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The claustrum coordinates cortical slow-wave activity

Nature Neuroscience volume 23, pages 741–753 (2020)Cite this article

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Abstract

During sleep and awake rest, the neocortex generates large-scale slow-wave (SW) activity. Here, we report that the claustrum coordinates neocortical SW generation. We established a transgenic mouse line that enabled the genetic interrogation of a subpopulation of claustral glutamatergic neurons. These neurons received inputs from and sent outputs to widespread neocortical areas. The claustral neuronal firings mostly correlated with cortical SW activity. In vitro optogenetic stimulation of the claustrum induced excitatory postsynaptic responses in most neocortical neurons, but elicited action potentials primarily in inhibitory interneurons. In vivo optogenetic stimulation induced a synchronized down-state featuring prolonged silencing of neural activity in all layers of many cortical areas, followed by a down-to-up state transition. In contrast, genetic ablation of claustral neurons attenuated SW activity in the frontal cortex. These results demonstrate a crucial role of claustral neurons in synchronizing inhibitory interneurons across wide cortical areas for the spatiotemporal coordination of SW activity.

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Fig. 1: Characterization of Cre-expressing neurons in Cla-Cre transgenic mice.
Fig. 2: Genetic neural circuit mapping of claustrum input–output patterning.
Fig. 3: Claustral activation drives a cortical fast-spiking interneuron network.
Fig. 4: Claustral neurons are active during neocortical SW activity.
Fig. 5: Optogenetic stimulation of claustrum induces a neocortical down-state.
Fig. 6: Optogenetic stimulation of the claustrum induces widespread SW activity in the neocortex.
Fig. 7: Claustrum ablation attenuates frontal cortex SW activity.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

The custom-written analysis code is available from the corresponding author upon reasonable request.

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Acknowledgements

We thank S. Tonegawa for valuable comments; C. Yokoyama for critical reading of the manuscript; H. Hioki (Juntendo University), J. Sohn and S. Okamoto (Kyoto University) for PV/myrGFP-LDLRct transgenic mice; I. R. Wickersham (MIT), H. S. Seung (Princeton University) and E. M. Callaway (Salk Institute) for modified rabies virus; K. Deisserroth (Stanford University) and E. S. Boyden (MIT) for AAV plasmids; S. Amemiya for help in statistical analyses; S. Mitsui, Y. Mishima and RIKEN CBS Research Resources Division for technical assistance; and members of the Yoshihara Lab for discussion. This work was supported by research funds from RIKEN to Y.Y., grants-in-aid for Scientific Research on Innovative Areas ‘Memory Dynamism’ (25115005) and ‘Brain Information Dynamics’ (18H05146) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and a grant from the Uehara Memorial Foundation to Y.Y.

Author information

Author notes

  1. Rumiko Mizuguchi

    Present address: Cell Signaling Technology Japan, Tokyo, Japan

  2. Momoko Shiozaki

    Present address: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA

  3. Hiroki Hamanaka

    Present address: Center for Information and Neural Networks, National Institute of Information and Communications Technology and Osaka University, Osaka, Japan

  4. These authors contributed equally: Kimiya Narikiyo, Rumiko Mizuguchi, Ayako Ajima.

Authors and Affiliations

  1. Laboratory for Neurobiology of Synapse, RIKEN Brain Science Institute, Saitama, Japan

    Kimiya Narikiyo, Rumiko Mizuguchi, Ayako Ajima, Momoko Shiozaki, Kensaku Mori & Yoshihiro Yoshihara

  2. Laboratory for Systems Molecular Ethology, RIKEN Center for Brain Science, Saitama, Japan

    Kimiya Narikiyo, Ayako Ajima, Momoko Shiozaki, Kensaku Mori & Yoshihiro Yoshihara

  3. Laboratory for Neural Circuit for Memory, RIKEN Brain Science Institute, Saitama, Japan

    Hiroki Hamanaka & Joshua P. Johansen

  4. Laboratory for Neural Circuitry of Learning and Memory, RIKEN Center for Brain Science, Saitama, Japan

    Joshua P. Johansen

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Contributions

K.N., R.M., A.A. and Y.Y. conceived the study. Y.Y. developed the Cla-Cre mouse. R.M., M.S., H.H., J.P.J. and Y.Y. performed the anatomical experiments. A.A. performed the in vitro electrophysiological experiments. K.N. performed the in vivo electrophysiological experiments. K.N., R.M., A.A., K.M. and Y.Y. wrote the paper.

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Correspondence to Yoshihiro Yoshihara.

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Peer review information Nature Neuroscience thanks Luis de Lecea, Igor Timofeev, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 A representative example of presynaptic input neurons to Cre-expressing claustral neurons.

