Diagnostic and statistical manual of mental disorders (DSM-5). 5th ed., Arlington (VA): American Psychiatric Association; 2013.
Fuccillo MV. Striatal circuits as a common node for autism pathophysiology. Front Neurosci. 2016;10:27.
Google Scholar
Li W, Pozzo-Miller L. Dysfunction of the corticostriatal pathway in autism spectrum disorders. J Neurosci Res. 2019;98:2130–47.
Google Scholar
Rapanelli M, Frick LR, Pittenger C. The role of interneurons in autism and tourette syndrome. Trends Neurosci. 2017;40:397–407.
Google Scholar
Contractor A, Ethell IM, Portera-Cailliau C. Cortical interneurons in autism. Nat Neurosci. 2021;24:1648–59.
Google Scholar
Ridley RM. The psychology of perserverative and stereotyped behaviour. Prog Neurobiol. 1994;44:221–31.
Google Scholar
Jutla A, Foss-Feig J, Veenstra-VanderWeele J. Autism spectrum disorder and schizophrenia: an updated conceptual review. Autism Res. 2022;15:384–412.
Google Scholar
Figee M, Pattij T, Willuhn I, Luigjes J, van den Brink W, Goudriaan A, et al. Compulsivity in obsessive-compulsive disorder and addictions. Eur Neuropsychopharmacol. 2016;26:856–68.
Google Scholar
Gerdeman GL, Partridge JG, Lupica CR, Lovinger DM. It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci. 2003;26:184–92.
Google Scholar
Burton CL, Longaretti A, Zlatanovic A, Gomes GM, Tonini R. Striatal insights: a cellular and molecular perspective on repetitive behaviors in pathology. Front Cell Neurosci. 2024;18:1386715.
Google Scholar
Kataoka Y, Kalanithi PS, Grantz H, Schwartz ML, Saper C, Leckman JF, et al. Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome. J Comp Neurol. 2010;518:277–91.
Google Scholar
Lennington JB, Coppola G, Kataoka-Sasaki Y, Fernandez TV, Palejev D, Li Y, et al. Transcriptome analysis of the human striatum in tourette syndrome. Biol Psychiatry. 2016;79:372–82.
Google Scholar
Xu M, Kobets A, Du JC, Lennington J, Li L, Banasr M, et al. Targeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome. Proc Natl Acad Sci USA. 2015;112:893–8.
Google Scholar
Martos YV, Braz BY, Beccaria JP, Murer MG, Belforte JE. Compulsive social behavior emerges after selective ablation of striatal cholinergic interneurons. J Neurosci. 2017;37:2849–58.
Google Scholar
Xu J, Liu RJ, Fahey S, Frick L, Leckman J, Vaccarino F, et al. Antibodies from children with PANDAS bind specifically to striatal cholinergic interneurons and alter their activity. Am J Psychiatry. 2021;178:48–64.
Google Scholar
Aliane V, Perez S, Bohren Y, Deniau JM, Kemel ML. Key role of striatal cholinergic interneurons in processes leading to arrest of motor stereotypies. Brain. 2011;134:110–8.
Google Scholar
Crittenden JR, Lacey CJ, Weng FJ, Garrison CE, Gibson DJ, Lin Y, et al. Striatal cholinergic interneurons modulate spike-timing in striosomes and matrix by an amphetamine-sensitive mechanism. Front Neuroanat. 2017;11:20.
Google Scholar
Prado VF, Janickova H, Al-Onaizi MA, Prado MA. Cholinergic circuits in cognitive flexibility. Neuroscience. 2017;345:130–41.
Google Scholar
Abudukeyoumu N, Hernandez-Flores T, Garcia-Munoz M, Arbuthnott GW. Cholinergic modulation of striatal microcircuits. Eur J Neurosci. 2019;49:604–22.
Google Scholar
Apicella P. The role of the intrinsic cholinergic system of the striatum: what have we learned from TAN recordings in behaving animals? Neuroscience. 2017;360:81–94.
Google Scholar
Goldberg JA, Wilson CJ. The cholinergic interneurons of the striatum: intrinsic properties underlie multiple discharge patterns. In: Steiner H, Tseng KY, editors. Handbook of basal ganglia structure and function. London (UK): Academic Press; 2010, pp 133–49.
