Activity-dependent tuning of intrinsic excitability in mouse and human neurogliaform cells
Ramesh Chittajallu, Kurt Auville, Vivek Mahadevan, Mandy Lai, Steven Hunt, Daniela Calvigioni, Kenneth A Pelkey, Kareem A Zaghloul, Chris J McBain, Ramesh Chittajallu, Kurt Auville, Vivek Mahadevan, Mandy Lai, Steven Hunt, Daniela Calvigioni, Kenneth A Pelkey, Kareem A Zaghloul, Chris J McBain
Abstract
The ability to modulate the efficacy of synaptic communication between neurons constitutes an essential property critical for normal brain function. Animal models have proved invaluable in revealing a wealth of diverse cellular mechanisms underlying varied plasticity modes. However, to what extent these processes are mirrored in humans is largely uncharted thus questioning their relevance in human circuit function. In this study, we focus on neurogliaform cells, that possess specialized physiological features enabling them to impart a widespread inhibitory influence on neural activity. We demonstrate that this prominent neuronal subtype, embedded in both mouse and human neural circuits, undergo remarkably similar activity-dependent modulation manifesting as epochs of enhanced intrinsic excitability. In principle, these evolutionary conserved plasticity routes likely tune the extent of neurogliaform cell mediated inhibition thus constituting canonical circuit mechanisms underlying human cognitive processing and behavior.
Trial registration: ClinicalTrials.gov NCT01273129.
Keywords: human; interneuron; intrinsic excitablity; mouse; neurogliaform cell; neuroscience; plasticity.
Conflict of interest statement
RC, KA, VM, ML, SH, DC, KP, KZ, CM No competing interests declared
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References
- Abs E, Poorthuis RB, Apelblat D, Muhammad K, Pardi MB, Enke L, Kushinsky D, Pu D-L, Eizinger MF, Conzelmann K-K, Spiegel I, Letzkus JJ. Learning-Related plasticity in Dendrite-Targeting layer 1 interneurons. Neuron. 2018;100:684–699. doi: 10.1016/j.neuron.2018.09.001.
- Alfaro-Ruíz R, Aguado C, Martín-Belmonte A, Moreno-Martínez AE, Luján R. Expression, cellular and subcellular localisation of Kv4.2 and Kv4.3 Channels in the Rodent Hippocampus. International Journal of Molecular Sciences. 2019;20:246. doi: 10.3390/ijms20020246.
- Armstrong C, Szabadics J, Tamás G, Soltesz I. Neurogliaform cells in the molecular layer of the dentate gyrus as feed-forward γ-aminobutyric acidergic modulators of entorhinal-hippocampal interplay. The Journal of Comparative Neurology. 2011;519:1476–1491. doi: 10.1002/cne.22577.
- Beaulieu-Laroche L, Toloza EHS, van der Goes MS, Lafourcade M, Barnagian D, Williams ZM, Eskandar EN, Frosch MP, Cash SS, Harnett MT. Enhanced dendritic compartmentalization in human cortical neurons. Cell. 2018;175:643–651. doi: 10.1016/j.cell.2018.08.045.
- Bekkers JM, Delaney AJ. Modulation of excitability by alpha-dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons. The Journal of Neuroscience. 2001;21:6553–6560. doi: 10.1523/JNEUROSCI.21-17-06553.2001.
- Bezaire MJ, Soltesz I. Quantitative assessment of CA1 local circuits: knowledge base for interneuron-pyramidal cell connectivity. Hippocampus. 2013;23:751–785. doi: 10.1002/hipo.22141.
- Bliss TVP, Collingridge GL. Persistent memories of long-term potentiation and the N -methyl-d-aspartate receptor. Brain and Neuroscience Advances. 2019;3:239821281984821. doi: 10.1177/2398212819848213.
- Boldog E, Bakken TE, Hodge RD, Novotny M, Aevermann BD, Baka J, Bordé S, Close JL, Diez-Fuertes F, Ding SL, Faragó N, Kocsis ÁK, Kovács B, Maltzer Z, McCorrison JM, Miller JA, Molnár G, Oláh G, Ozsvár A, Rózsa M, Shehata SI, Smith KA, Sunkin SM, Tran DN, Venepally P, Wall A, Puskás LG, Barzó P, Steemers FJ, Schork NJ, Scheuermann RH, Lasken RS, Lein ES, Tamás G. Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type. Nature Neuroscience. 2018;21:1185–1195. doi: 10.1038/s41593-018-0205-2.