Presynaptic input neurons to Cre-expressing claustral neurons were visualized with a modified rabies virus-mediated mono-synaptic retrograde tracing method. AON, anterior olfactory nucleus; Au, auditory cortex; BLA, basolateral amygdala; Cg, cingulate cortex; Cla, claustrum; DEn, dorsal endopiriform nucleus; DR, dorsal raphe nucleus; DTT, dorsal tenia tecta; Ect, ectorhinal cortex; Ent, entorhinal cortex; FrA, frontal association cortex, IC, insular cortex; LH, lateral hypothalamic area; M1, primary motor cortex; M2, secondary motor cortex; MD, mediodorsal thalamic nucleus; MnR, median raphe nucleus; OFC, orbitofrontal cortex; PaS, parasubiculum; Pir, piriform cortex; PrL, prelimbic cortex; PRh, perirhinal cortex; RS, retrosplenial cortex; S1, primary somatosensory cortex; S2, secondary somatosensory cortex; SI, substantia innominate; V1, primary visual cortex; V2, secondary visual cortex. The antero-posterior coordinates are indicated in each section (mm from the bregma). Scale bar, 1 mm. Similar results were obtained in four independent experiments.

Extended Data Fig. 2 A representative example of axonal trajectories of Cre-expressing claustral neurons.

Axonal trajectories of Cre-expressing claustral neurons were visualized with Cre-dependent tdTomato-expressing AAV. AON, anterior olfactory nucleus; Au, auditory cortex; BLA, basolateral amygdala; Cg, cingulate cortex; Cla, claustrum; DEn, dorsal endopiriform nucleus; DR, dorsal raphe nucleus; DTT, dorsal tenia tecta; Ect, ectorhinal cortex; Ent, entorhinal cortex; FrA, frontal association cortex, IC, insular cortex; LH, lateral hypothalamic area; M1, primary motor cortex; M2, secondary motor cortex; MD, mediodorsal thalamic nucelus; MnR, median raphe nucleus; OFC, orbitofrontal cortex; PaS, parasubiculum; Pir, piriform cortex; PrL, prelimbic cortex; PRh, perirhinal cortex; RS, retrosplenial cortex; S1, primary somatosensory cortex; S2, secondary somatosensory cortex; SI, substantia innominata; V1, primary visual cortex; V2, secondary visual cortex. The antero-posterior coordinates are indicated in each section (mm from the bregma). Scale bar, 1 mm. Similar results were obtained in four independent experiments.

Extended Data Fig. 3 A representative example of synaptic vesicle distributions of Cre-expressing claustral neurons.

Synaptic vesicle distributions of Cre-expressing claustral neurons were visualized with Cre-dependent synaptophysin-GFP (sypGFP)-expressing AAV. Coronal sections of the brain were immunolabeled with anti-GFP (white in left panels, green in right panels) and anti-NeuN (red in right panels) antibodies. The antero-posterior coordinates are indicated in each section (mm from the bregma). Similar results were obtained in four independent experiments. Scale bar, 200 μm.

Extended Data Fig. 4 Claustral activation drives PV-positive fast-spiking neurons in the insular cortex.

Three examples (a–c) of the PV-positive neurons in the insular cortex of PV/myrGFP-LDLRct transgenic mice. Upper panels show the morphology of the recorded neurons filled with biocytin (red) and immunostained with anti-GFP antibody (green). Scale bar, 50 μm. Arrows indicate the PV-positive recorded neurons. Lower panels show firing patterns induced by inward current pulse injection for 1 s (200 and 400 pA in a and b, respectively) or 250 ms × 3 (270 pA in c) and responses to optogenetic stimulation of the claustrum. Blue arrows and red asterisks indicate the timing of photostimulation (5 ms) and the evoked action potentials. The horizontal black bar on the left of each voltage trace indicates membrane potential at −60 mV. The photostimulation-evoked action potentials were observed in 48% (10/21) of the GFP-positive neurons recorded from 10 mice.

Extended Data Fig. 5 Claustral stimulation drives fast-spiking interneurons in the frontal cortex.

a, Current-clamp recordings of regular-spiking neurons in the frontal cortex. Firing patterns induced by inward current pulse injection for 1 s (top), and responses to the optogenetic stimulation of the claustral axons (bottom). b, Percentage of regular-spiking neurons (n = 90) that showed EPSP with action potential (red), EPSP without action potential (blue), and no response (white) upon the optogenetic claustral stimulation. c, Recordings from fast-spiking neurons. Firing patterns induced by inward current pulse injection for 1 s (top), and responses to the optogenetic stimulation of the claustral axons (bottom). d, Percentage of fast-spiking neurons (n = 27) that showed an EPSP with action potential (red), EPSP without action potential (blue), and no response (white) upon the optogenetic claustral stimulation. The horizontal black bar on the left of each voltage trace, −60 mV; the vertical black scale bar on the right of each top voltage trace, 10 mV; the blue arrow below each trace, photostimulation (5 ms); red asterisk, action potential.

Extended Data Fig. 6 Spike latencies of claustral and cortical neurons after photostimulation.

Top, Claustral photostimulation-triggered PSTHs (1-ms bins, smoothed by 3 bins moving average) of claustral units (Cla, n = 42, magenta), cortical narrow-spike waveform units (NS, n = 8, blue) and cortical wide-spike waveform units (WS, n = 5, brown). Bottom, the group average of each PSTH. The line graph shows mean ± s.e.m.

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Narikiyo, K., Mizuguchi, R., Ajima, A. et al. The claustrum coordinates cortical slow-wave activity. Nat Neurosci 23, 741–753 (2020). https://doi.org/10.1038/s41593-020-0625-7

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