Ahmed NY, Knowles R, Dehorter N. New insights into cholinergic neuron diversity. Front Mol Neurosci. 2019;12:204.
Google Scholar
Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci. 2000;23:120–6.
Google Scholar
Brimblecombe KR, Cragg SJ. The striosome and matrix compartments of the striatum: a path through the labyrinth from neurochemistry toward function. ACS Chem Neurosci. 2017;8:235–42.
Google Scholar
Kawaguchi Y. Neostriatal cell subtypes and their functional roles. Neurosci Res. 1997;27:1–8.
Google Scholar
Gerfen CR. The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci. 1992;15:133–9.
Google Scholar
Crittenden JR, Graybiel AM. Basal Ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front Neuroanat. 2011;5:59.
Google Scholar
Graybiel AM, Matsushima A. Striosomes and matrisomes: scaffolds for dynamic coupling of volition and action. Annu Rev Neurosci. 2023;46:359–80.
Google Scholar
Lazaridis I, Crittenden JR, Ahn G, Hirokane K, Wickersham IR, Yoshida T, et al. Striosomes control dopamine via dual pathways paralleling canonical basal ganglia circuits. Curr Biol. 2024;34:5263–83.e8.
Google Scholar
Kuo HY, Liu FC. Pathological alterations in striatal compartments in the human brain of autism spectrum disorder. Mol Brain. 2020;13:83.
Google Scholar
Kuo HY, Liu FC. Valproic acid induces aberrant development of striatal compartments and corticostriatal pathways in a mouse model of autism spectrum disorder. FASEB J. 2017;31:4458–71.
Google Scholar
Murray RC, Logan MC, Horner KA. Striatal patch compartment lesions reduce stereotypy following repeated cocaine administration. Brain Res. 2015;1618:286–98.
Google Scholar
Caubit X, Gubellini P, Andrieux J, Roubertoux PL, Metwaly M, Jacq B, et al. TSHZ3 deletion causes an autism syndrome and defects in cortical projection neurons. Nat Genet. 2016;48:1359–69.
Google Scholar
Caubit X, Gubellini P, Roubertoux PL, Carlier M, Molitor J, Chabbert D, et al. Targeted Tshz3 deletion in corticostriatal circuit components segregates core autistic behaviors. Transl Psychiatry. 2022;12:106.
Google Scholar
Caubit X, Arbeille E, Chabbert D, Desprez F, Messak I, Fatmi A, et al. Camk2a-Cre and Tshz3 expression in mouse striatal cholinergic interneurons: implications for autism spectrum disorder. Front Genet. 2021;12:683959.
Google Scholar
Chabbert D, Caubit X, Roubertoux PL, Carlier M, Habermann B, Jacq B, et al. Postnatal Tshz3 deletion drives altered corticostriatal function and autism spectrum disorder-like behavior. Biol Psychiatry. 2019;86:274–85.
Google Scholar
Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. Spatio-temporal transcriptome of the human brain. Nature. 2011;478:483–9.
Google Scholar
Roubertoux PL, Tordjman S, Caubit X, di Cristopharo J, Ghata A, Fasano L, et al. Construct validity and cross validity of a test battery modeling Autism Spectrum Disorder (ASD) in mice. Behav Genet. 2020;50:26–40.
Google Scholar
Knowles R, Dehorter N, Ellender T. From progenitors to progeny: shaping striatal circuit development and function. J Neurosci. 2021;41:9483–502.
Google Scholar
Marin O, Anderson SA, Rubenstein JL. Origin and molecular specification of striatal interneurons. J Neurosci. 2000;20:6063–76.
Google Scholar
Pappas SS, Li J, LeWitt TM, Kim JK, Monani UR, Dauer WT. A cell autonomous torsinA requirement for cholinergic neuron survival and motor control. Elife. 2018;7:e36691.
Google Scholar
Lopes R, Verhey van Wijk N, Neves G, Pachnis V. Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc Natl Acad Sci USA. 2012;109:3119–24.
Google Scholar
Furusho M, Ono K, Takebayashi H, Masahira N, Kagawa T, Ikeda K, et al. Involvement of the Olig2 transcription factor in cholinergic neuron development of the basal forebrain. Dev Biol. 2006;293:348–57.
Google Scholar
Caubit X, Tiveron MC, Cremer H, Fasano L. Expression patterns of the three Teashirt-related genes define specific boundaries in the developing and postnatal mouse forebrain. J Comp Neurol. 2005;486:76–88.