- Bourdeau ML, Morin F, Laurent CE, Azzi M, Lacaille JC. Kv4.3-mediated A-type K+ currents underlie rhythmic activity in hippocampal interneurons. Journal of Neuroscience. 2007;27:1942–1953. doi: 10.1523/JNEUROSCI.3208-06.2007.
- Bourdeau ML, Laplante I, Laurent CE, Lacaille JC. KChIP1 modulation of Kv4.3-mediated A-type K(+) currents and repetitive firing in hippocampal interneurons. Neuroscience. 2011;176:173–187. doi: 10.1016/j.neuroscience.2010.11.051.
- Butler A, Hoffman P, Smibert P, Papalexi E, Satija R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nature Biotechnology. 2018;36:411–420. doi: 10.1038/nbt.4096.
- Butt SJ, Stacey JA, Teramoto Y, Vagnoni C. A role for GABAergic interneuron diversity in circuit development and plasticity of the neonatal cerebral cortex. Current Opinion in Neurobiology. 2017;43:149–155. doi: 10.1016/j.conb.2017.03.011.
- Campanac E, Gasselin C, Baude A, Rama S, Ankri N, Debanne D. Enhanced intrinsic excitability in basket cells maintains excitatory-inhibitory balance in hippocampal circuits. Neuron. 2013;77:712–722. doi: 10.1016/j.neuron.2012.12.020.
- Capogna M. Neurogliaform cells and other interneurons of stratum lacunosum-moleculare gate entorhinal-hippocampal dialogue. The Journal of Physiology. 2011;589:1875–1883. doi: 10.1113/jphysiol.2010.201004.
- Carrasquillo Y, Burkhalter A, Nerbonne JM. A-type K+ channels encoded by Kv4.2, Kv4.3 and Kv1.4 differentially regulate intrinsic excitability of cortical pyramidal neurons. The Journal of Physiology. 2012;590:3877–3890. doi: 10.1113/jphysiol.2012.229013.
- Cembrowski MS, Bachman JL, Wang L, Sugino K, Shields BC, Spruston N. Spatial Gene-Expression gradients underlie prominent heterogeneity of CA1 pyramidal neurons. Neuron. 2016a;89:351–368. doi: 10.1016/j.neuron.2015.12.013.
- Cembrowski MS, Wang L, Sugino K, Shields BC, Spruston N. Hipposeq: a comprehensive RNA-seq database of gene expression in hippocampal principal neurons. eLife. 2016b;5:e14997. doi: 10.7554/eLife.14997.
- Chittajallu R, Pelkey KA, McBain CJ. Neurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation. Nature Neuroscience. 2013;16:13–15. doi: 10.1038/nn.3284.
- Chittajallu R, Wester JC, Craig MT, Barksdale E, Yuan XQ, Akgül G, Fang C, Collins D, Hunt S, Pelkey KA, McBain CJ. Afferent specific role of NMDA receptors for the circuit integration of hippocampal neurogliaform cells. Nature Communications. 2017;8:152. doi: 10.1038/s41467-017-00218-y.
- Chittajallu R. Mouse-CGE-NGFCs. 204db8eGitHub. 2020
- Chu Z, Galarreta M, Hestrin S. Synaptic interactions of late-spiking neocortical neurons in layer 1. The Journal of Neuroscience. 2003;23:96–102. doi: 10.1523/JNEUROSCI.23-01-00096.2003.
- Cummings KA, Clem RL. Prefrontal somatostatin interneurons encode fear memory. Nature Neuroscience. 2020;23:61–74. doi: 10.1038/s41593-019-0552-7.
- Debanne D, Inglebert Y, Russier M. Plasticity of intrinsic neuronal excitability. Current Opinion in Neurobiology. 2019;54:73–82. doi: 10.1016/j.conb.2018.09.001.
