Abstract
Neocortical inhibitory neurons exhibit remarkably diverse morphology, physiological properties and connectivity. Genetic access to molecularly defined subtypes of inhibitory neurons has aided their functional characterization in recent years. These studies have established that, instead of simply balancing excitatory neuron activity, inhibitory neurons actively shape excitatory circuits in a subtype-specific manner. We review the emerging view that inhibitory neuron subtypes perform context-dependent modulation of excitatory activity, as well as regulate experience-dependent plasticity of excitatory circuits. We then review the roles of neuromodulators in regulating the subtype-specific functions of inhibitory neurons. Finally, we discuss the idea that dysfunctions of inhibitory neuron subtypes may be responsible for various aspects of neurological disorders.
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References
Hangya, B., Pi, H.-J., Kvitsiani, D., Ranade, S.P. & Kepecs, A. From circuit motifs to computations: mapping the behavioral repertoire of cortical interneurons. Curr. Opin. Neurobiol. 26, 117–124 (2014).
Letzkus, J.J., Wolff, S.B.E. & Lüthi, A. Disinhibition, a circuit mechanism for associative learning and memory. Neuron 88, 264–276 (2015).
Tremblay, R., Lee, S. & Rudy, B. GABAergic interneurons in the neocortex: from cellular properties to circuits. Neuron 91, 260–292 (2016).
Karnani, M.M. et al. Cooperative subnetworks of molecularly similar interneurons in mouse neocortex. Neuron 90, 86–100 (2016).
Wall, N.R. et al. Brain-wide maps of synaptic input to cortical interneurons. J. Neurosci. 36, 4000–4009 (2016).
Ji, X.-Y. et al. Thalamocortical innervation pattern in mouse auditory and visual cortex: laminar and cell-type specificity. Cereb. Cortex 26, 2612–2625 (2016).
Pfeffer, C.K., Xue, M., He, M., Huang, Z.J. & Scanziani, M. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068–1076 (2013).
Naka, A. & Adesnik, H. Inhibitory circuits in cortical layer 5. Front. Neural Circuits 10, 35 (2016).
Kepecs, A. & Fishell, G. Interneuron cell types are fit to function. Nature 505, 318–326 (2014).
Caroni, P. Inhibitory microcircuit modules in hippocampal learning. Curr. Opin. Neurobiol. 35, 66–73 (2015).
Froemke, R.C. Plasticity of cortical excitatory-inhibitory balance. Annu. Rev. Neurosci. 38, 195–219 (2015).
Roux, L. & Buzsáki, G. Tasks for inhibitory interneurons in intact brain circuits. Neuropharmacology 88, 10–23 (2015).
Stryker, M.P. A neural circuit that controls cortical state, plasticity, and the gain of sensory responses in mouse. Cold Spring Harb. Symp. Quant. Biol. 79, 1–9 (2014).
Urban-Ciecko, J. & Barth, A.L. Somatostatin-expressing neurons in cortical networks. Nat. Rev. Neurosci. 17, 401–409 (2016).
Niell, C.M. & Stryker, M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472–479 (2010).
Fu, Y. et al. A cortical circuit for gain control by behavioral state. Cell 156, 1139–1152 (2014).
Polack, P.-O., Friedman, J. & Golshani, P. Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat. Neurosci. 16, 1331–1339 (2013).
Pakan, J.M. et al. Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex. Elife 5, e14985 (2016).
Nelson, A. et al. A circuit for motor cortical modulation of auditory cortical activity. J. Neurosci. 33, 14342–14353 (2013).
Schneider, D.M., Nelson, A. & Mooney, R. A synaptic and circuit basis for corollary discharge in the auditory cortex. Nature 513, 189–194 (2014).
Zhou, M. et al. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17, 841–850 (2014).
Pi, H.-J. et al. Cortical interneurons that specialize in disinhibitory control. Nature 503, 521–524 (2013).
Zhang, S. et al. Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing. Science 345, 660–665 (2014).
Goard, M.J., Pho, G.N., Woodson, J. & Sur, M. Distinct roles of visual, parietal, and frontal motor cortices in memory-guided sensorimotor decisions. Elife 5, e13764 (2016).
Kuchibhotla, K.V. et al. Parallel processing by cortical inhibition enables context-dependent behavior. Nat. Neurosci. 20, 62–71 (2017).
Carcea, I., Insanally, M.N. & Froemke, R.C. Dynamics of auditory cortical activity during behavioural engagement and auditory perception. Nat. Commun. 8, 14412 (2017).
