Spontaneous Synaptic Activation of Muscarinic Receptors by Striatal Cholinergic Neuron Firing

Adler, 2013, Different correlation patterns of cholinergic and GABAergic interneurons with striatal projection neurons, Front. Syst. Neurosci., 7, 47, 10.3389/fnsys.2013.00047 Aosaki, 1994, Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys, Science, 265, 412, 10.1126/science.8023166 Atallah, 2014, Neurons in the ventral striatum exhibit cell-type-specific representations of outcome during learning, Neuron, 82, 1145, 10.1016/j.neuron.2014.04.021 Bennett, 1999, Spontaneous activity of neostriatal cholinergic interneurons in vitro, J. Neurosci., 19, 5586, 10.1523/JNEUROSCI.19-13-05586.1999 Bennett, 2000, Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons, J. Neurosci., 20, 8493, 10.1523/JNEUROSCI.20-22-08493.2000 Bernard, 1992, Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes, J. Neurosci., 12, 3591, 10.1523/JNEUROSCI.12-09-03591.1992 Bolam, 1984, Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry, Golgi-impregnation and electron microscopy, Neuroscience, 12, 711, 10.1016/0306-4522(84)90165-9 Buhl, 1994, Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites, Nature, 368, 823, 10.1038/368823a0 Cachope, 2012, Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing, Cell Rep., 2, 33, 10.1016/j.celrep.2012.05.011 Calabresi, 1998, Muscarinic IPSPs in rat striatal cholinergic interneurones, J. Physiol., 510, 421, 10.1111/j.1469-7793.1998.421bk.x Chuhma, 2014, Dopamine neurons control striatal cholinergic neurons via regionally heterogeneous dopamine and glutamate signaling, Neuron, 81, 901, 10.1016/j.neuron.2013.12.027 Clements, 2000, Unveiling synaptic plasticity: a new graphical and analytical approach, Trends Neurosci., 23, 105, 10.1016/S0166-2236(99)01520-9 Contant, 1996, Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum, Neuroscience, 71, 937, 10.1016/0306-4522(95)00507-2 Courtney, 2014, The timing of dopamine- and noradrenaline-mediated transmission reflects underlying differences in the extent of spillover and pooling, J. Neurosci., 34, 7645, 10.1523/JNEUROSCI.0166-14.2014 Descarries, 2000, Ultrastructural evidence for diffuse transmission by monoamine and acetylcholine neurons of the central nervous system, Prog. Brain Res., 125, 27, 10.1016/S0079-6123(00)25005-X Ding, 2006, RGS4-dependent attenuation of M4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion, Nat. Neurosci., 9, 832, 10.1038/nn1700 English, 2011, GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons, Nat. Neurosci., 15, 123, 10.1038/nn.2984 Ford, 2009, The time course of dopamine transmission in the ventral tegmental area, J. Neurosci., 29, 13344, 10.1523/JNEUROSCI.3546-09.2009 Gerfen, 2011, Modulation of striatal projection systems by dopamine, Annu. Rev. Neurosci., 34, 441, 10.1146/annurev-neuro-061010-113641 Goldberg, 2011, Spontaneous firing and evoked pauses in the tonically active cholinergic interneurons of the striatum, Neuroscience, 198, 27, 10.1016/j.neuroscience.2011.08.067 Goldberg, 2012, Muscarinic modulation of striatal function and circuitry, Handbook Exp. Pharmacol., 208, 223, 10.1007/978-3-642-23274-9_10 Hebb, 1961, Gradient of choline acetylase activity, Nature, 189, 123, 10.1038/189123a0 Hersch, 1994, Distribution of m1-m4 muscarinic receptor proteins in the rat striatum: light and electron microscopic immunocytochemistry using subtype-specific antibodies, J. Neurosci., 14, 3351, 10.1523/JNEUROSCI.14-05-03351.1994 Higley, 2009, Cholinergic modulation of multivesicular release regulates striatal synaptic potency and integration, Nat. Neurosci., 12, 1121, 10.1038/nn.2368 Higley, 2011, Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum, PLoS ONE, 6, e19155, 10.1371/journal.pone.0019155 Howe, 1995, Muscarinic receptors modulate N-, P-, and L-type Ca2+ currents in rat striatal neurons through parallel pathways, J. Neurosci., 15, 458, 10.1523/JNEUROSCI.15-01-00458.1995 Jeon, 2010, A subpopulation of neuronal M4 muscarinic acetylcholine receptors plays a critical role in modulating dopamine-dependent behaviors, J. Neurosci., 30, 2396, 10.1523/JNEUROSCI.3843-09.2010 Kawaguchi, 1993, Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum, J. Neurosci., 13, 4908, 10.1523/JNEUROSCI.13-11-04908.1993 Koós, 2002, Dual cholinergic control of fast-spiking interneurons in the neostriatum, J. Neurosci., 22, 529, 10.1523/JNEUROSCI.22-02-00529.2002 Koos, 2004, Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum, J. Neurosci., 24, 7916, 10.1523/JNEUROSCI.2163-04.2004 Kraushaar, 2000, Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse, J. Neurosci., 20, 5594, 10.1523/JNEUROSCI.20-15-05594.2000 Kreitzer, 2009, Physiology and pharmacology of striatal neurons, Annu. Rev. Neurosci., 32, 127, 10.1146/annurev.neuro.051508.135422 Lim, 2014, Striatal cholinergic interneuron regulation and circuit effects, Front. Synaptic Neurosci., 6, 22, 