- Deemyad T, Lüthi J, Spruston N. Astrocytes integrate and drive action potential firing in inhibitory subnetworks. Nature Communications. 2018;9:4336. doi: 10.1038/s41467-018-06338-3.
- Dehorter N, Ciceri G, Bartolini G, Lim L, del Pino I, Marín O. Tuning of fast-spiking interneuron properties by an activity-dependent transcriptional switch. Science. 2015;349:1216–1220. doi: 10.1126/science.aab3415.
- Dimidschstein J, Chen Q, Tremblay R, Rogers SL, Saldi G-A, Guo L, Xu Q, Liu R, Lu C, Chu J, Grimley JS, Krostag A-R, Kaykas A, Avery MC, Rashid MS, Baek M, Jacob AL, Smith GB, Wilson DE, Kosche G, Kruglikov I, Rusielewicz T, Kotak VC, Mowery TM, Anderson SA, Callaway EM, Dasen JS, Fitzpatrick D, Fossati V, Long MA, Noggle S, Reynolds JH, Sanes DH, Rudy B, Feng G, Fishell G. A viral strategy for targeting and manipulating interneurons across vertebrate species. Nature Neuroscience. 2016;19:1743–1749. doi: 10.1038/nn.4430.
- Elgueta C, Köhler J, Bartos M. Persistent discharges in Dentate Gyrus perisoma-inhibiting interneurons require hyperpolarization-activated cyclic nucleotide-gated channel activation. Journal of Neuroscience. 2015;35:4131–4139. doi: 10.1523/JNEUROSCI.3671-14.2015.
- Eyal G, Verhoog MB, Testa-Silva G, Deitcher Y, Lodder JC, Benavides-Piccione R, Morales J, DeFelipe J, de Kock CPJ, Mansvelder HD, Segev I. Unique membrane properties and enhanced signal processing in human neocortical neurons. eLife. 2016;5:e16553. doi: 10.7554/eLife.16553.
- Gainey MA, Aman JW, Feldman DE. Rapid disinhibition by adjustment of PV intrinsic excitability during whisker map plasticity in mouse S1. The Journal of Neuroscience. 2018;38:4749–4761. doi: 10.1523/JNEUROSCI.3628-17.2018.
- Goldberg JH, Tamas G, Yuste R. Ca2+ imaging of mouse neocortical interneurone dendrites: ia-type K+ channels control action potential backpropagation. The Journal of Physiology. 2003;551:49–65. doi: 10.1113/jphysiol.2003.042580.
- Hebb DO. The Organization of Behavior: A Neurophysiological Theory. John Wiley and Sons; 1949.
- Hodge RD, Bakken TE, Miller JA, Smith KA, Barkan ER, Graybuck LT, Close JL, Long B, Johansen N, Penn O, Yao Z, Eggermont J, Höllt T, Levi BP, Shehata SI, Aevermann B, Beller A, Bertagnolli D, Brouner K, Casper T, Cobbs C, Dalley R, Dee N, Ding SL, Ellenbogen RG, Fong O, Garren E, Goldy J, Gwinn RP, Hirschstein D, Keene CD, Keshk M, Ko AL, Lathia K, Mahfouz A, Maltzer Z, McGraw M, Nguyen TN, Nyhus J, Ojemann JG, Oldre A, Parry S, Reynolds S, Rimorin C, Shapovalova NV, Somasundaram S, Szafer A, Thomsen ER, Tieu M, Quon G, Scheuermann RH, Yuste R, Sunkin SM, Lelieveldt B, Feng D, Ng L, Bernard A, Hawrylycz M, Phillips JW, Tasic B, Zeng H, Jones AR, Koch C, Lein ES. Conserved cell types with divergent features in human versus mouse cortex. Nature. 2019;573:61–68. doi: 10.1038/s41586-019-1506-7.
- Imbrosci B, Neitz A, Mittmann T. Physiological properties of supragranular cortical inhibitory interneurons expressing retrograde persistent firing. Neural Plasticity. 2015;2015:1–12. doi: 10.1155/2015/608141.
- Jerng HH, Pfaffinger PJ. Modulatory mechanisms and multiple functions of somatodendritic A-type K+ channel auxiliary subunits. Frontiers in Cellular Neuroscience. 2014;8:82. doi: 10.3389/fncel.2014.00082.
