Geometric Stability of Neural Population Codes: Regional Variation, Behavioral Relevance, and Circuit Dependence

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Summary

This paper introduces geometric stability as a measure of how reliably pairwise stimulus distances reproduce across trials, demonstrating its behavioral relevance and circuit dependence across brain regions, with an attractor network model explaining its emergence.

Current models of representational reliability in neural populations focus on temporal stability: whether population centroids are preserved across sessions and days. This framing leaves a fundamental question unanswered: how reliably does the pairwise distance structure among stimuli reproduce across independent observations within a session? We argue that this property, geometric stability, constitutes an independent axis of representational analysis that existing frameworks do not capture. We formalize geometric stability as the Spearman rank correlation between split-half representational dissimilarity matrices (Shesha) and show that it is empirically dissociable from both temporal stability and decoding accuracy. Across 229 area-session observations spanning 68 brain regions in a visual discrimination task (Steinmetz et al. 2019), geometric stability predicts trial-by-trial neural-behavioral coupling (ρ= 0.18, p = 0.005) while centroid drift does not (ρ= 0.002, p = 0.976). The regional hierarchy, with striatum most stable (S = 0.44) and hippocampus least (S = 0.19), runs roughly opposite to the temporal stability hierarchy. Directionally consistent olfactory data (Bolding \& Franks 2018) motivate an attractor network model in which recurrent excitatory coupling amplifies split-half RDM consistency by completing stimulus patterns from sparse feedforward input (ρ= +0.64, p = 0.010), providing a circuit-level account of how geometric stability emerges. These results establish geometric stability as a functionally relevant, circuit-dependent property of neural population codes, orthogonal to temporal drift measures and complementary to recent accounts of how recurrent connectivity balances representational stability with sequential dynamics in hippocampal circuits.
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Source: https://huggingface.co/papers/2606.29655

Abstract

Geometric stability measures the consistency of pairwise stimulus distances across trials, revealing a distinct aspect of neural representation that differs from temporal stability and decoding accuracy.

Current models ofrepresentational reliabilityin neural populations focus ontemporal stability: whetherpopulation centroidsare preserved across sessions and days. This framing leaves a fundamental question unanswered: how reliably does thepairwise distance structureamong stimuli reproduce across independent observations within a session? We argue that this property,geometric stability, constitutes an independent axis of representational analysis that existing frameworks do not capture. We formalizegeometric stabilityas theSpearman rank correlationbetweensplit-half representational dissimilarity matrices(Shesha) and show that it is empirically dissociable from bothtemporal stabilityand decoding accuracy. Across 229 area-session observations spanning 68 brain regions in a visual discrimination task (Steinmetz et al. 2019),geometric stabilitypredictstrial-by-trial neural-behavioral coupling(ρ= 0.18, p = 0.005) while centroid drift does not (ρ= 0.002, p = 0.976). The regional hierarchy, with striatum most stable (S = 0.44) and hippocampus least (S = 0.19), runs roughly opposite to thetemporal stabilityhierarchy. Directionally consistent olfactory data (Bolding \& Franks 2018) motivate anattractor network modelin whichrecurrent excitatory couplingamplifies split-half RDM consistency by completing stimulus patterns from sparsefeedforward input(ρ= +0.64, p = 0.010), providing a circuit-level account of howgeometric stabilityemerges. These results establishgeometric stabilityas a functionally relevant, circuit-dependent property of neural population codes, orthogonal to temporal drift measures and complementary to recent accounts of how recurrent connectivity balances representational stability with sequential dynamics inhippocampal circuits.

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