Rapid Neuromodulation of Layer 1 Interneurons in Human Neocortex

Cell Reports

Volumn 23, Issue 4, 2018, Pages 951-958

  Poorthuis, Rogier B ^a   Muhammad, Karzan ^a   Wang, Mantian ^a   Verhoog, Matthijs B ^b   Junek, Stephan ^a   Wrana, Anne ^a   Mansvelder, Huibert D ^b   Letzkus, Johannes J ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

cell types; evolution; genetic markers; human neocortex; interneuron types; layer 1 interneurons; mouse neocortex; neocortical circuits; neuromodulation; translation; whole cell recordings

Indexed keywords

IONOTROPIC RECEPTOR; SEROTONIN RECEPTOR; SEROTONIN 3 RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATIVE LEARNING; CLINICAL ARTICLE; CONNECTOME; FEMALE; GENETIC ANALYSIS; HTR3 GENE; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; INTERNEURON; LOCOMOTION; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PRIORITY JOURNAL; TRANSGENIC MOUSE; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; MIDDLE AGED; NEOCORTEX; SYNAPTIC TRANSMISSION;

ADULT; ANIMALS; FEMALE; HUMANS; INTERNEURONS; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; NEOCORTEX; RECEPTORS, SEROTONIN, 5-HT3; SYNAPTIC TRANSMISSION;

EID: 85045919145     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2018.03.111     Document Type: Article

References (51)