- Jung SC, Hoffman DA. Biphasic somatic A-type K channel downregulation mediates intrinsic plasticity in hippocampal CA1 pyramidal neurons. PLOS ONE. 2009;4:e6549. doi: 10.1371/journal.pone.0006549.
- Keck T, Toyoizumi T, Chen L, Doiron B, Feldman DE, Fox K, Gerstner W, Haydon PG, Hübener M, Lee H-K, Lisman JE, Rose T, Sengpiel F, Stellwagen D, Stryker MP, Turrigiano GG, van Rossum MC. Integrating hebbian and homeostatic plasticity: the current state of the field and future research directions. Philosophical Transactions of the Royal Society B: Biological Sciences. 2017;372:20160158. doi: 10.1098/rstb.2016.0158.
- Kepecs A, Fishell G. Interneuron cell types are fit to function. Nature. 2014;505:318–326. doi: 10.1038/nature12983.
- Kim J, Hoffman DA. Potassium channels: newly found players in synaptic plasticity. The Neuroscientist. 2008;14:276–286. doi: 10.1177/1073858408315041.
- Krienen FM, Goldman M, Zhang Q, del Rosario R, Florio M, Machold R, McCarroll SA. Innovations in primate interneuron repertoire. bioRxiv. 2019 doi: 10.1101/709501.
- Krook-Magnuson E, Luu L, Lee SH, Varga C, Soltesz I. Ivy and neurogliaform interneurons are a major target of μ-opioid receptor modulation. Journal of Neuroscience. 2011;31:14861–14870. doi: 10.1523/JNEUROSCI.2269-11.2011.
- Kullmann DM, Moreau AW, Bakiri Y, Nicholson E. Plasticity of inhibition. Neuron. 2012;75:951–962. doi: 10.1016/j.neuron.2012.07.030.
- Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B. The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. Journal of Neuroscience. 2010;30:16796–16808. doi: 10.1523/JNEUROSCI.1869-10.2010.
- Li K, Lu Y-M, Xu Z-H, Zhang J, Zhu J-M, Zhang J-M, Cao S-X, Chen X-J, Chen Z, Luo J-H, Duan S, Li X-M. Neuregulin 1 regulates excitability of fast-spiking neurons through Kv1.1 and acts in epilepsy. Nature Neuroscience. 2012;15:267–273. doi: 10.1038/nn.3006.
- Li G, Stewart R, Canepari M, Capogna M. Firing of hippocampal neurogliaform cells induces suppression of synaptic inhibition. Journal of Neuroscience. 2014;34:1280–1292. doi: 10.1523/JNEUROSCI.3046-13.2014.
- Lien CC, Martina M, Schultz JH, Ehmke H, Jonas P. Gating, modulation and subunit composition of voltage-gated K(+) channels in dendritic inhibitory interneurones of rat Hippocampus. The Journal of Physiology. 2002;538:405–419. doi: 10.1113/jphysiol.2001.013066.
- Lovett-Barron M, Kaifosh P, Kheirbek MA, Danielson N, Zaremba JD, Reardon TR, Turi GF, Hen R, Zemelman BV, Losonczy A. Dendritic inhibition in the Hippocampus supports fear learning. Science. 2014;343:857–863. doi: 10.1126/science.1247485.
- Maffie JK, Dvoretskova E, Bougis PE, Martin-Eauclaire MF, Rudy B. Dipeptidyl-peptidase-like-proteins confer high sensitivity to the scorpion toxin AmmTX3 to Kv4-mediated A-type K+ channels. The Journal of Physiology. 2013;591:2419–2427. doi: 10.1113/jphysiol.2012.248831.
- Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron. 2004;44:5–21. doi: 10.1016/j.neuron.2004.09.012.
- Mansvelder HD, Verhoog MB, Goriounova NA. Synaptic plasticity in human cortical circuits: cellular mechanisms of learning and memory in the human brain? Current Opinion in Neurobiology. 2019;54:186–193. doi: 10.1016/j.conb.2018.06.013.
- Marín O. Interneuron dysfunction in psychiatric disorders. Nature Reviews Neuroscience. 2012;13:107–120. doi: 10.1038/nrn3155.
