arXiv subjects

Benjamin Y. Hayden

Publications and source records attributed to Benjamin Y. Hayden.

7 recordsLinked to original sources

arXiv2026

Neural geometry in the human hippocampus enables generalization across spatial position and gaze

Hippocampal neurons track positions of self, others, and gaze direction. However, it is unclear how their respective neural codes differ enough to avoid confusion while allowing for abstraction. We recorded from populations of hippocampal neurons while participants performed a joystick-controlled virtual prey pursuit task involving multiple moving agents. We found that neurons have mixed selective responses that map positions of self, prey, and predator, as well as gaze. Their codes occupied mostly orthogonal subspaces, but these subspaces geometric structure allowed them to be aligned by simple linear transformations. Moreover, their geometry supported generalization across spatial maps, such that a linear rule learned on one agent transfers to another. This scheme enables reliable individuation and abstraction across both agent identity and viewpoint. Together, these findings suggest that hippocampal spatial knowledge is structured as a family of geometrically related manifolds that can be flexibly aligned to different agents and gaze directions.

q-bio.NC↗

arXiv2023

Semi-orthogonal subspaces for value mediate a tradeoff between binding and generalization

When choosing between options, we must associate their values with the action needed to select them. We hypothesize that the brain solves this binding problem through neural population subspaces. To test this hypothesis, we examined neuronal responses in five reward-sensitive regions in macaques performing a risky choice task with sequential offers. Surprisingly, in all areas, the neural population encoded the values of offers presented on the left and right in distinct subspaces. We show that the encoding we observe is sufficient to bind the values of the offers to their respective positions in space while preserving abstract value information, which may be important for rapid learning and generalization to novel contexts. Moreover, after both offers have been presented, all areas encode the value of the first and second offers in orthogonal subspaces. In this case as well, the orthogonalization provides binding. Our binding-by-subspace hypothesis makes two novel predictions borne out by the data. First, behavioral errors should correlate with putative spatial (but not temporal) misbinding in the neural representation. Second, the specific representational geometry that we observe across animals also indicates that behavioral errors should increase when offers have low or high values, compared to when they have medium values, even when controlling for value difference. Together, these results support the idea that the brain makes use of semi-orthogonal subspaces to bind features together.

q-bio.NC↗

arXiv2023

Subspace orthogonalization as a mechanism for binding values to space

When choosing between options, we must solve an important binding problem. The values of the options must be associated with information about the action needed to select them. We hypothesize that the brain solves this binding problem through use of distinct population subspaces. To test this hypothesis, we examined the responses of single neurons in five reward-sensitive regions in rhesus macaques performing a risky choice task. In all areas, neurons encoded the value of the offers presented on both the left and the right side of the display in semi-orthogonal subspaces, which served to bind the values of the two offers to their positions in space. Supporting the idea that this orthogonalization is functionally meaningful, we observed a session-to-session covariation between choice behavior and the orthogonalization of the two value subspaces: trials with less orthogonalized subspaces were associated with greater likelihood of choosing the less valued option. Further inspection revealed that these semi-orthogonal subspaces arose from a combination of linear and nonlinear mixed selectivity in the neural population. We show this combination of selectivity balances reliable binding with an ability to generalize value across different spatial locations. These results support the hypothesis that semi-orthogonal subspaces support reliable binding, which is essential to flexible behavior in the face of multiple options.

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arXiv2022

The promise of behavioral tracking systems for advancing primate animal welfare

Recent years have witnessed major advances in the ability of computerized systems to track the positions of animals as they move through large and unconstrained environments. These systems have so far been a great boon in the fields of primatology, psychology, neuroscience, and biomedicine. Here, we discuss the promise of these technologies for animal welfare. Their potential benefits include identifying and reducing pain, suffering, and distress in captive populations, improving laboratory animal welfare within the context of the three Rs of animal research (reduction, refinement, and replacement), and applying our understanding of animal behavior to increase the natural behaviors in captive and wild populations facing human impact challenges. We note that these benefits are often incidental to the designed purpose of these tracking systems, a reflection of the fact that animal welfare is not inimical to research progress, but instead, that the aligned interests between basic research and welfare hold great promise for improvements to animal well-being.

q-bio.NC↗

arXiv2021

Self-supervised Secondary Landmark Detection via 3D Representation Learning

Recent technological developments have spurred great advances in the computerized tracking of joints and other landmarks in moving animals, including humans. Such tracking promises important advances in biology and biomedicine. Modern tracking models depend critically on labor-intensive annotated datasets of primary landmarks by non-expert humans. However, such annotation approaches can be costly and impractical for secondary landmarks, that is, ones that reflect fine-grained geometry of animals, and that are often specific to customized behavioral tasks. Due to visual and geometric ambiguity, nonexperts are often not qualified for secondary landmark annotation, which can require anatomical and zoological knowledge. These barriers significantly impede downstream behavioral studies because the learned tracking models exhibit limited generalizability. We hypothesize that there exists a shared representation between the primary and secondary landmarks because the range of motion of the secondary landmarks can be approximately spanned by that of the primary landmarks. We present a method to learn this spatial relationship of the primary and secondary landmarks in three dimensional space, which can, in turn, self-supervise the secondary landmark detector. This 3D representation learning is generic, and can therefore be applied to various multiview settings across diverse organisms, including macaques, flies, and humans.

cs.CV↗

arXiv2021

The population doctrine in cognitive neuroscience

A major shift is happening within neurophysiology: a population doctrine is drawing level with the single-neuron doctrine that has long dominated the field. Population-level ideas have so far had their greatest impact in motor neuroscience, but they hold great promise for resolving open questions in cognition as well. Here, we codify the population doctrine and survey recent work that leverages this view to specifically probe cognition. Our discussion is organized around five core concepts that provide a foundation for population-level thinking: (1) state spaces, (2) manifolds, (3) coding dimensions, (4) subspaces, and (5) dynamics. The work we review illustrates the progress and promise that population neurophysiology holds for cognitive neuroscience$-$for delivering new insight into attention, working memory, decision-making, executive function, learning, and reward processing.

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arXiv2021

The whole prefrontal cortex is premotor cortex

We propose that the entirety of the prefrontal cortex can be seen as fundamentally premotor in nature. By this, we mean that the prefrontal cortex consists of an action abstraction hierarchy whose core function is the potentiation and depotentiation of possible action plans at different levels of granularity. We argue that the apex of the hierarchy should revolve around the process of goal selection, which we posit is inherently a form of abstract action optimization. Anatomical and functional evidence supports the idea that this hierarchy originates on the orbital surface of the brain and extends dorsally to motor cortex. Our view, therefore, positions the orbitofrontal cortex as the central site for the optimization of goal selection policies, and suggests that other proposed roles are aspects of this more general function. We conclude by proposing that the dynamical systems approach, which works well in motor systems, can be extended to the rest of prefrontal cortex. Our proposed perspective will reframe outstanding questions, open up new areas of inquiry, and will align theories of prefrontal function with evolutionary principles.

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