Sleep down state-active ID2/Nkx2.1 interneurons in the neocortex.
Action Potentials
/ physiology
Animals
Inhibitor of Differentiation Protein 2
/ metabolism
Interneurons
/ metabolism
Male
Mice
Mice, Transgenic
Neural Pathways
/ physiology
Nitric Oxide Synthase Type I
/ metabolism
Optogenetics
Parietal Lobe
/ metabolism
Pyramidal Cells
/ physiology
Sleep
/ physiology
Thyroid Nuclear Factor 1
/ metabolism
Journal
Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
14
04
2020
accepted:
08
01
2021
pubmed:
24
2
2021
medline:
30
3
2021
entrez:
23
2
2021
Statut:
ppublish
Résumé
Pyramidal cells and GABAergic interneurons fire together in balanced cortical networks. In contrast to this general rule, we describe a distinct neuron type in mice and rats whose spiking activity is anti-correlated with all principal cells and interneurons in all brain states but, most prevalently, during the down state of non-REM (NREM) sleep. We identify these down state-active (DSA) neurons as deep-layer neocortical neurogliaform cells that express ID2 and Nkx2.1 and are weakly immunoreactive to neuronal nitric oxide synthase. DSA neurons are weakly excited by deep-layer pyramidal cells and strongly inhibited by several other GABAergic cell types. Spiking of DSA neurons modified the sequential firing order of other neurons at down-up transitions. Optogenetic activation of ID2
Identifiants
pubmed: 33619404
doi: 10.1038/s41593-021-00797-6
pii: 10.1038/s41593-021-00797-6
pmc: PMC9662703
mid: NIHMS1756465
doi:
Substances chimiques
Idb2 protein, mouse
0
Inhibitor of Differentiation Protein 2
0
Nkx2-1 protein, mouse
0
Thyroid Nuclear Factor 1
0
Nitric Oxide Synthase Type I
EC 1.14.13.39
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
401-411Subventions
Organisme : NINDS NIH HHS
ID : P01 NS074972
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH054671
Pays : United States
Organisme : Medical Research Council
ID : MC_UU_12024/4
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : R01 NS107257
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH107396
Pays : United States
Organisme : Medical Research Council
ID : MR/R011567/1
Pays : United Kingdom
Organisme : NINDS NIH HHS
ID : U01 NS090583
Pays : United States
Organisme : NINDS NIH HHS
ID : U19 NS104590
Pays : United States
Organisme : NINDS NIH HHS
ID : U19 NS107616
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS110079
Pays : United States
Organisme : NINDS NIH HHS
ID : F31 NS106793
Pays : United States
Références
Buzsaki, G. et al. Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J. Neurosci. 8, 4007–4026 (1988).
pubmed: 3183710
pmcid: 6569493
doi: 10.1523/JNEUROSCI.08-11-04007.1988
Steriade, M., Nunez, A. & Amzica, F. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 13, 3252–3265 (1993).
pubmed: 8340806
pmcid: 6576541
doi: 10.1523/JNEUROSCI.13-08-03252.1993
Sanchez-Vives, M. V. & McCormick, D. A. Cellular and network mechanisms of rhytmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).
pubmed: 11017176
doi: 10.1038/79848
Hasenstaub, A. et al. Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47, 423–435 (2005).
pubmed: 16055065
doi: 10.1016/j.neuron.2005.06.016
Steriade, M. & Timofeev, I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37, 563–576 (2003).
pubmed: 12597855
doi: 10.1016/S0896-6273(03)00065-5
Tononi, G. & Cirelli, C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81, 12–34 (2014).
pubmed: 24411729
pmcid: 3921176
doi: 10.1016/j.neuron.2013.12.025
Takehara-Nishiuchi, K. & McNaughton, B. L. Spontaneous changes of neocortical code for associative memory during consolidation. Science 322, 960–963 (2008).
pubmed: 18988855
doi: 10.1126/science.1161299
Todorova, R. & Zugaro, M. Isolated cortical computations during delta waves support memory consolidation. Science 366, 377–381 (2019).