Google Scholar
van Vulpen EH, van der Kooy D. Striatal cholinergic interneurons: birthdates predict compartmental localization. Brain Res Dev Brain Res. 1998;109:51–8.
Google Scholar
Balleine BW, Liljeholm M, Ostlund SB. The integrative function of the basal ganglia in instrumental conditioning. Behav Brain Res. 2009;199:43–52.
Google Scholar
Rusu SI, Pennartz CMA. Learning, memory and consolidation mechanisms for behavioral control in hierarchically organized cortico-basal ganglia systems. Hippocampus. 2020;30:73–98.
Google Scholar
Song MR, Lee SW. Rethinking dopamine-guided action sequence learning. Eur J Neurosci. 2024;60:3447–65.
Google Scholar
Arlotta P, Molyneaux BJ, Jabaudon D, Yoshida Y, Macklis JD. Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J Neurosci. 2008;28:622–32.
Google Scholar
Wilson CJ. The mechanism of intrinsic amplification of hyperpolarizations and spontaneous bursting in striatal cholinergic interneurons. Neuron. 2005;45:575–85.
Google Scholar
Zhao Z, Zhang K, Liu X, Yan H, Ma X, Zhang S, et al. Involvement of HCN channel in muscarinic inhibitory action on tonic firing of dorsolateral striatal cholinergic interneurons. Front Cell Neurosci. 2016;10:71.
Google Scholar
Bennett BD, Wilson CJ. Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci. 1999;19:5586–96.
Google Scholar
Wilson CJ, Chang HT, Kitai ST. Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci. 1990;10:508–19.
Google Scholar
Prado VF, Roy A, Kolisnyk B, Gros R, Prado MA. Regulation of cholinergic activity by the vesicular acetylcholine transporter. Biochem J. 2013;450:265–74.
Google Scholar
Chen E, Lallai V, Sherafat Y, Grimes NP, Pushkin AN, Fowler JP, et al. Altered baseline and nicotine-mediated behavioral and cholinergic profiles in ChAT-Cre mouse lines. J Neurosci. 2018;38:2177–88.
Google Scholar
Hirsch EC, Graybiel AM, Hersh LB, Duyckaerts C, Agid Y. Striosomes and extrastriosomal matrix contain different amounts of immunoreactive choline acetyltransferase in the human striatum. Neurosci Lett. 1989;96:145–50.
Google Scholar
Graybiel AM, Baughman RW, Eckenstein F. Cholinergic neuropil of the striatum observes striosomal boundaries. Nature. 1986;323:625–7.
Google Scholar
Van Zandt M, Flanagan D, Pittenger C. Sex differences in the distribution and density of regulatory interneurons in the striatum. Front Cell Neurosci. 2024;18:1415015.
Google Scholar
Unal B, Ibanez-Sandoval O, Shah F, Abercrombie ED, Tepper JM. Distribution of tyrosine hydroxylase-expressing interneurons with respect to anatomical organization of the neostriatum. Front Syst Neurosci. 2011;5:41.
Google Scholar
Almey A, Filardo EJ, Milner TA, Brake WG. Estrogen receptors are found in glia and at extranuclear neuronal sites in the dorsal striatum of female rats: evidence for cholinergic but not dopaminergic colocalization. Endocrinology. 2012;153:5373–83.
Google Scholar
Kovesdi E, Udvaracz I, Kecskes A, Szocs S, Farkas S, Faludi P, et al. 17beta-estradiol does not have a direct effect on the function of striatal cholinergic interneurons in adult mice in vitro. Front Endocrinol (Lausanne). 2022;13:993552.
Google Scholar
van der Kooy D, Fishell G. Neuronal birthdate underlies the development of striatal compartments. Brain Res. 1987;401:155–61.
Google Scholar
Song DD, Harlan RE. Genesis and migration patterns of neurons forming the patch and matrix compartments of the rat striatum. Brain Res Dev Brain Res. 1994;83:233–45.
Google Scholar
Graybiel AM, Hickey TL. Chemospecificity of ontogenetic units in the striatum: demonstration by combining [3H]thymidine neuronography and histochemical staining. Proc Natl Acad Sci USA. 1982;79:198–202.
