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

• Published in: Cell reports (Cambridge) Vol. 22; no. 11; pp. 2873 - 2885
• Main Authors: Kuroki, Satoshi, Yoshida, Takamasa, Tsutsui, Hidekazu, Iwama, Mizuho, Ando, Reiko, Michikawa, Takayuki, Miyawaki, Atsushi, Ohshima, Toshio, Itohara, Shigeyoshi
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 13.03.2018; Elsevier
• Subjects: Animals; association cortex; Cerebral Cortex - cytology; Cerebral Cortex - physiology; cortical slow waves; excitatory neuron; fluorescence resonance energy transfer; inhibitory neuron; Mice; mouse; multisensory integration; Neurons - physiology; phase locking; spontaneous activity; wide-field calcium imaging; mouse; excitatory neuron; cortical slow waves; multisensory integration; association cortex; fluorescence resonance energy transfer; spontaneous activity; inhibitory neuron; phase locking; wide-field calcium imaging
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2018.02.056

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. [Display omitted] [Display omitted] •Yellow cameleon mouse lines enabled wide-field cell-type-specific cortical imaging•Spontaneous slow waves formed balanced neuronal hubs in association cortical areas•Slow-wave flows in excitatory hubs were phase-locked during multisensory inputs•Balanced excitatory inputs in cortical hubs may coordinate multimodal integration Kuroki et al. performed cell-type-specific, wide-field FRET-based calcium imaging to visualize cortical network activity induced by multisensory inputs. They observed phase-locking of cortical slow waves in excitatory neuronal hubs in association cortical areas that may underlie multisensory integration.