a computational learning model that predicts trial-by-trial when memories are created versus updated. We found distinct neural engagement in anterior hippocampus and ventral striatum for model-predicted memory create and update events during early learning. Notably, the degree of this effect in hippocampus, but not ventral striatum, significantly related to learning outcome. Hippocampus additionally showed distinct patterns of functional coactivation with ventromedial prefrontal cortex and angular gyrus during memory creation and premotor cortex during memory updating. These findings suggest that complementary memory functions, as formalized in computational learning models, underlie the rapid formation of novel conceptual knowledge, with the hippocampus and its interactions with frontoparietal circuits playing a crucial role in successful learning. Significance statementHow do we reconcile new experiences with existing knowledge? Prominent theories suggest that novel information is either captured by creating new memories or leveraged to update existing memories, yet empirical support of how these distinct memory operations unfold during learning is limited. Here, we combine computational modeling of human learning behaviour with functional neuroimaging to identify moments of memory formation and updating and characterize their neural signatures. We find that both hippocampus and ventral striatum are distinctly engaged when memories are created versus updated; however, it is only hippocampus activation that is associated with learning outcomes. Our findings motivate a key theoretical refinement that positions hippocampus is a key player in building organized memories from the earliest moments of learning.

neuroscience↗

bioRxiv2024

The inevitability and superfluousness of cell types in spatial cognition

Discoveries of functional cell types, exemplified by the cataloging of spatial cells in the hippocampal formation, are heralded as scientific breakthroughs. We question whether the identification of cell types based on human intuitions has scientific merit and suggest that "spatial cells" may arise in non-spatial computations of sufficient complexity. We show that deep neural networks (DNNs) for object recognition, which lack spatial grounding, contain numerous units resembling place, border, and head-direction cells. Strikingly, even untrained DNNs with randomized weights contained such units and support decoding of spatial information. Moreover, when these "spatial" units are excluded, spatial information can be decoded from the remaining DNN units, which highlights the superfluousness of cell types to spatial cognition. Now that large-scale simulations are feasible, the complexity of the brain should be respected and intuitive notions of cell type, which can be misleading and arise in any complex network, should be relegated to history.

neuroscience↗

bioRxiv2023

Adaptive stretching of representations across brain regions and deep learning model layers

Prefrontal cortex (PFC) is known to modulate the visual system to favor goal-relevant information by accentuating task-relevant stimulus dimensions. Does the brain broadly re-configures itself to optimize performance by stretching visual representations along task-relevant dimensions? We considered a task that required monkeys to selectively attend on a trial-by-trial basis to one of two dimensions (color or motion direction) to make a decision. Except for V4 (color bound) and MT (motion bound), the brain radically re-configured itself to stretch representations along task-relevant dimensions in lateral PFC, frontal eye fields (FEF), lateral intraparietal cortex (LIP), and inferotemporal cortex (IT). Spike timing was crucial to this code. A deep learning model was trained on the same visual input and rewards as the monkeys. Despite lacking an explicit selective attention or other control mechanism, the model displayed task-relevant stretching as a consequence of error minimization, indicating that stretching is an adaptive strategy.

neuroscience↗

bioRxiv2023

A controller-peripheral architecture and costly energy principle for learning

Complex behavior is supported by the coordination of multiple brain regions. How do brain regions coordinate absent a homunculus? We propose coordination is achieved by a controller-peripheral architecture in which peripherals (e.g., the ventral visual stream) aim to supply needed inputs to their controllers (e.g., the hippocampus and prefrontal cortex) while expending minimal resources. We developed a formal model within this framework to address how multiple brain regions coordinate to support rapid learning from a few example images. The model captured how higher-level activity in the controller shaped lower-level visual representations, affecting their precision and sparsity in a manner that paralleled brain measures. In particular, the peripheral encoded visual information to the extent needed to support the smooth operation of the controller. Alternative models optimized by gradient descent irrespective of architectural constraints could not account for human behavior or brain responses, and, typical of standard deep learning approaches, were unstable trial-by-trial learners. While previous work offered accounts of specific faculties, such as perception, attention, and learning, the controller-peripheral approach is a step toward addressing next generation questions concerning how multiple faculties coordinate.

neuroscience↗

bioRxiv2022

A multi-level account of hippocampal function from behaviour to neurons

A complete neuroscience requires multi-level theories that address phenomena ranging from higher-level cognitive behaviors to activities within a cell. A levels-of-mechanism approach that decomposes a higher-level model of cognition and behavior into component mechanisms provides a coherent and richer understanding of the system than any level alone. Toward this end, we decomposed a cognitive model into neuron-like units using a neural flocking approach that parallels recurrent hippocampal activity. Neural flocking coordinates units that collectively form higher-level mental constructs. The decomposed model suggested how brain-scale neural populations coordinate to form assemblies encoding concept and spatial representations, and why so many neurons are needed for robust performance at the cognitive level. This multi-level explanation provides a way to understand how cognition and symbol-like representations are supported by coordinated neural populations (assemblies) formed through learning.