pubmed: 31624215
doi: 10.1126/science.aay0616
Massimini, M., Huber, R., Ferrarelli, F., Hill, S. & Tononi, G. The sleep slow oscillation as a traveling wave. J. Neurosci. 24, 6862–6870 (2004).
pubmed: 15295020
pmcid: 6729597
doi: 10.1523/JNEUROSCI.1318-04.2004
Luczak, A., Barthó, P., Marguet, S. L., Buzsáki, G. & Harris, K. D. Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl Acad. Sci. USA 104, 347–352 (2007).
pubmed: 17185420
doi: 10.1073/pnas.0605643104
Gerashchenko, D. et al. Identification of a population of sleep-active cerebral cortex neurons. Proc. Natl Acad. Sci. USA 105, 10227–10232 (2008).
pubmed: 18645184
doi: 10.1073/pnas.0803125105
Morairty, S. R. et al. A role for cortical nNOS/NK1 neurons in coupling homeostatic sleep drive to EEG slow wave activity. Proc. Natl Acad. Sci. USA 110, 20272–20277 (2013).
pubmed: 24191004
doi: 10.1073/pnas.1314762110
Zielinski, M. R. et al. Somatostatin
Compte, A., Sanchez-Vives, M. V., McCormick, D. A. & Wang, X. J. Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J. Neurophysiol. 89, 2707–2725 (2003).
pubmed: 12612051
doi: 10.1152/jn.00845.2002
Jercog, D. et al. UP-DOWN cortical dynamics reflect state transitions in a bistable network. eLife 6, e22425 (2017).
pubmed: 28826485
pmcid: 5582872
doi: 10.7554/eLife.22425
Senzai, Y., Fernandez-Ruiz, A. & Buzsáki, G. Layer-specific physiological features and interlaminar interactions in the primary visual cortex of the mouse. Neuron 101, 500–513(2019).
pubmed: 30635232
pmcid: 6367010
doi: 10.1016/j.neuron.2018.12.009
Watson, B. O., Levenstein, D., Greene, J. P., Gelinas, J. N. & Buzsáki, G. Network homeostasis and state dynamics of neocortical sleep. Neuron 90, 839–852 (2016).
pubmed: 27133462
pmcid: 4873379
doi: 10.1016/j.neuron.2016.03.036
Okun, M. et al. Diverse coupling of neurons to populations in sensory cortex. Nature 521, 511–515 (2015).
pubmed: 25849776
pmcid: 4449271
doi: 10.1038/nature14273
English, D. F. et al. Pyramidal cell–interneuron circuit architecture and dynamics in hippocampal networks. Neuron 96, 505–520 (2017).
pubmed: 29024669
pmcid: 5659748
doi: 10.1016/j.neuron.2017.09.033
Tremblay, R., Lee, S. & Rudy, B. GABAergic interneurons in the neocortex: from cellular properties to circuits. Neuron 91, 260–292 (2016).
pubmed: 27477017
pmcid: 4980915
doi: 10.1016/j.neuron.2016.06.033
Tasic, B. et al. Shared and distinct transcriptomic cell types across neocortical areas. Nature 563, 72–78 (2018).
pubmed: 30382198
pmcid: 6456269
doi: 10.1038/s41586-018-0654-5
Hodge, R. D. et al. Conserved cell types with divergent features in human versus mouse cortex. Nature 573, 61–68 (2019).
pubmed: 31435019
pmcid: 6919571
doi: 10.1038/s41586-019-1506-7
Krienen, F. M. et al. Innovations present in the primate interneuron repertoire. Nature 586, 262–269 (2020).
pubmed: 32999462
doi: 10.1038/s41586-020-2781-z
Oláh, S. et al. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461, 1278–1281 (2009).
pubmed: 19865171
pmcid: 2771344
doi: 10.1038/nature08503
Overstreet-Wadiche, L. & McBain, C. J. Neurogliaform cells in cortical circuits. Nat. Rev. Neurosci. 16, 458–468 (2015).
pubmed: 26189693
pmcid: 5207343
doi: 10.1038/nrn3969
Schuman, B. et al. Four unique interneuron populations reside in neocortical layer 1. J. Neurosci. 39, 125–139 (2019).
pubmed: 30413647
pmcid: 6325270
doi: 10.1523/JNEUROSCI.1613-18.2018
Jiang, X. et al. Principles of connectivity among morphologically defined cell types in adult neocortex. Science 350, aac9462 (2015).
