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Global organization of neuronal activity only requires unstructured local connectivity.

ABSTRACT: Modern electrophysiological recordings simultaneously capture single-unit spiking activities of hundreds of neurons spread across large cortical distances. Yet, this parallel activity is often confined to relatively low-dimensional manifolds. This implies strong coordination also among neurons that are most likely not even connected. Here, we combine in vivo recordings with network models and theory to characterize the nature of mesoscopic coordination patterns in macaque motor cortex and to expose their origin: We find that heterogeneity in local connectivity supports network states with complex long-range cooperation between neurons that arises from multi-synaptic, short-range connections. Our theory explains the experimentally observed spatial organization of covariances in resting state recordings as well as the behaviorally related modulation of covariance patterns during a reach-to-grasp task. The ubiquity of heterogeneity in local cortical circuits suggests that the brain uses the described mechanism to flexibly adapt neuronal coordination to momentary demands.

SUBMITTER: Dahmen D

PROVIDER: S-EPMC8776256 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Global organization of neuronal activity only requires unstructured local connectivity.

Dahmen David D Layer Moritz M Deutz Lukas L Dąbrowska Paulina Anna PA Voges Nicole N von Papen Michael M Brochier Thomas T Riehle Alexa A Diesmann Markus M Grün Sonja S Helias Moritz M

eLife 20220120

Modern electrophysiological recordings simultaneously capture single-unit spiking activities of hundreds of neurons spread across large cortical distances. Yet, this parallel activity is often confined to relatively low-dimensional manifolds. This implies strong coordination also among neurons that are most likely not even connected. Here, we combine in vivo recordings with network models and theory to characterize the nature of mesoscopic coordination patterns in macaque motor cortex and to exp ...[more]

PMID: 35049496

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Project description:How the connectivity of cortical networks determines the neural dynamics and the resulting computations is one of the key questions in neuroscience. Previous works have pursued two complementary approaches to quantify the structure in connectivity. One approach starts from the perspective of biological experiments where only the local statistics of connectivity motifs between small groups of neurons are accessible. Another approach is based instead on the perspective of artificial neural networks where the global connectivity matrix is known, and in particular its low-rank structure can be used to determine the resulting low-dimensional dynamics. A direct relationship between these two approaches is however currently missing. Specifically, it remains to be clarified how local connectivity statistics and the global low-rank connectivity structure are inter-related and shape the low-dimensional activity. To bridge this gap, here we develop a method for mapping local connectivity statistics onto an approximate global low-rank structure. Our method rests on approximating the global connectivity matrix using dominant eigenvectors, which we compute using perturbation theory for random matrices. We demonstrate that multi-population networks defined from local connectivity statistics for which the central limit theorem holds can be approximated by low-rank connectivity with Gaussian-mixture statistics. We specifically apply this method to excitatory-inhibitory networks with reciprocal motifs, and show that it yields reliable predictions for both the low-dimensional dynamics, and statistics of population activity. Importantly, it analytically accounts for the activity heterogeneity of individual neurons in specific realizations of local connectivity. Altogether, our approach allows us to disentangle the effects of mean connectivity and reciprocal motifs on the global recurrent feedback, and provides an intuitive picture of how local connectivity shapes global network dynamics.

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Global organization of neuronal activity only requires unstructured local connectivity.

Publications

Global organization of neuronal activity only requires unstructured local connectivity.

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