Krupa, D.J., Wiest, M.C., Shuler, M.G., Laubach, M. & Nicolelis, M.A.L. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 304, 1989–1992 (2004).
Moore, T. & Armstrong, K.M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003).
Squire, R.F., Noudoost, B., Schafer, R.J. & Moore, T. Prefrontal contributions to visual selective attention. Annu. Rev. Neurosci. 36, 451–466 (2013).
Miller, E.K. & Buschman, T.J. Cortical circuits for the control of attention. Curr. Opin. Neurobiol. 23, 216–222 (2013).
Fiser, A. et al. Experience-dependent spatial expectations in mouse visual cortex. Nat. Neurosci. 19, 1658–1664 (2016).
Karnani, M.M. et al. Opening holes in the blanket of inhibition: localized lateral disinhibition by VIP interneurons. J. Neurosci. 36, 3471–3480 (2016).
Silberberg, G. & Markram, H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735–746 (2007).
Kapfer, C., Glickfeld, L.L., Atallah, B.V. & Scanziani, M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10, 743–753 (2007).
Fino, E. & Yuste, R. Dense inhibitory connectivity in neocortex. Neuron 69, 1188–1203 (2011).
Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z.J. & Scanziani, M. A neural circuit for spatial summation in visual cortex. Nature 490, 226–231 (2012).
Makino, H. & Komiyama, T. Learning enhances the relative impact of top-down processing in the visual cortex. Nat. Neurosci. 18, 1116–1122 (2015).
Hamm, J.P. & Yuste, R. Somatostatin interneurons control a key component of mismatch negativity in mouse visual cortex. Cell Rep. 16, 597–604 (2016).
Wolff, S.B.E. et al. Amygdala interneuron subtypes control fear learning through disinhibition. Nature 509, 453–458 (2014).
Lovett-Barron, M. et al. Dendritic inhibition in the hippocampus supports fear learning. Science 343, 857–863 (2014).
Muñoz, W., Tremblay, R., Levenstein, D. & Rudy, B. Layer-specific modulation of neocortical dendritic inhibition during active wakefulness. Science 355, 954–959 (2017).
Lee, S., Kruglikov, I., Huang, Z.J., Fishell, G. & Rudy, B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat. Neurosci. 16, 1662–1670 (2013).
Garcia-Junco-Clemente, P. et al. An inhibitory pull-push circuit in frontal cortex. Nat. Neurosci. 20, 389–392 (2017).
Espinosa, J.S. & Stryker, M.P. Development and plasticity of the primary visual cortex. Neuron 75, 230–249 (2012).
Lazarus, M.S. & Huang, Z.J. Distinct maturation profiles of perisomatic and dendritic targeting GABAergic interneurons in the mouse primary visual cortex during the critical period of ocular dominance plasticity. J. Neurophysiol. 106, 775–787 (2011).
Kuhlman, S.J. et al. A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501, 543–546 (2013).
Hengen, K.B., Lambo, M.E., Van Hooser, S.D., Katz, D.B. & Turrigiano, G.G. Firing rate homeostasis in visual cortex of freely behaving rodents. Neuron 80, 335–342 (2013).
Maffei, A., Lambo, M.E. & Turrigiano, G.G. Critical period for inhibitory plasticity in rodent binocular V1. J. Neurosci. 30, 3304–3309 (2010).
Kannan, M., Gross, G.G., Arnold, D.B. & Higley, M.J. Visual deprivation during the critical period enhances layer 2/3 GABAergic inhibition in mouse V1. J. Neurosci. 36, 5914–5919 (2016).
Froemke, R.C., Merzenich, M.M. & Schreiner, C.E. A synaptic memory trace for cortical receptive field plasticity. Nature 450, 425–429 (2007).
Keck, T. et al. Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat. Neurosci. 11, 1162–1167 (2008).
Hofer, S.B., Mrsic-Flogel, T.D., Bonhoeffer, T. & Hübener, M. Experience leaves a lasting structural trace in cortical circuits. Nature 457, 313–317 (2009).
Keck, T. et al. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71, 869–882 (2011).
Chen, J.L. et al. Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat. Neurosci. 14, 587–594 (2011).
van Versendaal, D. et al. Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74, 374–383 (2012).
Villa, K.L. et al. Inhibitory synapses are repeatedly assembled and removed at persistent sites in vivo. Neuron 89, 756–769 (2016).
Kaneko, M. & Stryker, M.P. Sensory experience during locomotion promotes recovery of function in adult visual cortex. Elife 3, e02798 (2014).
Fu, Y., Kaneko, M., Tang, Y., Alvarez-Buylla, A. & Stryker, M.P. A cortical disinhibitory circuit for enhancing adult plasticity. Elife 4, e05558 (2015).