Cadwell, C. R. et al. Electrophysiological, transcriptomic and morphologic profiling of single neurons using Patch-seq. Nat. Biotechnol. 34, 199–203 (2016).
pubmed: 26689543
doi: 10.1038/nbt.3445
Szabadics, J., Tamás, G. & Soltesz, I. Different transmitter transients underlie presynaptic cell type specificity of GABAA,slow and GABAA,fast. Proc. Natl Acad. Sci. USA 104, 14831–14836 (2007).
pubmed: 17785408
doi: 10.1073/pnas.0707204104
Goldberg, E. M. et al. K
pubmed: 18466749
pmcid: 2730466
doi: 10.1016/j.neuron.2008.03.003
Karube, F., Kubota, Y. & Kawaguchi, Y. Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J. Neurosci. 24, 2853–2865 (2004).
pubmed: 15044524
pmcid: 6729850
doi: 10.1523/JNEUROSCI.4814-03.2004
Peyrache, A., Battaglia, F. P. & Destexhe, A. Inhibition recruitment in prefrontal cortex during sleep spindles and gating of hippocampal inputs. Proc. Natl Acad. Sci. USA 108, 17207–17212 (2011).
pubmed: 21949372
doi: 10.1073/pnas.1103612108
Levenstein, D., Buzsáki, G. & Rinzel, J. NREM sleep in the rodent neocortex and hippocampus reflects excitable dynamics. Nat. Commun. 10, 1–12 (2019).
doi: 10.1038/s41467-019-10327-5
Harvey, C. D., Coen, P. & Tank, D. W. Choice-specific sequences in parietal cortex during a virtual-navigation decision task. Nature 484, 62–68 (2012).
pubmed: 22419153
pmcid: 3321074
doi: 10.1038/nature10918
Hoffman, K. L. & McNaughton, B. L. Coordinated reactivation of distributed memory traces in primate neocortex. Science 297, 2070–2073 (2002).
pubmed: 12242447
doi: 10.1126/science.1073538
Kubota, Y., Hattori, R. & Yui, Y. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res. 649, 159–173 (1994).
pubmed: 7525007
doi: 10.1016/0006-8993(94)91060-X
Perrenoud, Q., Rossier, J., Geoffroy, H., Vitalis, T. & Gallopin, T. Diversity of GABAergic interneurons in layer VIa and VIb of mouse barrel cortex. Cereb. Cortex 23, 423–441 (2013).
pubmed: 22357664
doi: 10.1093/cercor/bhs032
Tamás, G., Lörincz, A., Simon, A. & Szabadics, J. Identified sources and targets of slow inhibition in the neocortex. Science 299, 1902–1905 (2003).
pubmed: 12649485
doi: 10.1126/science.1082053
Craig, M. T. & McBain, C. J. The emerging role of GABAB receptors as regulators of network dynamics: fast actions from a ‘slow’ receptor? Curr. Opin. Neurobiol. 26, 15–21 (2014).
pubmed: 24650499
doi: 10.1016/j.conb.2013.10.002
Tricoire, L. et al. Common origins of hippocampal ivy and nitric oxide synthase expressing neurogliaform cells. J. Neurosci. 30, 2165–2176 (2010).
pubmed: 20147544
pmcid: 2825142
doi: 10.1523/JNEUROSCI.5123-09.2010
Niquille, M. et al. Neurogliaform cortical interneurons derive from cells in the preoptic area. eLife 7, e32017 (2018).