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bioRxiv2021

Directly interfacing brain and deep networks exposes non-hierarchical visual processing

One reason the mammalian visual system is viewed as hierarchical, such that successive stages of processing contain ever higher-level information, is because of functional correspondences with deep convolutional neural networks (DCNNs). However, these correspondences between brain and model activity involve shared, not task-relevant, variance. We propose a stricter test of correspondence: If a DCNN layer corresponds to a brain region, then replacing model activity with brain activity should successfully drive the DCNNs object recognition decision. Using this approach on three datasets, we found all regions along the ventral visual stream best corresponded with later model layers, indicating all stages of processing contained higher-level information about object category. Time course analyses suggest long-range recurrent connections transmit object class information from late to early visual areas.

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bioRxiv2021

A neural network account of memory replay and knowledge consolidation

Replay can consolidate memories through offline neural reactivation related to past experiences. Category knowledge is learned across multiple experiences, and its subsequent generalisation is promoted by consolidation and replay during rest and sleep. However, aspects of replay are difficult to determine from neuroimaging studies. We provided insights into category knowledge replay by simulating these processes in a neural network which approximated the roles of the human ventral visual stream and hippocampus. Generative replay, akin to imagining new category instances, facilitated generalisation to new experiences. Consolidation-related replay may therefore help to prepare us for the future as much as remember the past. Generative replay was more effective in later network layers functionally similar to the lateral occipital cortex than layers corresponding to early visual cortex, drawing a distinction between neural replay and its relevance to consolidation. Category replay was most beneficial for newly acquired knowledge, suggesting replay helps us adapt to changes in our environment. Finally, we present a novel mechanism for the observation that the brain selectively consolidates weaker information; a reinforcement learning process in which categories were replayed according to their contribution to network performance. This reinforces the idea of consolidation-related replay as an active rather than passive process.

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bioRxiv2020

The neural link between subjective value and decision entropy

AO_SCPLOWBSTRACTC_SCPLOWRecent work has considered the relationship between value and confidence in both behavior and neural representation. Here we evaluated whether the brain organizes value and confidence signals in a systematic fashion that reflects the overall desirability of options. If so, regions that respond to either increases or decreases in both value and confidence should be widespread. We strongly confirmed these predictions through a model-based fMRI analysis of a mixed gambles task that assessed subjective value (SV) and inverse decision entropy (iDE), which is related to confidence. Purported value areas more strongly signalled iDE than SV, underscoring how intertwined value and confidence are. A gradient tied to the desirability of actions transitioned from positive SV and iDE in ventromedial prefrontal cortex to negative SV and iDE in dorsal medial prefrontal cortex. This alignment of SV and iDE signals could support retrospective evaluation to guide learning and subsequent decisions.

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bioRxiv2020

Abstract neural representations of category membership beyond information coding stimulus or response

For decades, researchers have debated whether mental representations are symbolic or grounded in sensory inputs and motor programs. Certainly, aspects of mental representations are grounded. However, does the brain also contain abstract concept representations that mediate between perception and action in a flexible manner not tied to the details of sensory inputs and motor programs? Such conceptual pointers would be useful when concept remain constant despite changes in appearance and associated actions. We evaluated whether human participants acquire such representations using functional magnetic resonance imaging (fMRI). Participants completed a probabilistic concept learning task in which sensory, motor, and category variables were not perfectly coupled nor entirely independent, making it possible to observe evidence for abstract representations or purely grounded representations. To assess how the learned concept structure is represented in the brain, we examined brain regions implicated in flexible cognition (e.g., prefrontal and parietal cortex) that are most likely to encode an abstract representation removed from sensory-motor details. We also examined sensory-motor regions that might encode grounded sensory-motor based representations tuned for categorization. Using a cognitive model to estimate participants category rule and multivariate pattern analysis of fMRI data, we found left prefrontal cortex and MT coded for category in absence of information coding for stimulus or response. Because category was based on the stimulus, finding an abstract representation of category was not inevitable. Our results suggest that certain brain areas support categorization behaviour by constructing concept representations in a format akin to a symbol that differs from stimulus-motor codes.