10.3389/fnsyn.2014.00022 Lüscher, 2010, Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease, Nat. Rev. Neurosci., 11, 301, 10.1038/nrn2834 Macintosh, 1941, The distribution of acetylcholine in the peripheral and the central nervous system, J. Physiol., 99, 436, 10.1113/jphysiol.1941.sp003913 Marcott, 2014, Phasic dopamine release drives rapid activation of striatal D2-receptors, Neuron, 84, 164, 10.1016/j.neuron.2014.08.058 Marty, 2011, Short-term plasticity impacts information transfer at glutamate synapses onto parvocellular neuroendocrine cells in the paraventricular nucleus of the hypothalamus, J. Physiol., 589, 4259, 10.1113/jphysiol.2011.208082 Morris, 2004, Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons, Neuron, 43, 133, 10.1016/j.neuron.2004.06.012 Nelson, 2014, Striatal cholinergic neurotransmission requires VGLUT3, J. Neurosci., 34, 8772, 10.1523/JNEUROSCI.0901-14.2014 Nelson, 2014, Striatal cholinergic interneurons Drive GABA release from dopamine terminals, Neuron, 82, 63, 10.1016/j.neuron.2014.01.023 Pakhotin, 2007, Cholinergic interneurons control the excitatory input to the striatum, J. Neurosci., 27, 391, 10.1523/JNEUROSCI.3709-06.2007 Perez-Rosello, 2005, Cholinergic control of firing pattern and neurotransmission in rat neostriatal projection neurons: role of CaV2.1 and CaV2.2 Ca2+ channels, J. Neurophysiol., 93, 2507, 10.1152/jn.00853.2004 Pisani, 2002, Metabotropic glutamate 2 receptors modulate synaptic inputs and calcium signals in striatal cholinergic interneurons, J. Neurosci., 22, 6176, 10.1523/JNEUROSCI.22-14-06176.2002 Salin, 2009, Changes to interneuron-driven striatal microcircuits in a rat model of Parkinson’s disease, Neurobiol. Dis., 34, 545, 10.1016/j.nbd.2009.03.006 Scheuss, 2001, Estimating synaptic parameters from mean, variance, and covariance in trains of synaptic responses, Biophys. J., 81, 1970, 10.1016/S0006-3495(01)75848-1 Schulz, 2013, Pause and rebound: sensory control of cholinergic signaling in the striatum, Trends Neurosci., 36, 41, 10.1016/j.tins.2012.09.006 Shen, 2007, Cholinergic modulation of Kir2 channels selectively elevates dendritic excitability in striatopallidal neurons, Nat. Neurosci., 10, 1458, 10.1038/nn1972 Shen, 2015, M4 Muscarinic Receptor Signaling Ameliorates Striatal Plasticity Deficits in Models of L-DOPA-Induced Dyskinesia, Neuron, 88, 762, 10.1016/j.neuron.2015.10.039 Shimo, 2001, Role of tonically active neurons in primate caudate in reward-oriented saccadic eye movement, J. Neurosci., 21, 7804, 10.1523/JNEUROSCI.21-19-07804.2001 Silver, 1998, Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses, J. Physiol., 510, 881, 10.1111/j.1469-7793.1998.881bj.x Sodickson, 1996, GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons, J. Neurosci., 16, 6374, 10.1523/JNEUROSCI.16-20-06374.1996 Sodickson, 1998, Neurotransmitter activation of inwardly rectifying potassium current in dissociated hippocampal CA3 neurons: interactions among multiple receptors, J. Neurosci., 18, 8153, 10.1523/JNEUROSCI.18-20-08153.1998 Straub, 2014, Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents, J. Neurosci., 34, 8557, 10.1523/JNEUROSCI.0589-14.2014 Sullivan, 2008, Recurrent inhibitory network among striatal cholinergic interneurons, J. Neurosci., 28, 8682, 10.1523/JNEUROSCI.2411-08.2008 Swapna, 2016, Differential Dopamine Regulation of Ca(2+) Signaling and Its Timing Dependence in the Nucleus Accumbens, Cell Rep., 15, 563, 10.1016/j.celrep.2016.03.055 Taverna, 2008, Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson’s disease, J. Neurosci., 28, 5504, 10.1523/JNEUROSCI.5493-07.2008 Tecuapetla, 2007, Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses, Proc. Natl. Acad. Sci. USA, 104, 10258, 10.1073/pnas.0703813104 Threlfell, 2012, Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons, Neuron, 75, 58, 10.1016/j.neuron.2012.04.038 Tritsch, 2012, Dopaminergic neurons inhibit striatal output through non-canonical release of GABA, Nature, 490, 262, 10.1038/nature11466 Wall, 2013, Differential innervation of direct- and indirect-pathway striatal projection neurons, Neuron, 79, 347, 10.1016/j.neuron.2013.05.014 Wilson, 2005, The mechanism of intrinsic amplification of hyperpolarizations and spontaneous bursting in striatal cholinergic interneurons, Neuron, 45, 575, 10.1016/j.neuron.2004.12.053 Wilson, 1990, Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum, J. Neurosci., 10, 508, 10.1523/JNEUROSCI.10-02-00508.1990 Yagishita, 2014, A critical time window for dopamine actions on the structural plasticity of dendritic spines, Science, 345, 1616, 10.1126/science.1255514 Yamamoto, 2013, Reciprocal regulation of inhibitory synaptic transmission by nicotinic and muscarinic receptors in rat nucleus accumbens shell, J. Physiol., 591, 5745, 10.1113/jphysiol.2013.258558 Yan, 2001, Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons, Neuroscience, 103, 1017, 10.1016/S0306-4522(01)00039-2