Google Scholar
Lebouc M, Richard Q, Garret M, Baufreton J. Striatal circuit development and its alterations in Huntington’s disease. Neurobiol Dis. 2020;145:105076.
Google Scholar
Chen L, Chatterjee M, Li JY. The mouse homeobox gene Gbx2 is required for the development of cholinergic interneurons in the striatum. J Neurosci. 2010;30:14824–34.
Google Scholar
Poppi LA, Ho-Nguyen KT, Shi A, Daut CT, Tischfield MA. Recurrent implication of striatal cholinergic interneurons in a range of neurodevelopmental, neurodegenerative, and neuropsychiatric disorders. Cells. 2021;10:907.
Google Scholar
Crittenden JR, Lacey CJ, Lee T, Bowden HA, Graybiel AM. Severe drug-induced repetitive behaviors and striatal overexpression of VAChT in ChAT-ChR2-EYFP BAC transgenic mice. Front Neural Circuits. 2014;8:57.
Google Scholar
Kubota Y, Kawaguchi Y. Spatial distributions of chemically identified intrinsic neurons in relation to patch and matrix compartments of rat neostriatum. J Comp Neurol. 1993;332:499–513.
Google Scholar
Johnston JG, Gerfen CR, Haber SN, van der Kooy D. Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization. Brain Res Dev Brain Res. 1990;57:93–102.
Google Scholar
Lee H, Leamey CA, Sawatari A. Rapid reversal of chondroitin sulfate proteoglycan associated staining in subcompartments of mouse neostriatum during the emergence of behaviour. PLoS One. 2008;3:e3020.
Google Scholar
Martone ME, Young SJ, Armstrong DM, Groves PM. The distribution of cholinergic perikarya with respect to enkephalin-rich patches in the caudate nucleus of the adult cat. J Chem Neuroanat. 1994;8:47–59.
Google Scholar
Bennett BD, Callaway JC, Wilson CJ. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci. 2000;20:8493–503.
Google Scholar
Lozovaya N, Eftekhari S, Cloarec R, Gouty-Colomer LA, Dufour A, Riffault B, et al. GABAergic inhibition in dual-transmission cholinergic and GABAergic striatal interneurons is abolished in Parkinson disease. Nat Commun. 2018;9:1422.
Google Scholar
Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci. 1993;13:4908–23.
Google Scholar
Marotta R, Risoleo MC, Messina G, Parisi L, Carotenuto M, Vetri L, et al. The neurochemistry of autism. Brain Sci. 2020;10:163.
Google Scholar
Karvat G, Kimchi T. Acetylcholine elevation relieves cognitive rigidity and social deficiency in a mouse model of autism. Neuropsychopharmacology. 2014;39:831–40.
Google Scholar
Rapanelli M, Frick LR, Xu M, Groman SM, Jindachomthong K, Tamamaki N, et al. Targeted interneuron depletion in the dorsal striatum produces autism-like behavioral abnormalities in male but not female mice. Biol Psychiatry. 2017;82:194–203.
Google Scholar
Athnaiel O, Job GA, Ocampo R, Teneqexhi P, Messer WS, Ragozzino ME. Effects of the partial M1 muscarinic cholinergic receptor agonist CDD-0102A on stereotyped motor behaviors and reversal learning in the BTBR mouse model of autism. Int J Neuropsychopharmacol. 2022;25:64–74.
Google Scholar
Ferhat AT, Verpy E, Biton A, Forget B, De Chaumont F, Mueller F, et al. Excessive self-grooming, gene dysregulation and imbalance between the striosome and matrix compartments in the striatum of Shank3 mutant mice. Front Mol Neurosci. 2023;16:1139118.
Google Scholar
Canales JJ, Graybiel AM. A measure of striatal function predicts motor stereotypy. Nat Neurosci. 2000;3:377–83.
Google Scholar
Sako W, Morigaki R, Nagahiro S, Kaji R, Goto S. Olfactory type G-protein alpha subunit in striosome-matrix dopamine systems in adult mice. Neuroscience. 2010;170:497–502.
Google Scholar
Saka E, Goodrich C, Harlan P, Madras BK, Graybiel AM. Repetitive behaviors in monkeys are linked to specific striatal activation patterns. J Neurosci. 2004;24:7557–65.
