Cholinergic Interneurons Amplify Thalamostriatal Excitation of Striatal Indirect Pathway Neurons in Parkinson’s Disease Models

Abercrombie, 1997, Substantia nigra D1 receptors and stimulation of striatal cholinergic interneurons by dopamine: a proposed circuit mechanism, J. Neurosci., 17, 8498, 10.1523/JNEUROSCI.17-21-08498.1997 Albin, 1989, The functional anatomy of basal ganglia disorders, Trends Neurosci., 12, 366, 10.1016/0166-2236(89)90074-X Aoki, 2015, Role of Striatal Cholinergic Interneurons in Set-Shifting in the Rat, J. Neurosci., 35, 9424, 10.1523/JNEUROSCI.0490-15.2015 Assous, 2017, Differential processing of thalamic information via distinct striatal interneuron circuits, Nat. Commun., 8, 15860, 10.1038/ncomms15860 Beatty, 2009, Two distinct populations of projection neurons in the rat lateral parafascicular thalamic nucleus and their cholinergic responsiveness, Neuroscience, 162, 155, 10.1016/j.neuroscience.2009.04.043 Bernard, 1992, Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes, J. Neurosci., 12, 3591, 10.1523/JNEUROSCI.12-09-03591.1992 Bohr, 2005, Cholinergic nicotinic receptor involvement in movement disorders associated with Lewy body diseases. An autoradiography study using [(125)I]alpha-conotoxinMII in the striatum and thalamus, Exp. Neurol., 191, 292, 10.1016/j.expneurol.2004.10.004 Bradfield, 2013, The thalamostriatal pathway and cholinergic control of goal-directed action: interlacing new with existing learning in the striatum, Neuron, 79, 153, 10.1016/j.neuron.2013.04.039 Brown, 2010, The parafascicular thalamic nucleus concomitantly influences behavioral flexibility and dorsomedial striatal acetylcholine output in rats, J. Neurosci., 30, 14390, 10.1523/JNEUROSCI.2167-10.2010 Calabresi, 2014, Direct and indirect pathways of basal ganglia: a critical reappraisal, Nat. Neurosci., 17, 1022, 10.1038/nn.3743 Campos, 2013, Rodent models of Parkinson’s disease: beyond the motor symptomatology, Front. Behav. Neurosci., 7, 175, 10.3389/fnbeh.2013.00175 Carvalho, 2013, Behavioral characterization of the 6-hydroxidopamine model of Parkinson’s disease and pharmacological rescuing of non-motor deficits, Mol. Neurodegener., 8, 14, 10.1186/1750-1326-8-14 Chen, 2014, Short latency cerebellar modulation of the basal ganglia, Nat. Neurosci., 17, 1767, 10.1038/nn.3868 Cheng, 2014, Presynaptic α7 nicotinic acetylcholine receptors enhance hippocampal mossy fiber glutamatergic transmission via PKA activation, J. Neurosci., 34, 124, 10.1523/JNEUROSCI.2973-13.2014 Chung, 2016, Postsynaptic nicotinic acetylcholine receptors facilitate excitation of developing CA1 pyramidal neurons, J. Neurophysiol., 116, 2043, 10.1152/jn.00370.2016 Consolo, 1996, The cerebral cortex and parafascicular thalamic nucleus facilitate in vivo acetylcholine release in the rat striatum through distinct glutamate receptor subtypes, Eur. J. Neurosci., 8, 2702, 10.1111/j.1460-9568.1996.tb01565.x Dani, 2001, Overview of nicotinic receptors and their roles in the central nervous system, Biol. Psychiatry, 49, 166, 10.1016/S0006-3223(00)01011-8 Day, 2006, Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models, Nat. Neurosci., 9, 251, 10.1038/nn1632 Deng, 2007, Involvement of I(h) in dopamine modulation of tonic firing in striatal cholinergic interneurons, J. Neurosci., 27, 3148, 10.1523/JNEUROSCI.5535-06.2007 Ding, 2006, RGS4-dependent attenuation of M4 autoreceptor function in striatal cholinergic interneurons following dopamine depletion, Nat. Neurosci., 9, 