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Geometric constraints on neuronal connectivity facilitate a concise synaptic adhesive code.

ABSTRACT: The nervous system contains trillions of neurons, each forming thousands of synaptic connections. It has been suggested that this complex connectivity is determined by a synaptic "adhesive code," where connections are dictated by a variable set of cell surface proteins, combinations of which form neuronal addresses. The estimated number of neuronal addresses is orders of magnitude smaller than the number of neurons. Here, we show that the limited number of addresses dictates constraints on the possible neuronal network topologies. We show that to encode arbitrary networks, in which each neuron can potentially connect to any other neuron, the number of neuronal addresses needed scales linearly with network size. In contrast, the number of addresses needed to encode the wiring of geometric networks grows only as the square root of network size. The more efficient encoding in geometric networks is achieved through the reutilization of the same addresses in physically independent portions of the network. We also find that ordered geometric networks, in which the same connectivity patterns are iterated throughout the network, further reduce the required number of addresses. We demonstrate our findings using simulated networks and the C. elegans neuronal network. Geometric neuronal connectivity with recurring connectivity patterns have been suggested to confer an evolutionary advantage by saving biochemical resources on the one hand and reutilizing functionally efficient neuronal circuits. Our study suggests an additional advantage of these prominent topological features--the facilitation of the ability to genetically encode neuronal networks given constraints on the number of addresses.

SUBMITTER: Itzkovitz S

PROVIDER: S-EPMC2453736 | biostudies-literature | 2008 Jul

REPOSITORIES: biostudies-literature

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Geometric constraints on neuronal connectivity facilitate a concise synaptic adhesive code.

Itzkovitz Shalev S Baruch Leehod L Shapiro Ehud E Segal Eran E

Proceedings of the National Academy of Sciences of the United States of America 20080626 27

The nervous system contains trillions of neurons, each forming thousands of synaptic connections. It has been suggested that this complex connectivity is determined by a synaptic "adhesive code," where connections are dictated by a variable set of cell surface proteins, combinations of which form neuronal addresses. The estimated number of neuronal addresses is orders of magnitude smaller than the number of neurons. Here, we show that the limited number of addresses dictates constraints on the p ...[more]

PMID: 18583478

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Project description:BackgroundNeurons are dynamically coupled with each other through neurite-mediated adhesion during development. Understanding the collective behavior of neurons in circuits is important for understanding neural development. While a number of genetic and activity-dependent factors regulating neuronal migration have been discovered on single cell level, systematic study of collective neuronal migration has been lacking. Various biological systems are shown to be self-organized, and it is not known if neural circuit assembly is self-organized. Besides, many of the molecular factors take effect through spatial patterns, and coupled biological systems exhibit emergent property in response to geometric constraints. How geometric constraints of the patterns regulate neuronal migration and circuit assembly of neurons within the patterns remains unexplored.Methodology/principal findingsWe established a two-dimensional model for studying collective neuronal migration of a circuit, with hippocampal neurons from embryonic rats on Matrigel-coated self-assembled monolayers (SAMs). When the neural circuit is subject to geometric constraints of a critical scale, we found that the collective behavior of neuronal migration is spatiotemporally coordinated. Neuronal somata that are evenly distributed upon adhesion tend to aggregate at the geometric center of the circuit, forming mono-clusters. Clustering formation is geometry-dependent, within a critical scale from 200 µm to approximately 500 µm. Finally, somata clustering is neuron-type specific, and glutamatergic and GABAergic neurons tend to aggregate homo-philically.Conclusions/significanceWe demonstrate self-organization of neural circuits in response to geometric constraints through spatiotemporally coordinated neuronal migration, possibly via mechanical coupling. We found that such collective neuronal migration leads to somata clustering, and mono-cluster appears when the geometric constraints fall within a critical scale. The discovery of geometry-dependent collective neuronal migration and the formation of somata clustering in vitro shed light on neural development in vivo.

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Geometric constraints on neuronal connectivity facilitate a concise synaptic adhesive code.

Publications

Geometric constraints on neuronal connectivity facilitate a concise synaptic adhesive code.

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