Peters, A.J., Chen, S.X. & Komiyama, T. Emergence of reproducible spatiotemporal activity during motor learning. Nature 510, 263–267 (2014).
Chen, S.X., Kim, A.N., Peters, A.J. & Komiyama, T. Subtype-specific plasticity of inhibitory circuits in motor cortex during motor learning. Nat. Neurosci. 18, 1109–1115 (2015).
Xue, M., Atallah, B.V. & Scanziani, M. Equalizing excitation-inhibition ratios across visual cortical neurons. Nature 511, 596–600 (2014).
Donato, F., Rompani, S.B. & Caroni, P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504, 272–276 (2013).
Shibata, K. et al. Overlearning hyperstabilizes a skill by rapidly making neurochemical processing inhibitory-dominant. Nat. Neurosci. 20, 470–475 (2017).
Vallentin, D., Kosche, G., Lipkind, D. & Long, M.A. Inhibition protects acquired song segments during vocal learning in zebra finches. Science 351, 267–271 (2016).
Cichon, J. & Gan, W.-B. Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity. Nature 520, 180–185 (2015).
Yang, G. et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344, 1173–1178 (2014).
Turrigiano, G. Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 34, 89–103 (2011).
D'amour, J.A. & Froemke, R.C. Inhibitory and excitatory spike-timing-dependent plasticity in the auditory cortex. Neuron 86, 514–528 (2015).
Bloodgood, B.L., Sharma, N., Browne, H.A., Trepman, A.Z. & Greenberg, M.E. The activity-dependent transcription factor NPAS4 regulates domain-specific inhibition. Nature 503, 121–125 (2013).
Marder, E., O'Leary, T. & Shruti, S. Neuromodulation of circuits with variable parameters: single neurons and small circuits reveal principles of state-dependent and robust neuromodulation. Annu. Rev. Neurosci. 37, 329–346 (2014).
Bargmann, C.I. & Marder, E. From the connectome to brain function. Nat. Methods 10, 483–490 (2013).
Kruglikov, I. & Rudy, B. Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58, 911–924 (2008).
Marlin, B.J., Mitre, M., D'amour, J.A., Chao, M.V. & Froemke, R.C. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature 520, 499–504 (2015).
Hangya, B., Ranade, S.P., Lorenc, M. & Kepecs, A. Central cholinergic neurons are rapidly recruited by reinforcement feedback. Cell 162, 1155–1168 (2015).
Pinto, L. et al. Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16, 1857–1863 (2013).
Chubykin, A.A., Roach, E.B., Bear, M.F. & Shuler, M.G.H. A cholinergic mechanism for reward timing within primary visual cortex. Neuron 77, 723–735 (2013).
Goard, M. & Dan, Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat. Neurosci. 12, 1444–1449 (2009).
Sara, S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 10, 211–223 (2009).
Bouret, S. & Sara, S.J. Network reset: a simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci. 28, 574–582 (2005).
Aston-Jones, G. & Cohen, J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403–450 (2005).
Dayan, P. & Huys, Q.J.M. Serotonin in affective control. Annu. Rev. Neurosci. 32, 95–126 (2009).
Seamans, J.K. & Yang, C.R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog. Neurobiol. 74, 1–58 (2004).
Huang, G.Z. & Woolley, C.S. Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism. Neuron 74, 801–808 (2012).
Mitre, M. et al. A distributed network for social cognition enriched for oxytocin receptors. J. Neurosci. 36, 2517–2535 (2016).
Bakin, J.S. & Weinberger, N.M. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc. Natl. Acad. Sci. USA 93, 11219–11224 (1996).
Kilgard, M.P. & Merzenich, M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714–1718 (1998).
Froemke, R.C. et al. Long-term modification of cortical synapses improves sensory perception. Nat. Neurosci. 16, 79–88 (2013).
Letzkus, J.J. et al. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331–335 (2011).
Reed, A. et al. Cortical map plasticity improves learning but is not necessary for improved performance. Neuron 70, 121–131 (2011).
Znamenskiy, P. & Zador, A.M. Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination. Nature 497, 482–485 (2013).
Xiong, Q., Znamenskiy, P. & Zador, A.M. Selective corticostriatal plasticity during acquisition of an auditory discrimination task. Nature 521, 348–351 (2015).
Nelson, A. & Mooney, R. The basal forebrain and motor cortex provide convergent yet distinct movement-related inputs to the auditory cortex. Neuron 90, 635–648 (2016).