832, 10.1038/nn1700 Ding, 2010, Thalamic gating of corticostriatal signaling by cholinergic interneurons, Neuron, 67, 294, 10.1016/j.neuron.2010.06.017 Doeppner, 2014, Effects of neural progenitor cells on post-stroke neurological impairment-a detailed and comprehensive analysis of behavioral tests, Front. Cell. Neurosci., 8, 338, 10.3389/fncel.2014.00338 Doig, 2014, Cortical and thalamic excitation mediate the multiphasic responses of striatal cholinergic interneurons to motivationally salient stimuli, J. Neurosci., 34, 3101, 10.1523/JNEUROSCI.4627-13.2014 Ellender, 2013, Heterogeneous properties of central lateral and parafascicular thalamic synapses in the striatum, J. Physiol., 591, 257, 10.1113/jphysiol.2012.245233 Ferguson, 2011, Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization, Nat. Neurosci., 14, 22, 10.1038/nn.2703 Fieblinger, 2014, Cell type-specific plasticity of striatal projection neurons in parkinsonism and L-DOPA-induced dyskinesia, Nat. Commun., 5, 5316, 10.1038/ncomms6316 Fioravante, 2011, Short-term forms of presynaptic plasticity, Curr. Opin. Neurobiol., 21, 269, 10.1016/j.conb.2011.02.003 Fogarty, 2013, A method for the three-dimensional reconstruction of Neurobiotin™-filled neurons and the location of their synaptic inputs, Front. Neural Circuits, 7, 153, 10.3389/fncir.2013.00153 Francardo, 2011, Impact of the lesion procedure on the profiles of motor impairment and molecular responsiveness to L-DOPA in the 6-hydroxydopamine mouse model of Parkinson’s disease, Neurobiol. Dis., 42, 327, 10.1016/j.nbd.2011.01.024 Gerfen, 2011, Modulation of striatal projection systems by dopamine, Annu. Rev. Neurosci., 34, 441, 10.1146/annurev-neuro-061010-113641 Gerfen, 2013, GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits, Neuron, 80, 1368, 10.1016/j.neuron.2013.10.016 Gomez, 2017, Chemogenetics revealed: DREADD occupancy and activation via converted clozapine, Science, 357, 503, 10.1126/science.aan2475 Gong, 2003, A gene expression atlas of the central nervous system based on bacterial artificial chromosomes, Nature, 425, 917, 10.1038/nature02033 Graybiel, 2015, The striatum: where skills and habits meet, Cold Spring Harb. Perspect. Biol., 7, a021691, 10.1101/cshperspect.a021691 Groenewegen, 1994, The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei, Trends Neurosci., 17, 52, 10.1016/0166-2236(94)90074-4 Guo, 2015, Whole-brain mapping of inputs to projection neurons and cholinergic interneurons in the dorsal striatum, PLoS ONE, 10, e0123381, 10.1371/journal.pone.0123381 Heintz, 2001, BAC to the future: the use of bac transgenic mice for neuroscience research, Nat. Rev. Neurosci., 2, 861, 10.1038/35104049 Higley, 2011, Cholinergic interneurons mediate fast VGluT3-dependent glutamatergic transmission in the striatum, PLoS ONE, 6, e19155, 10.1371/journal.pone.0019155 Hill, 1993, Immunocytochemical localization of a neuronal nicotinic receptor: the beta 2-subunit, J. Neurosci., 13, 1551, 10.1523/JNEUROSCI.13-04-01551.1993 Ichinohe, 2000, A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat, Brain Res., 880, 191, 10.1016/S0006-8993(00)02744-X Ikarashi, 1997, Suppression of cholinergic activity via the dopamine D2 receptor in the rat striatum, Neurochem. Int., 30, 191, 10.1016/S0197-0186(96)00024-1 Jones, 2001, Presynaptic localisation of the nicotinic acetylcholine receptor beta2 subunit immunoreactivity in rat nigrostriatal dopaminergic neurones, J. Comp. Neurol., 439, 235, 10.1002/cne.1345 Jouve, 2010, Deep