Google Scholar
Peter Z, Oliphant ME, Fernandez TV. Motor stereotypies: a pathophysiological review. Front Neurosci. 2017;11:171.
Google Scholar
Magno L, Barry C, Schmidt-Hieber C, Theodotou P, Hausser M, Kessaris N. NKX2-1 is required in the embryonic septum for cholinergic system development, learning, and memory. Cell Rep. 2017;20:1572–84.
Google Scholar
Fragkouli A, van Wijk NV, Lopes R, Kessaris N, Pachnis V. LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development. 2009;136:3841–51.
Google Scholar
Sreenivasan V, Serafeimidou-Pouliou E, Exposito-Alonso D, Bercsenyi K, Bernard C, Bae SE, et al. Input-specific control of interneuron numbers in nascent striatal networks. Proc Natl Acad Sci USA. 2022;119:e2118430119.
Google Scholar
Fino E, Vandecasteele M, Perez S, Saudou F, Venance L. Region-specific and state-dependent action of striatal GABAergic interneurons. Nat Commun. 2018;9:3339.
Google Scholar
Choi SJ, Ma TC, Ding Y, Cheung T, Joshi N, Sulzer D, et al. Alterations in the intrinsic properties of striatal cholinergic interneurons after dopamine lesion and chronic L-DOPA. Elife. 2020;9:e56920.
Google Scholar
Cheng J, Umschweif G, Leung J, Sagi Y, Greengard P. HCN2 Channels in Cholinergic Interneurons of Nucleus Accumbens Shell Regulate Depressive Behaviors. Neuron. 2019;101:662–72.e5.
Google Scholar
Ahmed NY, Knowles R, Liu L, Yan Y, Li X, Schumann U, et al. Developmental deficits of MGE-derived interneurons in the Cntnap2 knockout mouse model of autism spectrum disorder. Front Cell Dev Biol. 2023;11:1112062.
Google Scholar
Bonsi P, Cuomo D, Martella G, Madeo G, Schirinzi T, Puglisi F, et al. Centrality of striatal cholinergic transmission in Basal Ganglia function. Front Neuroanat. 2011;5:6.
Google Scholar
Gertler TS, Chan CS, Surmeier DJ. Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci. 2008;28:10814–24.
Google Scholar
Inoue R, Suzuki T, Nishimura K, Miura M. Nicotinic acetylcholine receptor-mediated GABAergic inputs to cholinergic interneurons in the striosomes and the matrix compartments of the mouse striatum. Neuropharmacology. 2016;105:318–28.
Google Scholar
Friedman A, Hueske E, Drammis SM, Toro Arana SE, Nelson ED, Carter CW, et al. Striosomes mediate value-based learning vulnerable in age and a Huntington’s disease model. Cell. 2020;183:918–34.e49.
Google Scholar
Caubit X, Lye CM, Martin E, Core N, Long DA, Vola C, et al. Teashirt 3 is necessary for ureteral smooth muscle differentiation downstream of SHH and BMP4. Development. 2008;135:3301–10.
Google Scholar
Mao X, Fujiwara Y, Orkin SH. Improved reporter strain for monitoring Cre recombinase-mediated DNA excisions in mice. Proc Natl Acad Sci USA. 1999;96:5037–42.
Google Scholar
Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci. 2010;13:133–40.
Google Scholar
Rossi J, Balthasar N, Olson D, Scott M, Berglund E, Lee CE, et al. Melanocortin-4 receptors expressed by cholinergic neurons regulate energy balance and glucose homeostasis. Cell Metab. 2011;13:195–204.
Google Scholar
Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 1995;18:527–35.
Google Scholar
Haghdoust H, Janahmadi M, Behzadi G. Physiological role of dendrotoxin-sensitive K+ channels in the rat cerebellar Purkinje neurons. Physiol Res. 2007;56:807–13.
Google Scholar
Maisano X, Litvina E, Tagliatela S, Aaron GB, Grabel LB, Naegele JR. Differentiation and functional incorporation of embryonic stem cell-derived GABAergic interneurons in the dentate gyrus of mice with temporal lobe epilepsy. J Neurosci. 2012;32:46–61.
Google Scholar
Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates, 2nd Edition. ed., San Diego (CA): Academic Press; 2001.
Akoglu H. User’s guide to correlation coefficients. Turk J Emerg Med. 2018;18:91–3.
Google Scholar