1. Alitto, H.J., Dan, Y., Cell-type-specific modulation of neocortical activity by basal forebrain input. Front. Syst. Neurosci., 6, 2013, 79.
2. Alkondon, M., Pereira, E.F., Eisenberg, H.M., Albuquerque, E.X., Nicotinic receptor activation in human cerebral cortical interneurons: A mechanism for inhibition and disinhibition of neuronal networks. J. Neurosci. 20 (2000), 66–75.
3. Arroyo, S., Bennett, C., Aziz, D., Brown, S.P., Hestrin, S., Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons. J. Neurosci. 32 (2012), 3859–3864.
4. Arroyo, S., Bennett, C., Hestrin, S., Nicotinic modulation of cortical circuits. Front. Neural Circuits, 8, 2014, 30.
5. Bennett, C., Arroyo, S., Berns, D., Hestrin, S., Mechanisms generating dual-component nicotinic EPSCs in cortical interneurons. J. Neurosci. 32 (2012), 17287–17296.
6. Cauller, L., Layer I of primary sensory neocortex: Where top-down converges upon bottom-up. Behav. Brain Res. 71 (1995), 163–170.
7. Chameau, P., van Hooft, J.A., Serotonin 5-HT(3) receptors in the central nervous system. Cell Tissue Res. 326 (2006), 573–581.
8. Christophe, E., Roebuck, A., Staiger, J.F., Lavery, D.J., Charpak, S., Audinat, E., Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. J. Neurophysiol. 88 (2002), 1318–1327.
9. Chu, Z., Galarreta, M., Hestrin, S., Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23 (2003), 96–102.
10. Cordero-Erausquin, M., Marubio, L.M., Klink, R., Changeux, J.P., Nicotinic receptor function: New perspectives from knockout mice. Trends Pharmacol. Sci. 21 (2000), 211–217.
11. Cruikshank, S.J., Ahmed, O.J., Stevens, T.R., Patrick, S.L., Gonzalez, A.N., Elmaleh, M., Connors, B.W., Thalamic control of layer 1 circuits in prefrontal cortex. J. Neurosci. 32 (2012), 17813–17823.
12. DeFelipe, J., Alonso-Nanclares, L., Arellano, J.I., Microstructure of the neocortex: Comparative aspects. J. Neurocytol. 31 (2002), 299–316.
13. Douglas, R.J., Martin, K.A., Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27 (2004), 419–451.
14. Eyal, G., Verhoog, M.B., Testa-Silva, G., Deitcher, Y., Lodder, J.C., Benavides-Piccione, R., Morales, J., DeFelipe, J., de Kock, C.P., Mansvelder, H.D., Segev, I., Unique membrane properties and enhanced signal processing in human neocortical neurons. eLife 5 (2016), 1–18.
15. Férézou, I., Cauli, B., Hill, E.L., Rossier, J., Hamel, E., Lambolez, B., 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J. Neurosci. 22 (2002), 7389–7397.
16. Fu, Y., Tucciarone, J.M., Espinosa, J.S., Sheng, N., Darcy, D.P., Nicoll, R.A., Huang, Z.J., Stryker, M.P., A cortical circuit for gain control by behavioral state. Cell 156 (2014), 1139–1152.
17. Gong, S., Zheng, C., Doughty, M.L., Losos, K., Didkovsky, N., Schambra, U.B., Nowak, N.J., Joyner, A., Leblanc, G., Hatten, M.E., Heintz, N., A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425 (2003), 917–925.
18. Ibrahim, L.A., Mesik, L., Ji, X.Y., Fang, Q., Li, H.F., Li, Y.T., Zingg, B., Zhang, L.I., Tao, H.W., Cross-Modality Sharpening of Visual Cortical Processing through Layer-1-Mediated Inhibition and Disinhibition. Neuron 89 (2016), 1031–1045.
19. Jiang, M., Zhu, J., Liu, Y., Yang, M., Tian, C., Jiang, S., Wang, Y., Guo, H., Wang, K., Shu, Y., Enhancement of asynchronous release from fast-spiking interneuron in human and rat epileptic neocortex. PLoS Biol., 10, 2012, e1001324.
20. Jiang, X., Wang, G., Lee, A.J., Stornetta, R.L., Zhu, J.J., The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16 (2013), 210–218.
21. Jiang, X., Shen, S., Cadwell, C.R., Berens, P., Sinz, F., Ecker, A.S., Patel, S., Tolias, A.S., Principles of connectivity among morphologically defined cell types in adult neocortex. Science, 350, 2015, aac9462.
22. Kepecs, A., Fishell, G., Interneuron cell types are fit to function. Nature 505 (2014), 318–326.
23. Kuchibhotla, K.V., Gill, J.V., Lindsay, G.W., Papadoyannis, E.S., Field, R.E., Sten, T.A., Miller, K.D., Froemke, R.C., Parallel processing by cortical inhibition enables context-dependent behavior. Nat. Neurosci. 20 (2017), 62–71.
24. Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G., Rudy, B., The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J. Neurosci. 30 (2010), 16796–16808.
25. Letzkus, J.J., Wolff, S.B., Meyer, E.M., Tovote, P., Courtin, J., Herry, C., Lüthi, A., A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480 (2011), 331–335.
26. Letzkus, J.J., Wolff, S.B., Lüthi, A., Disinhibition, a circuit mechanism for associative learning and memory. Neuron 88 (2015), 264–276.