- Mayer C, Hafemeister C, Bandler RC, Machold R, Batista Brito R, Jaglin X, Allaway K, Butler A, Fishell G, Satija R. Developmental diversification of cortical inhibitory interneurons. Nature. 2018;555:457–462. doi: 10.1038/nature25999.
- Mehta P, Kreeger L, Wylie DC, Pattadkal JJ, Lusignan T, Davis MJ, Turi GF, Li W-K, Whitmire MP, Chen Y, Kajs BL, Seidemann E, Priebe NJ, Losonczy A, Zemelman BV. Functional access to neuron subclasses in rodent and primate forebrain. Cell Reports. 2019;26:2818–2832. doi: 10.1016/j.celrep.2019.02.011.
- Menegola M, Misonou H, Vacher H, Trimmer JS. Dendritic A-type potassium channel subunit expression in CA1 hippocampal interneurons. Neuroscience. 2008;154:953–964. doi: 10.1016/j.neuroscience.2008.04.022.
- Mercier MS, Magloire V, Cornford JH, Kullmann DM. Long-term synaptic plasticity in hippocampal neurogliaform interneurons. bioRxiv. 2019 doi: 10.1101/531822.
- Mich JK, Graybuck LT, Hess EE, Mahoney JT, Kojima Y, Ding Y, Levi BP. Functional enhancer elements drive subclass-selective expression from mouse to primate neocortex. bioRxiv. 2020 doi: 10.1101/555318.
- Molnár G, Rózsa M, Baka J, Holderith N, Barzó P, Nusser Z, Tamás G. Human pyramidal to interneuron synapses are mediated by multi-vesicular release and multiple docked vesicles. eLife. 2016;5:e18167. doi: 10.7554/eLife.18167.
- Obermayer J, Heistek TS, Kerkhofs A, Goriounova NA, Kroon T, Baayen JC, Idema S, Testa-Silva G, Couey JJ, Mansvelder HD. Lateral inhibition by martinotti interneurons is facilitated by cholinergic inputs in human and mouse neocortex. Nature Communications. 2018;9:4101. doi: 10.1038/s41467-018-06628-w.
- Oláh S, Komlósi G, Szabadics J, Varga C, Tóth E, Barzó P, Tamás G. Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex. Frontiers in Neural Circuits. 2007;1:4. doi: 10.3389/neuro.04.004.2007.
- Oláh VJ, Lukacsovich D, Winterer J, Arszovszki A, Lőrincz A, Nusser Z, Földy C, Szabadics J. Functional specification of CCK+ interneurons by alternative isoforms of Kv4.3 auxiliary subunits. eLife. 2020;9:e58515. doi: 10.7554/eLife.58515.
- Overstreet-Wadiche L, McBain CJ. Neurogliaform cells in cortical circuits. Nature Reviews Neuroscience. 2015;16:458–468. doi: 10.1038/nrn3969.
- Pelkey KA, Chittajallu R, Craig MT, Tricoire L, Wester JC, McBain CJ. Hippocampal GABAergic inhibitory interneurons. Physiological Reviews. 2017;97:1619–1747. doi: 10.1152/physrev.00007.2017.
- Poorthuis RB, Muhammad K, Wang M, Verhoog MB, Junek S, Wrana A, Mansvelder HD, Letzkus JJ. Rapid neuromodulation of layer 1 interneurons in human neocortex. Cell Reports. 2018;23:951–958. doi: 10.1016/j.celrep.2018.03.111.
- Povysheva NV, Zaitsev AV, Kröner S, Krimer OA, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS. Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. Journal of Neurophysiology. 2007;97:1030–1039. doi: 10.1152/jn.00794.2006.
- Povysheva NV, Zaitsev AV, Rotaru DC, Gonzalez-Burgos G, Lewis DA, Krimer LS. Parvalbumin-positive basket interneurons in monkey and rat prefrontal cortex. Journal of Neurophysiology. 2008;100:2348–2360. doi: 10.1152/jn.90396.2008.
- Pozo K, Goda Y. Unraveling mechanisms of homeostatic synaptic plasticity. Neuron. 2010;66:337–351. doi: 10.1016/j.neuron.2010.04.028.
- Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M. Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. Journal of Neuroscience. 2005;25:6775–6786. doi: 10.1523/JNEUROSCI.1135-05.2005.
- Rhodes KJ, Carroll KI, Sung MA, Doliveira LC, Monaghan MM, Burke SL, Strassle BW, Buchwalder L, Menegola M, Cao J, An WF, Trimmer JS. KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. Journal of Neuroscience. 2004;24:7903–7915. doi: 10.1523/JNEUROSCI.0776-04.2004.
- Rózsa M, Toth M, Olah G, Baka J, Barzo P, Tamas G. Rhythmic Persistent Firing of Neurogliaform Interneurons in the Human and Rodent Neocortex. Program No. 202.07. 2017 Neuroscience Meeting Planner. Washington DC: Society for Neuroscience; 2017.
- Rudy B. Diversity and ubiquity of K channels. Neuroscience. 1988;25:729–749. doi: 10.1016/0306-4522(88)90033-4.
- Rudy B, McBain CJ. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends in Neurosciences. 2001;24:517–526. doi: 10.1016/S0166-2236(00)01892-0.
- Serôdio P, Rudy B. Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K+ (A-type) currents in rat brain. Journal of Neurophysiology. 1998;79:1081–1091. doi: 10.1152/jn.1998.79.2.1081.
- Sheffield MEJ, Best TK, Mensh BD, Kath WL, Spruston N. Slow integration leads to persistent action potential firing in distal axons of coupled interneurons. Nature Neuroscience. 2011;14:200–207. doi: 10.1038/nn.2728.
- Sheffield ME, Edgerton GB, Heuermann RJ, Deemyad T, Mensh BD, Spruston N. Mechanisms of retroaxonal barrage firing in hippocampal interneurons. The Journal of Physiology. 2013;591:4793–4805. doi: 10.1113/jphysiol.2013.258418.
- Simon A, Oláh S, Molnár G, Szabadics J, Tamás G. Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. Journal of Neuroscience. 2005;25:6278–6285. doi: 10.1523/JNEUROSCI.1431-05.2005.
- Storm JF. Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature. 1988;336:379–381. doi: 10.1038/336379a0.
- Stuart T, Butler A, Hoffman P, Hafemeister C, Papalexi E, Mauck WM, Hao Y, Stoeckius M, Smibert P, Satija R. Comprehensive integration of Single-Cell data. Cell. 2019;177:1888–1902. doi: 10.1016/j.cell.2019.05.031.
- Sun QQ. Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. Journal of Neurophysiology. 2009;102:2955–2973. doi: 10.1152/jn.00562.2009.
- Suzuki N, Tang CS, Bekkers JM. Persistent barrage firing in cortical interneurons can be induced in vivo and may be important for the suppression of epileptiform activity. Frontiers in Cellular Neuroscience. 2014;8:76. doi: 10.3389/fncel.2014.00076.
- Szabadics J, Varga C, Molnár G, Oláh S, Barzó P, Tamás G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science. 2006;311:233–235. doi: 10.1126/science.1121325.
- Szegedi V, Paizs M, Csakvari E, Molnar G, Barzo P, Tamas G, Lamsa K. Plasticity in single axon glutamatergic connection to GABAergic interneurons regulates complex events in the human neocortex. PLOS Biology. 2016;14:e2000237. doi: 10.1371/journal.pbio.2000237.
- Szegedi V, Paizs M, Baka J, Barzó P, Molnár G, Tamas G, Lamsa K. Robust perisomatic GABAergic self-innervation inhibits basket cells in the human and mouse supragranular neocortex. eLife. 2020;9:e51691. doi: 10.7554/eLife.51691.
- Takesian AE, Hensch TK. Balancing plasticity/stability across brain development. Progress in Brain Research. 2013;207:3–34. doi: 10.1016/B978-0-444-63327-9.00001-1.
- Tasic B, Menon V, Nguyen TN, Kim TK, Jarsky T, Yao Z, Levi B, Gray LT, Sorensen SA, Dolbeare T, Bertagnolli D, Goldy J, Shapovalova N, Parry S, Lee C, Smith K, Bernard A, Madisen L, Sunkin SM, Hawrylycz M, Koch C, Zeng H. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nature Neuroscience. 2016;19:335–346. doi: 10.1038/nn.4216.