Xiang, Z., Huguenard, J.R. & Prince, D.A. Cholinergic switching within neocortical inhibitory networks. Science 281, 985–988 (1998).
Kawaguchi, Y. Selective cholinergic modulation of cortical GABAergic cell subtypes. J. Neurophysiol. 78, 1743–1747 (1997).
Dayan, P. Twenty-five lessons from computational neuromodulation. Neuron 76, 240–256 (2012).
Schwarz, L.A. et al. Viral-genetic tracing of the input–output organization of a central noradrenaline circuit. Nature 524, 88–92 (2015).
Kebschull, J.M. et al. High-throughput mapping of single-neuron projections by sequencing of barcoded RNA. Neuron 91, 975–987 (2016).
Woodward, D.J., Moises, H.C., Waterhouse, B.D., Hoffer, B.J. & Freedman, R. Modulatory actions of norepinephrine in the central nervous system. Fed. Proc. 38, 2109–2116 (1979).
Martins, A.R.O. & Froemke, R.C. Coordinated forms of noradrenergic plasticity in the locus coeruleus and primary auditory cortex. Nat. Neurosci. 18, 1483–1492 (2015).
Manunta, Y. & Edeline, J.-M. Noradrenergic induction of selective plasticity in the frequency tuning of auditory cortex neurons. J. Neurophysiol. 92, 1445–1463 (2004).
Paspalas, C.D. & Papadopoulos, G.C. Noradrenergic innervation of peptidergic interneurons in the rat visual cortex. Cereb. Cortex 9, 844–853 (1999).
Sara, S.J. & Segal, M. Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog. Brain Res. 88, 571–585 (1991).
McGinley, M.J., David, S.V. & McCormick, D.A. Cortical membrane potential signature of optimal states for sensory signal detection. Neuron 87, 179–192 (2015).
Tritsch, N.X. & Sabatini, B.L. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 76, 33–50 (2012).
Bao, S., Chan, V.T. & Merzenich, M.M. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412, 79–83 (2001).
Constantinidis, C., Williams, G.V. & Goldman-Rakic, P.S. A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat. Neurosci. 5, 175–180 (2002).
Kvitsiani, D. et al. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498, 363–366 (2013).
Pinto, L. & Dan, Y. Cell-type-specific activity in prefrontal cortex during goal-directed behavior. Neuron 87, 437–450 (2015).
Kim, D. et al. Distinct roles of parvalbumin- and somatostatin-expressing interneurons in working memory. Neuron 92, 902–915 (2016).
Gao, W.-J., Wang, Y. & Goldman-Rakic, P.S. Dopamine modulation of perisomatic and peridendritic inhibition in prefrontal cortex. J. Neurosci. 23, 1622–1630 (2003).
Gao, W.-J. & Goldman-Rakic, P.S. Selective modulation of excitatory and inhibitory microcircuits by dopamine. Proc. Natl. Acad. Sci. USA 100, 2836–2841 (2003).
Gorelova, N., Seamans, J.K. & Yang, C.R. Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J. Neurophysiol. 88, 3150–3166 (2002).
Karunakaran, S. et al. PV plasticity sustained through D1/5 dopamine signaling required for long-term memory consolidation. Nat. Neurosci. 19, 454–464 (2016).
Puig, M.V. & Gulledge, A.T. Serotonin and prefrontal cortex function: neurons, networks, and circuits. Mol. Neurobiol. 44, 449–464 (2011).
Lladó-Pelfort, L., Santana, N., Ghisi, V., Artigas, F. & Celada, P. 5-HT1A receptor agonists enhance pyramidal cell firing in prefrontal cortex through a preferential action on GABA interneurons. Cereb. Cortex 22, 1487–1497 (2012).
Lewis, D.A. Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia. Curr. Opin. Neurobiol. 26, 22–26 (2014).
Schmid, L.C. et al. Dysfunction of somatostatin-positive interneurons associated with memory deficits in an Alzheimer's disease model. Neuron 92, 114–125 (2016).
Verret, L. et al. Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149, 708–721 (2012).
Sasaki, S., Huda, K., Inoue, T., Miyata, M. & Imoto, K. Impaired feedforward inhibition of the thalamocortical projection in epileptic Ca2+ channel mutant mice, tottering. J. Neurosci. 26, 3056–3065 (2006).
Paz, J.T. et al. A new mode of corticothalamic transmission revealed in the Gria4−/− model of absence epilepsy. Nat. Neurosci. 14, 1167–1173 (2011).
Paz, J.T. & Huguenard, J.R. Microcircuits and their interactions in epilepsy: is the focus out of focus? Nat. Neurosci. 18, 351–359 (2015).
