Modular architecture facilitates noise-driven control of synchrony in neuronal networks

Author:

Yamamoto Hideaki12ORCID,Spitzner F. Paul3ORCID,Takemuro Taiki14,Buendía Victor567ORCID,Murota Hakuba12ORCID,Morante Carla89,Konno Tomohiro10ORCID,Sato Shigeo12ORCID,Hirano-Iwata Ayumi12411ORCID,Levina Anna56,Priesemann Viola312ORCID,Muñoz Miguel A.713ORCID,Zierenberg Johannes3ORCID,Soriano Jordi89ORCID

Affiliation:

1. Research Institute of Electrical Communication (RIEC), Tohoku University, Sendai, Japan.

2. Graduate School of Engineering, Tohoku University, Sendai, Japan.

3. Max Planck Institute for Dynamics and Self-Organization, Göttingen, Germany.

4. Graduate School of Biomedical Engineering, Tohoku University, Sendai, Japan.

5. Max Planck Institute for Biological Cybernetics, Tübingen, Germany.

6. Department of Computer Science, University of Tübingen, Tübingen, Germany.

7. Departamento de Electromagnetismo y Física de la Materia, Universidad de Granada, Granada, Spain.

8. Departament de Física de la Matèria Condensada, Universitat de Barcelona, Barcelona, Spain.

9. Universitat de Barcelona Institute of Complex Systems (UBICS), Barcelona, Spain.

10. Graduate School of Pharmaceutical Sciences, Tohoku University, Sendai, Japan.

11. Advanced Institute for Materials Research (WPI-AIMR), Tohoku University, Sendai, Japan.

12. Institute for the Dynamics of Complex Systems, University of Göttingen, Göttingen, Germany.

13. Instituto Carlos I de Física Teórica y Computacional, Universidad de Granada, Granada, Spain.

Abstract

High-level information processing in the mammalian cortex requires both segregated processing in specialized circuits and integration across multiple circuits. One possible way to implement these seemingly opposing demands is by flexibly switching between states with different levels of synchrony. However, the mechanisms behind the control of complex synchronization patterns in neuronal networks remain elusive. Here, we use precision neuroengineering to manipulate and stimulate networks of cortical neurons in vitro, in combination with an in silico model of spiking neurons and a mesoscopic model of stochastically coupled modules to show that (i) a modular architecture enhances the sensitivity of the network to noise delivered as external asynchronous stimulation and that (ii) the persistent depletion of synaptic resources in stimulated neurons is the underlying mechanism for this effect. Together, our results demonstrate that the inherent dynamical state in structured networks of excitable units is determined by both its modular architecture and the properties of the external inputs.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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