brain stimulation of the center median-parafascicular complex of the thalamus has efficient anti-parkinsonian action associated with widespread cellular responses in the basal ganglia network in a rat model of Parkinson’s disease, J. Neurosci., 30, 9919, 10.1523/JNEUROSCI.1404-10.2010 Kato, 2011, Selective neural pathway targeting reveals key roles of thalamostriatal projection in the control of visual discrimination, J. Neurosci., 31, 17169, 10.1523/JNEUROSCI.4005-11.2011 Kauer, 1988, A persistent postsynaptic modification mediates long-term potentiation in the hippocampus, Neuron, 1, 911, 10.1016/0896-6273(88)90148-1 Kerkerian-Le Goff, 2009, Rationale for targeting the thalamic centre-median parafascicular complex in the surgical treatment of Parkinson’s disease, Parkinsonism Relat. Disord., 15, S167, 10.1016/S1353-8020(09)70807-7 Klapoetke, 2014, Independent optical excitation of distinct neural populations, Nat. Methods, 11, 338, 10.1038/nmeth.2836 Kobayashi, 2003, Synaptic organization of the rat parafascicular nucleus, with special reference to its afferents from the superior colliculus and the pedunculopontine tegmental nucleus, Brain Res., 980, 80, 10.1016/S0006-8993(03)02921-4 Kravitz, 2010, Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry, Nature, 466, 622, 10.1038/nature09159 Kreitzer, 2011, Investigating striatal function through cell-type-specific manipulations, Neuroscience, 198, 19, 10.1016/j.neuroscience.2011.08.018 Kreitzer, 2007, Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models, Nature, 445, 643, 10.1038/nature05506 Kress, 2013, Convergent cortical innervation of striatal projection neurons, Nat. Neurosci., 16, 665, 10.1038/nn.3397 Kusnoor, 2009, Is the loss of thalamostriatal neurons protective in parkinsonism?, Parkinsonism Relat. Disord., 15, S162, 10.1016/S1353-8020(09)70806-5 Lacey, 2007, Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections, J. Neurosci., 27, 4374, 10.1523/JNEUROSCI.5519-06.2007 Lapper, 1992, Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat, Neuroscience, 51, 533, 10.1016/0306-4522(92)90293-B Lim, 2014, Striatal cholinergic interneuron regulation and circuit effects, Front. Synaptic Neurosci., 6, 22, 10.3389/fnsyn.2014.00022 MacDermott, 1999, Presynaptic ionotropic receptors and the control of transmitter release, Annu. Rev. Neurosci., 22, 443, 10.1146/annurev.neuro.22.1.443 Mallet, 2006, Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats, J. Neurosci., 26, 3875, 10.1523/JNEUROSCI.4439-05.2006 Matsumoto, 2001, Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events, J. Neurophysiol., 85, 960, 10.1152/jn.2001.85.2.960 Maurice, 2004, D2 dopamine receptor-mediated modulation of voltage-dependent Na+ channels reduces autonomous activity in striatal cholinergic interneurons, J. Neurosci., 24, 10289, 10.1523/JNEUROSCI.2155-04.2004 Maurice, 2015, Striatal Cholinergic Interneurons Control Motor Behavior and Basal Ganglia Function in Experimental Parkinsonism, Cell Rep., 13, 657, 10.1016/j.celrep.2015.09.034 McGehee, 1995, Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors, Science, 269, 1692, 10.1126/science.7569895 Meyer, 2006, Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms, J. Neurosci., 26, 3604, 10.1523/JNEUROSCI.0223-06.2006 Muller, 1988, Long-term potentiation differentially affects two components of synaptic responses in hippocampus, Proc. Natl. Acad. Sci. USA, 85, 9346, 10.1073/pnas.85.23.9346 Nelson, 2014, Striatal cholinergic neurotransmission requires