27. Levin, E.D., Complex relationships of nicotinic receptor actions and cognitive functions. Biochem. Pharmacol. 86 (2013), 1145–1152.
28. Marín, O., Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13 (2012), 107–120.
29. Nelson, S.B., Valakh, V., Excitatory/inhibitory balance and circuit homeostasis in autism spectrum disorders. Neuron 87 (2015), 684–698.
30. 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. Front. Neural Circuits, 1, 2007, 4.
31. Palmer, L.M., Schulz, J.M., Murphy, S.C., Ledergerber, D., Murayama, M., Larkum, M.E., The cellular basis of GABA(B)-mediated interhemispheric inhibition. Science 335 (2012), 989–993.
32. Pi, H.J., Hangya, B., Kvitsiani, D., Sanders, J.I., Huang, Z.J., Kepecs, A., Cortical interneurons that specialize in disinhibitory control. Nature 503 (2013), 521–524.
33. Poorthuis, R.B., Enke, L., Letzkus, J.J., Cholinergic circuit modulation through differential recruitment of neocortical interneuron types during behaviour. J. Physiol. 592 (2014), 4155–4164.
34. Povysheva, N.V., Zaitsev, A.V., Kröner, S., Krimer, O.A., Rotaru, D.C., Gonzalez-Burgos, G., Lewis, D.A., Krimer, L.S., Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J. Neurophysiol. 97 (2007), 1030–1039.
35. Prönneke, A., Scheuer, B., Wagener, R.J., Möck, M., Witte, M., Staiger, J.F., Characterizing VIP neurons in the barrel cortex of VIPcre/tdTomato mice reveals layer-specific differences. Cereb. Cortex 25 (2015), 4854–4868.
36. Rakic, P., Evolution of the neocortex: A perspective from developmental biology. Nat. Rev. Neurosci. 10 (2009), 724–735.
37. Sihver, W., Gillberg, P.G., Nordberg, A., Laminar distribution of nicotinic receptor subtypes in human cerebral cortex as determined by [3H](-)nicotine, [3H]cytisine and [3H]epibatidine in vitro autoradiography. Neuroscience 85 (1998), 1121–1133.
38. Silberberg, G., Polysynaptic subcircuits in the neocortex: Spatial and temporal diversity. Curr. Opin. Neurobiol. 18 (2008), 332–337.
39. Smiley, J.F., Morrell, F., Mesulam, M.M., Cholinergic synapses in human cerebral cortex: An ultrastructural study in serial sections. Exp. Neurol. 144 (1997), 361–368.
40. 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 Biol., 2016, 10.1371/journal.pbio.2000237 Published online November 9, 2016.
41. Tasic, B., Menon, V., Nguyen, T.N., Kim, T.K., Jarsky, T., Yao, Z., Levi, B., Gray, L.T., Sorensen, S.A., Dolbeare, T., et al. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19 (2016), 335–346.
42. Testa-Silva, G., Verhoog, M.B., Linaro, D., de Kock, C.P., Baayen, J.C., Meredith, R.M., De Zeeuw, C.I., Giugliano, M., Mansvelder, H.D., High bandwidth synaptic communication and frequency tracking in human neocortex. PLoS Biol., 2014, 10.1371/journal.pbio.1002007 Published online November 25, 2014.
43. Trottier, S., Evrard, B., Vignal, J.P., Scarabin, J.M., Chauvel, P., The serotonergic innervation of the cerebral cortex in man and its changes in focal cortical dysplasia. Epilepsy Res. 25 (1996), 79–106.
44. Verhoog, M.B., Goriounova, N.A., Obermayer, J., Stroeder, J., Hjorth, J.J., Testa-Silva, G., Baayen, J.C., de Kock, C.P., Meredith, R.M., Mansvelder, H.D., Mechanisms underlying the rules for associative plasticity at adult human neocortical synapses. J. Neurosci. 33 (2013), 17197–17208.
45. Verhoog, M.B., Obermayer, J., Kortleven, C.A., Wilbers, R., Wester, J., Baayen, J.C., De Kock, C.P., Meredith, R.M., Mansvelder, H.D., Layer-specific cholinergic control of human and mouse cortical synaptic plasticity. Nat. Commun., 7, 2016, 12826.
46. Ward, J.M., Cockcroft, V.B., Lunt, G.G., Smillie, F.S., Wonnacott, S., Methyllycaconitine: A selective probe for neuronal alpha-bungarotoxin binding sites. FEBS Lett. 270 (1990), 45–48.
47. Wester, J.C., McBain, C.J., Behavioral state-dependent modulation of distinct interneuron subtypes and consequences for circuit function. Curr. Opin. Neurobiol. 29 (2014), 118–125.
48. Wozny, C., Williams, S.R., Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb. Cortex 21 (2011), 1818–1826.
49. Xu, X., Roby, K.D., Callaway, E.M., Immunochemical characterization of inhibitory mouse cortical neurons: Three chemically distinct classes of inhibitory cells. J. Comp. Neurol. 518 (2010), 389–404.
50. Zhou, F.M., Hablitz, J.J., Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. J. Neurophysiol. 82 (1999), 2989–2999.
51. Zhu, Y., Zhu, J.J., Rapid arrival and integration of ascending sensory information in layer 1 nonpyramidal neurons and tuft dendrites of layer 5 pyramidal neurons of the neocortex. J. Neurosci. 24 (2004), 1272–1279.