Rossignol, E., Kruglikov, I., van den Maagdenberg, A.M.J.M., Rudy, B. & Fishell, G. CaV 2.1 ablation in cortical interneurons selectively impairs fast-spiking basket cells and causes generalized seizures. Ann. Neurol. 74, 209–222 (2013).
Tai, C., Abe, Y., Westenbroek, R.E., Scheuer, T. & Catterall, W.A. Impaired excitability of somatostatin- and parvalbumin-expressing cortical interneurons in a mouse model of Dravet syndrome. Proc. Natl. Acad. Sci. USA 111, E3139–E3148 (2014).
Khoshkhoo, S., Vogt, D. & Sohal, V.S. Dynamic, cell-type-specific roles for GABAergic interneurons in a mouse model of optogenetically inducible seizures. Neuron 93, 291–298 (2017).
Chao, H.-T. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature 468, 263–269 (2010).
Ure, K. et al. Restoration of Mecp2 expression in GABAergic neurons is sufficient to rescue multiple disease features in a mouse model of Rett syndrome. Elife 5, e14198 (2016).
Ito-Ishida, A., Ure, K., Chen, H., Swann, J.W. & Zoghbi, H.Y. Loss of MeCP2 in parvalbumin-and somatostatin-expressing neurons in mice leads to distinct Rett syndrome-like phenotypes. Neuron 88, 651–658 (2015).
Dimidschstein, J. et al. A viral strategy for targeting and manipulating interneurons across vertebrate species. Nat. Neurosci. 19, 1743–1749 (2016).
Buzsáki, G. & Wang, X.-J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203–225 (2012).
Fries, P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32, 209–224 (2009).
Sohal, V.S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698–702 (2009).
Yizhar, O. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171–178 (2011).
Cardin, J.A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667 (2009).
Veit, J., Hakim, R., Jadi, M.P., Sejnowski, T.J. & Adesnik, H. Cortical gamma band synchronization through somatostatin interneurons. Nat. Neurosci. 20, 951–959 (2017).
Uhlhaas, P.J. & Singer, W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11, 100–113 (2010).
Belforte, J.E. et al. Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat. Neurosci. 13, 76–83 (2010).
Carlén, M. et al. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol. Psychiatry 17, 537–548 (2012).
Cho, K.K.A. et al. Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in Dlx5/6+/− mice. Neuron 85, 1332–1343 (2015).
Gillespie, A.K. et al. Apolipoprotein E4 causes age-dependent disruption of slow gamma oscillations during hippocampal sharp-wave ripples. Neuron 90, 740–751 (2016).
Iaccarino, H.F. et al. Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nature 540, 230–235 (2016).
Xie, Y., Chen, S., Wu, Y. & Murphy, T.H. Prolonged deficits in parvalbumin neuron stimulation-evoked network activity despite recovery of dendritic structure and excitability in the somatosensory cortex following global ischemia in mice. J. Neurosci. 34, 14890–14900 (2014).
Martínez-Cerdeño, V. et al. Embryonic MGE precursor cells grafted into adult rat striatum integrate and ameliorate motor symptoms in 6-OHDA-lesioned rats. Cell Stem Cell 6, 238–250 (2010).
Lin, F.G., Galindo-Leon, E.E., Ivanova, T.N., Mappus, R.C. & Liu, R.C. A role for maternal physiological state in preserving auditory cortical plasticity for salient infant calls. Neuroscience 247, 102–116 (2013).
He, M. et al. Strategies and tools for combinatorial targeting of GABAergic neurons in mouse cerebral cortex. Neuron 92, 555 (2016).
Wertz, A. et al. Single-cell-initiated monosynaptic tracing reveals layer-specific cortical network modules. Science 349, 70–74 (2015).
Acknowledgements
This work was supported by grants from the NIH (R01 NS091010A, R01 EY025349, R01 DC014690 and U01 NS094342), Pew Charitable Trusts, David & Lucile Packard Foundation, McKnight Foundation and New York Stem Cell Foundation to T.K., from the NIH (DC009635 and DC012557), Pew Charitable Trusts, McKnight Foundation and HHMI Faculty Scholars Program to R.C.F., and from the NIH (DC05014) to K.V.K.
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Hattori, R., Kuchibhotla, K., Froemke, R. et al. Functions and dysfunctions of neocortical inhibitory neuron subtypes. Nat Neurosci 20, 1199–1208 (2017). https://doi.org/10.1038/nn.4619
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DOI: https://doi.org/10.1038/nn.4619
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