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bioRxiv2019

Levels of Representation in a Deep Learning Model of Categorization

Deep convolutional neural networks (DCNNs) rival humans in object recognition. The layers (or levels of representation) in DCNNs have been successfully aligned with processing stages along the ventral stream for visual processing. Here, we propose a model of concept learning that uses visual representations from these networks to build memory representations of novel categories, which may rely on the medial temporal lobe (MTL) and medial prefrontal cortex (mPFC). Our approach opens up two possibilities: a) formal investigations can involve photographic stimuli as opposed to stimuli handcrafted and coded by the experimenter; b) model comparison can determine which level of representation within a DCNN a learner is using during categorization decisions. Pursuing the latter point, DCNNs suggest that the shape bias in children relies on representations at more advanced network layers whereas a learner that relied on lower network layers would display a color bias. These results confirm the role of natural statistics in the shape bias (i.e., shape is predictive of category membership) while highlighting that the type of statistics matter, i.e., those from lower or higher levels of representation. We use the same approach to provide evidence that pigeons performing seemingly sophisticated categorization of complex imagery may in fact be relying on representations that are very low-level (i.e., retinotopic). Although complex features, such as shape, relatively predominate at more advanced network layers, even simple features, such as spatial frequency and orientation, are better represented at the more advanced layers, contrary to a standard hierarchical view.

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bioRxiv2018

Exploration in the wild

Making good decisions requires people to appropriately explore their available options and generalize what they have learned. While computational models have successfully explained exploratory behavior in constrained laboratory tasks, it is unclear to what extent these models generalize to complex real world choice problems. We investigate the factors guiding exploratory behavior in a data set consisting of 195,333 customers placing 1,613,967 orders from a large online food delivery service. We find important hallmarks of adaptive exploration and generalization, which we analyze using computational models. We find evidence for several theoretical predictions: (1) customers engage in uncertainty-directed exploration, (2) they adjust their level of exploration to the average restaurant quality in a city, and (3) they use feature-based generalization to guide exploration towards promising restaurants. Our results provide new evidence that people use sophisticated strategies to explore complex, real-world environments.

animal behavior and cognition↗

bioRxiv2018

Measures of neural similarity

One fundamental question is what makes two brain states similar. For example, what makes the activity in visual cortex elicited from viewing a robin similar to a sparrow? One common assumption in fMRI analysis is that neural similarity is described by Pearson correlation. However, there are a host of other possibilities, including Minkowski and Mahalanobis measures, with each differing in its mathematical, theoretical, neural computational assumptions. Moreover, the operable measures may vary across brain regions and tasks. Here, we evaluated which of several competing similarity measures best captured neural similarity. Our technique uses a decoding approach to assess the information present in a brain region and the similarity measures that best correspond to the classifiers confusion matrix are preferred. Across two published fMRI datasets, we found the preferred neural similarity measures were common across brain regions, but differed across tasks. Moreover, Pearson correlation was consistently surpassed by alternatives.

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bioRxiv2018

A non-spatial account of place and grid cells based on clustering models of concept learning

One view is that conceptual knowledge is organized using the circuitry in the medial temporal lobe (MTL) that supports spatial processing and navigation. In contrast, we find that a domain-general learning algorithm explains key findings in both spatial and conceptual domains. When the clustering model is applied to spatial navigation tasks, so called place and grid cell-like representations emerge because of the relatively uniform distribution of possible inputs in these tasks. The same mechanism applied to conceptual tasks, where the overall space can be higher-dimensional and sampling sparser, leads to representations more aligned with human conceptual knowledge. Although the types of memory supported by the MTL are superficially dissimilar, the information processing steps appear shared. Our account suggests that the MTL uses a general-purpose algorithm to learn and organize context-relevant information in a useful format, rather than relying on navigation-specific neural circuitry.

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bioRxiv2018

Dynamic integration of conceptual information during learning

The development and application of concepts is a critical component of cognition. Although concepts can be formed on the basis of simple perceptual or semantic features, conceptual representations can also capitalize on similarities across feature relationships. By representing these types of higher-order relationships, concepts can simplify the learning problem and facilitate decisions. Despite this, little is known about the neural mechanisms that support the construction and deployment of these kinds of higher-order concepts during learning. To address this question, we combined a carefully designed associative learning task with computational model-based functional magnetic resonance imaging (fMRI). Participants were scanned as they learned and made decisions about sixteen pairs of cues and associated outcomes. Associations were structured such that individual cues shared feature relationships, operationalized as shared patterns of cue pair-outcome associations. In order to capture the large number of possible conceptual representational structures that participants might employ and to evaluate how conceptual representations are used during learning, we leveraged a well-specified Bayesian computational model of category learning [1]. Behavioral and model-based results revealed that participants who displayed a tendency to link experiences in memory benefitted from faster learning rates, suggesting that the use of the conceptual structure in the task facilitated decisions about cue pair-outcome associations. Model-based fMRI analyses revealed that trial-by-trial integration of cue information into higher-order conceptual representations was supported by an anterior temporal (AT) network of regions previously implicated in representing complex conjunctions of features and meaning-based information.