- Tasic B, Yao Z, Graybuck LT, Smith KA, Nguyen TN, Bertagnolli D, Goldy J, Garren E, Economo MN, Viswanathan S, Penn O, Bakken T, Menon V, Miller J, Fong O, Hirokawa KE, Lathia K, Rimorin C, Tieu M, Larsen R, Casper T, Barkan E, Kroll M, Parry S, Shapovalova NV, Hirschstein D, Pendergraft J, Sullivan HA, Kim TK, Szafer A, Dee N, Groblewski P, Wickersham I, Cetin A, Harris JA, Levi BP, Sunkin SM, Madisen L, Daigle TL, Looger L, Bernard A, Phillips J, Lein E, Hawrylycz M, Svoboda K, Jones AR, Koch C, Zeng H. Shared and distinct transcriptomic cell types across neocortical Areas. Nature. 2018;563:72–78. doi: 10.1038/s41586-018-0654-5.
- Tien NW, Kerschensteiner D. Homeostatic plasticity in neural development. Neural Development. 2018;13:9. doi: 10.1186/s13064-018-0105-x.
- Tricoire L, Pelkey KA, Erkkila BE, Jeffries BW, Yuan X, McBain CJ. A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. Journal of Neuroscience. 2011;31:10948–10970. doi: 10.1523/JNEUROSCI.0323-11.2011.
- Trimmer JS. Subcellular localization of K+ channels in mammalian brain neurons: remarkable precision in the midst of extraordinary complexity. Neuron. 2015;85:238–256. doi: 10.1016/j.neuron.2014.12.042.
- Varga C, Tamas G, Barzo P, Olah S, Somogyi P. Molecular and electrophysiological characterization of GABAergic interneurons expressing the transcription factor COUP-TFII in the adult human temporal cortex. Cerebral Cortex. 2015;25:4430–4449. doi: 10.1093/cercor/bhv045.
- Vormstein-Schneider D, Lin J, Pelkey K, Chittajallu R, Guo B, Garcia MA, Sakopoulos S, Stevenson O, Schneider G, Zhang Q, Sharma J, Franken TP, Smith J, Vogel I, Sanchez V, Ibrahim LA, Burbridge T, Favuzzi E, Saldi GA, Xu Q, Guo L, Yuan X, Zaghloul KA, Sabri E, Goldberg EM, Devinsky O, Batista-Brito R, Reynolds J, Feng G, Fu Z, McBain CJ, Fishell GJ, Dimidschstein J. Viral manipulation of functionally distinct neurons from mice to humans. bioRxiv. 2020 doi: 10.1101/808170.
- Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H. Anatomical, physiological and molecular properties of martinotti cells in the somatosensory cortex of the juvenile rat. The Journal of Physiology. 2004;561:65–90. doi: 10.1113/jphysiol.2004.073353.
- Wang B, Yin L, Zou X, Ye M, Liu Y, He T, Deng S, Jiang Y, Zheng R, Wang Y, Yang M, Lu H, Wu S, Shu Y. A subtype of inhibitory interneuron with intrinsic persistent activity in human and monkey neocortex. Cell Reports. 2015;10:1450–1458. doi: 10.1016/j.celrep.2015.02.018.
- Williams SB, Hablitz JJ. Differential modulation of repetitive firing and synchronous network activity in neocortical interneurons by inhibition of A-type K(+) channels and ih. Frontiers in Cellular Neuroscience. 2015;9:89. doi: 10.3389/fncel.2015.00089.
- Yoshida M, Hasselmo ME. Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. Journal of Neuroscience. 2009;29:4945–4952. doi: 10.1523/JNEUROSCI.5154-08.2009.
- Zaitsev AV, Povysheva NV, Gonzalez-Burgos G, Rotaru D, Fish KN, Krimer LS, Lewis DA. Interneuron diversity in layers 2-3 of monkey prefrontal cortex. Cerebral Cortex. 2009;19:1597–1615. doi: 10.1093/cercor/bhn198.
Source: PubMed