VGLUT3, J. Neurosci., 34, 8772, 10.1523/JNEUROSCI.0901-14.2014 Parker, 2004, Up-regulation of brain nicotinic acetylcholine receptors in the rat during long-term self-administration of nicotine: disproportionate increase of the alpha6 subunit, Mol. Pharmacol., 65, 611, 10.1124/mol.65.3.611 Parker, 2016, Pathway-Specific Remodeling of Thalamostriatal Synapses in Parkinsonian Mice, Neuron, 89, 734, 10.1016/j.neuron.2015.12.038 Parr-Brownlie, 2009, Parafascicular thalamic nucleus activity in a rat model of Parkinson’s disease, Exp. Neurol., 217, 269, 10.1016/j.expneurol.2009.02.010 Petreanu, 2009, The subcellular organization of neocortical excitatory connections, Nature, 457, 1142, 10.1038/nature07709 Pisani, 2007, Re-emergence of striatal cholinergic interneurons in movement disorders, Trends Neurosci., 30, 545, 10.1016/j.tins.2007.07.008 Quick, 2002, Desensitization of neuronal nicotinic receptors, J. Neurobiol., 53, 457, 10.1002/neu.10109 Redgrave, 2010, Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease, Nat. Rev. Neurosci., 11, 760, 10.1038/nrn2915 Ruiz-DeDiego, 2015, Dopaminergic regulation of olfactory type G-protein α subunit expression in the striatum, Mov. Disord., 30, 1039, 10.1002/mds.26197 Sadikot, 1992, Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity, J. Comp. Neurol., 320, 228, 10.1002/cne.903200207 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 Sanz, 2009, Cell-type-specific isolation of ribosome-associated mRNA from complex tissues, Proc. Natl. Acad. Sci. USA, 106, 13939, 10.1073/pnas.0907143106 Schallert, 2000, CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury, Neuropharmacology, 39, 777, 10.1016/S0028-3908(00)00005-8 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 Smith, 2004, The thalamostriatal system: a highly specific network of the basal ganglia circuitry, Trends Neurosci., 27, 520, 10.1016/j.tins.2004.07.004 Smith, 2009, The thalamostriatal systems: anatomical and functional organization in normal and parkinsonian states, Brain Res. Bull., 78, 60, 10.1016/j.brainresbull.2008.08.015 Suárez, 2014, L-DOPA treatment selectively restores spine density in dopamine receptor D2-expressing projection neurons in dyskinetic mice, Biol. Psychiatry, 75, 711, 10.1016/j.biopsych.2013.05.006 Surmeier, 2017, Parkinson’s Disease Is Not Simply a Prion Disorder, J. Neurosci., 37, 9799, 10.1523/JNEUROSCI.1787-16.2017 Tanimura, 2018, Striatal cholinergic interneurons and Parkinson’s disease, Eur. J. Neurosci., 47, 1148, 10.1111/ejn.13638 Ungless, 2001, Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons, Nature, 411, 583, 10.1038/35079077 Van der Werf, 2002, The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness, Brain Res. Brain Res. Rev., 39, 107, 10.1016/S0165-0173(02)00181-9 Villalba, 2014, Neuronal loss in the caudal intralaminar thalamic nuclei in a primate model of Parkinson’s disease, Brain Struct. Funct., 219, 381, 10.1007/s00429-013-0507-9 Wada, 1989, Distribution of alpha 2, alpha 3, alpha 4, and beta 2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat, J. Comp. Neurol., 284, 314, 10.1002/cne.902840212 Yan, 1997, D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway, J. Neurophysiol., 77, 1003, 10.1152/jn.1997.77.2.1003 Yan, 2001, Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons, Neuroscience, 103, 1017, 10.1016/S0306-4522(01)00039-2 Zhou, 2002, Cholinergic interneuron characteristics and nicotinic properties in the striatum, J. Neurobiol., 53, 590, 10.1002/neu.10150