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bioRxiv2018

Occipitotemporal Representations Reflect Individual Differences in Conceptual Knowledge

Through selective attention, decision-makers can learn to ignore behaviorally-irrelevant stimulus dimensions. This can improve learning and increase the perceptual discriminability of relevant stimulus information. To account for this effect, popular contemporary cognitive models of categorization typically include of attentional parameters, which provide information about the importance of each stimulus dimension in decision-making. The effect of these parameters on psychological representation is often described geometrically, such that perceptual differences over relevant psychological dimensions are accentuated (or stretched), and differences over irrelevant dimensions are down-weighted (or compressed). In sensory and association cortex, representations of stimulus features are known to covary with their behavioral relevance. Although this implies that neural representational space might closely resemble that hypothesized by formal categorization theory, to date, attentional effects in the brain have been demonstrated through powerful experimental manipulations (e.g., contrasts between relevant and irrelevant features). This approach sidesteps the role of idiosyncratic conceptual knowledge in guiding attention to useful information sources. To bridge this divide, we used formal categorization models, which were fit to behavioral data, to make inferences about the concepts and strategies used by individual participants during decision-making. We found that when greater attentional weight was devoted to a particular visual feature (e.g., \"color\"), its value (e.g., \"red\") was more accurately decoded from occipitotemporal cortex. We additionally found that this effect was sufficiently sensitive to reflect individual differences in conceptual knowledge. The results indicate that occipitotemporal stimulus representations are embedded within a space closely resembling that proposed by classic categorization models.

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bioRxiv2017

Active learning reveals underlying decision strategies

One key question is whether people rely on frugal heuristics or full-information strategies when making preference decisions. We propose a novel method, model-based active learning, to answer whether people conform more to a rank-based heuristic (Take-The-Best) or a weight-based full-information strategy (logistic regression). Our method eclipses traditional model comparison techniques by using information theory to characterize model predictions for how decision makers should actively sample information. These analyses capture how sampling affects learning and how learning affects decisions on subsequent trials. We develop and test model-based active learning algorithms for both Take-The-Best and logistic regression. Our findings reveal that people largely follow a weight-based learning strategy rather than a rank-based strategy, even in cases where their preference decisions are better predicted by the Take-The-Best heuristic. This finding suggests that people may have more refined knowledge than is revealed by their preference decisions, but which can be revealed by their information sampling behavior. We argue that model-based active learning is an effective and sensitive method for model selection that expands the basis for model comparison.

animal behavior and cognition↗

bioRxiv2017

Estimating the functional dimensionality of neural representations

Recent advances in multivariate fMRI analysis stress the importance of information inherent to voxel patterns. Key to interpreting these patterns is estimating the underlying dimensionality of neural representations. Dimensions may correspond to psychological dimensions, such as length and orientation, or involve other coding schemes. Unfortunately, the noise structure of fMRI data inflates dimensionality estimates and thus makes it difficult to assess the true underlying dimensionality of a pattern. To address this challenge, we developed a novel approach to identify brain regions that carry reliable task-modulated signal and to derive an estimate of the signals functional dimensionality. We combined singular value decomposition with cross-validation to find the best low-dimensional projection of a pattern of voxel-responses at a single-subject level. Goodness of the low-dimensional reconstruction is measured as Pearson correlation with a test set, which allows to test for significance of the low-dimensional reconstruction across participants. Using hierarchical Bayesian modeling, we derive the best estimate and associated uncertainty of underlying dimensionality across participants. We validated our method on simulated data of varying underlying dimensionality, showing that recovered dimensionalities match closely true dimensionalities. We then applied our method to three published fMRI data sets all involving processing of visual stimuli. The results highlight three possible applications of estimating the functional dimensionality of neural data. Firstly, it can aid evaluation of model-based analyses by revealing which areas express reliable, task-modulated signal that could be missed by specific models. Secondly, it can reveal functional differences across brain regions. Thirdly, knowing the functional dimensionality allows assessing task-related differences in the complexity of neural patterns.

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bioRxiv2017

Medial prefrontal cortex compresses concept representations through learning

Prefrontal cortex (PFC) is thought to support the ability to focus on goal-relevant information by filtering out irrelevant information, a process akin to dimensionality reduction. Here, we test this dimensionality reduction hypothesis by combining a data-driven approach to characterizing the complexity of neural representation with a theoretically-supported computational model of learning. We find strong evidence of goal-directed dimensionality reduction within human ventromedial PFC during learning. Importantly, by using model predictions of each participants attentional strategies during learning, we find that that the degree of neural compression predicts an individuals ability to selectively attend to concept-specific information. These findings suggest a domain-general mechanism of learning through compression in ventromedial PFC.

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