Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex

Satoshi Kuroki; Takamasa Yoshida; Hidekazu Tsutsui; Mizuho Iwama; Reiko Ando; Takayuki Michikawa; Atsushi Miyawaki; Toshio Ohshima; Shigeyoshi Itohara

doi:10.1016/j.celrep.2018.02.056

Excitatory Neuronal Hubs Configure Multisensory Integration of Slow Waves in Association Cortex

Cell Rep. 2018 Mar 13;22(11):2873-2885. doi: 10.1016/j.celrep.2018.02.056.

Authors

Satoshi Kuroki¹, Takamasa Yoshida², Hidekazu Tsutsui³, Mizuho Iwama², Reiko Ando², Takayuki Michikawa⁴, Atsushi Miyawaki⁵, Toshio Ohshima⁶, Shigeyoshi Itohara⁷

Affiliations

¹ Laboratory for Behavioral Genetics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan; Laboratory for Molecular Brain Science, Department of Life Science and Medical Bioscience, Waseda University, Tokyo 169-8555, Japan.
² Laboratory for Behavioral Genetics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan.
³ Laboratory for Cell Function Dynamics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan; Department of Material Science, Japan Advanced Institute of Science and Technology, Nomi, Ishikawa 923-1292, Japan.
⁴ Laboratory for Cell Function Dynamics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan; Biotechnological Optics Research Team, RIKEN Center for Advanced Photonics, Wako, Saitama 351-0198, Japan.
⁵ Laboratory for Cell Function Dynamics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan.
⁶ Laboratory for Molecular Brain Science, Department of Life Science and Medical Bioscience, Waseda University, Tokyo 169-8555, Japan.
⁷ Laboratory for Behavioral Genetics, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan. Electronic address: [email protected].

PMID: 29539417
DOI: 10.1016/j.celrep.2018.02.056

Abstract

Multisensory integration (MSI) is a fundamental emergent property of the mammalian brain. During MSI, perceptual information encoded in patterned activity is processed in multimodal association cortex. The systems-level neuronal dynamics that coordinate MSI, however, are unknown. Here, we demonstrate intrinsic hub-like network activity in the association cortex that regulates MSI. We engineered calcium reporter mouse lines based on the fluorescence resonance energy transfer sensor yellow cameleon (YC2.60) expressed in excitatory or inhibitory neurons. In medial and parietal association cortex, we observed spontaneous slow waves that self-organized into hubs defined by long-range excitatory and local inhibitory circuits. Unlike directional source/sink-like flows in sensory areas, medial/parietal excitatory and inhibitory hubs had net-zero balanced inputs. Remarkably, multisensory stimulation triggered rapid phase-locking mainly of excitatory hub activity persisting for seconds after the stimulus offset. Therefore, association cortex tends to form balanced excitatory networks that configure slow-wave phase-locking for MSI. VIDEO ABSTRACT.

Keywords: association cortex; cortical slow waves; excitatory neuron; fluorescence resonance energy transfer; inhibitory neuron; mouse; multisensory integration; phase locking; spontaneous activity; wide-field calcium imaging.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Cerebral Cortex / cytology
Cerebral Cortex / physiology*
Mice
Neurons / physiology*