pubmed: 29557780
pmcid: 5860868
doi: 10.7554/eLife.32017
Taniguchi, H., Lu, J. & Huang, Z. J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339, 70–74 (2013).
pubmed: 23180771
doi: 10.1126/science.1227622
Van Der Werf, Y. D., Witter, M. P. & Groenewegen, H. J. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res. Rev. 39, 107–140 (2002).
pubmed: 12423763
doi: 10.1016/S0165-0173(02)00181-9
Brombas, A., Fletcher, L. N. & Williams, S. R. Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine. J. Neurosci. 34, 1932–1941 (2014).
pubmed: 24478372
pmcid: 6827591
doi: 10.1523/JNEUROSCI.4470-13.2014
Olsen, S. R., Bortone, D. S., Adesnik, H. & Scanziani, M. Gain control by layer six in cortical circuits of vision. Nature 483, 47–54 (2012).
pubmed: 22367547
pmcid: 3636977
doi: 10.1038/nature10835
Stark, E., Koos, T. & Buzsáki, G. Diode probes for spatiotemporal optical control of multiple neurons in freely moving animals. J. Neurophysiol. 108, 349–363 (2012).
pubmed: 22496529
pmcid: 3434617
doi: 10.1152/jn.00153.2012
Pachitariu, M., Steinmetz., N. A., Kadir, S. N., Carandini, M. & Harris, K. D. Fast and accurate spike sorting of high-channel count probes with KiloSort. Adv. Neural Inform. Process. Sys. 29, 4448–4456 (2016).
Valero, M. et al. Mechanisms for selective single-cell reactivation during offline sharp-wave ripples and their distortion by fast ripples. Neuron 94, 1234–1247.e7 (2017).
pubmed: 28641116
doi: 10.1016/j.neuron.2017.05.032
Navas-Olive, A. et al. Multimodal determinants of phase-locked dynamics across deep-superficial hippocampal sublayers during theta oscillations. Nat. Commun. 11, 2217 (2020).
Stark, E. & Abeles, M. Unbiased estimation of precise temporal correlations between spike trains. J. Neurosci. Methods 179, 90–100 (2009).
pubmed: 19167428
doi: 10.1016/j.jneumeth.2008.12.029
Barrio-Alonso, E., Fontana, B., Valero, M. & Frade, J. M. Pathological aspects of neuronal hyperploidization in Alzheimer’s disease evidenced by computer simulation. Front. Genet. 11, 287 (2020).
pubmed: 32292421
pmcid: 7121139
doi: 10.3389/fgene.2020.00287
Stimberg, M., Brette, R. & Goodman, D. F. M. Brian 2, an intuitive and efficient neural simulator. eLife 8, e47314 (2019).
pubmed: 31429824
pmcid: 6786860
doi: 10.7554/eLife.47314
Valero, M. et al. Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples. Nat. Neurosci. 18, 1281–1290 (2015).
pubmed: 26214372
pmcid: 4820637
doi: 10.1038/nn.4074
Viney, T. J. et al. Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo. Nat. Neurosci. 16, 1802–1811 (2013).
pubmed: 24141313
pmcid: 4471148
doi: 10.1038/nn.3550
Salib, M. et al. GABAergic medial septal neurons with low-rhythmic firing innervating the dentate gyrus and hippocampal area CA3. J. Neurosci. 39, 4527–4549 (2019).
pubmed: 30926750
pmcid: 6554630
doi: 10.1523/JNEUROSCI.3024-18.2019
Hovde, K., Gianatti, M., Witter, M. P. & Whitlock, J. R. Architecture and organization of mouse posterior parietal cortex relative to extrastriate areas. Eur. J. Neurosci. 49, 1313–1329 (2019).
pubmed: 30456892
Feng, L., Zhao, T. & Kim, J. Neutube 1.0: a new design for efficient neuron reconstruction software based on the SWC format. eNeuro 2, ENEURO.0049-14.2014 (2015).