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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The thalamostriatal system in normal and diseased states</title><author><name sortKey="Smith, Yoland" sort="Smith, Yoland" uniqKey="Smith Y" first="Yoland" last="Smith">Yoland Smith</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Galvan, Adriana" sort="Galvan, Adriana" uniqKey="Galvan A" first="Adriana" last="Galvan">Adriana Galvan</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Ellender, Tommas J" sort="Ellender, Tommas J" uniqKey="Ellender T" first="Tommas J." last="Ellender">Tommas J. Ellender</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author><author><name sortKey="Doig, Natalie" sort="Doig, Natalie" uniqKey="Doig N" first="Natalie" last="Doig">Natalie Doig</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author><author><name sortKey="Villalba, Rosa M" sort="Villalba, Rosa M" uniqKey="Villalba R" first="Rosa M." last="Villalba">Rosa M. Villalba</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Huerta Ocampo, Icnelia" sort="Huerta Ocampo, Icnelia" uniqKey="Huerta Ocampo I" first="Icnelia" last="Huerta-Ocampo">Icnelia Huerta-Ocampo</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author><author><name sortKey="Wichmann, Thomas" sort="Wichmann, Thomas" uniqKey="Wichmann T" first="Thomas" last="Wichmann">Thomas Wichmann</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Bolam, J Paul" sort="Bolam, J Paul" uniqKey="Bolam J" first="J. Paul" last="Bolam">J. Paul Bolam</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24523677</idno><idno type="pmc">3906602</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3906602</idno><idno type="RBID">PMC:3906602</idno><idno type="doi">10.3389/fnsys.2014.00005</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000334</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000334</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The thalamostriatal system in normal and diseased states</title><author><name sortKey="Smith, Yoland" sort="Smith, Yoland" uniqKey="Smith Y" first="Yoland" last="Smith">Yoland Smith</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Galvan, Adriana" sort="Galvan, Adriana" uniqKey="Galvan A" first="Adriana" last="Galvan">Adriana Galvan</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Ellender, Tommas J" sort="Ellender, Tommas J" uniqKey="Ellender T" first="Tommas J." last="Ellender">Tommas J. Ellender</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author><author><name sortKey="Doig, Natalie" sort="Doig, Natalie" uniqKey="Doig N" first="Natalie" last="Doig">Natalie Doig</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author><author><name sortKey="Villalba, Rosa M" sort="Villalba, Rosa M" uniqKey="Villalba R" first="Rosa M." last="Villalba">Rosa M. Villalba</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Huerta Ocampo, Icnelia" sort="Huerta Ocampo, Icnelia" uniqKey="Huerta Ocampo I" first="Icnelia" last="Huerta-Ocampo">Icnelia Huerta-Ocampo</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author><author><name sortKey="Wichmann, Thomas" sort="Wichmann, Thomas" uniqKey="Wichmann T" first="Thomas" last="Wichmann">Thomas Wichmann</name><affiliation><nlm:aff id="aff1"><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></nlm:aff></affiliation></author><author><name sortKey="Bolam, J Paul" sort="Bolam, J Paul" uniqKey="Bolam J" first="J. Paul" last="Bolam">J. Paul Bolam</name><affiliation><nlm:aff id="aff4"><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Systems Neuroscience</title><idno type="eISSN">1662-5137</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Because of our limited knowledge of the functional role of the thalamostriatal system, this massive network is often ignored in models of the pathophysiology of brain disorders of basal ganglia origin, such as Parkinson’s disease (PD). However, over the past decade, significant advances have led to a deeper understanding of the anatomical, electrophysiological, behavioral and pathological aspects of the thalamostriatal system. The cloning of the vesicular glutamate transporters 1 and 2 (vGluT1 and vGluT2) has provided powerful tools to differentiate thalamostriatal from corticostriatal glutamatergic terminals, allowing us to carry out comparative studies of the synaptology and plasticity of these two systems in normal and pathological conditions. Findings from these studies have led to the recognition of two thalamostriatal systems, based on their differential origin from the caudal intralaminar nuclear group, the center median/parafascicular (CM/Pf) complex, or other thalamic nuclei. The recent use of optogenetic methods supports this model of the organization of the thalamostriatal systems, showing differences in functionality and glutamate receptor localization at thalamostriatal synapses from Pf and other thalamic nuclei. At the functional level, evidence largely gathered from thalamic recordings in awake monkeys strongly suggests that the thalamostriatal system from the CM/Pf is involved in regulating alertness and switching behaviors. Importantly, there is evidence that the caudal intralaminar nuclei and their axonal projections to the striatum partly degenerate in PD and that CM/Pf deep brain stimulation (DBS) may be therapeutically useful in several movement disorders.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Ackermans, L" uniqKey="Ackermans L">L. Ackermans</name></author><author><name sortKey="Duits, A" uniqKey="Duits A">A. Duits</name></author><author><name sortKey="Temel, Y" uniqKey="Temel Y">Y. Temel</name></author><author><name sortKey="Winogrodzka, A" uniqKey="Winogrodzka A">A. Winogrodzka</name></author><author><name sortKey="Peeters, F" uniqKey="Peeters F">F. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Syst Neurosci</journal-id><journal-id journal-id-type="iso-abbrev">Front Syst Neurosci</journal-id><journal-id journal-id-type="publisher-id">Front. Syst. Neurosci.</journal-id><journal-title-group><journal-title>Frontiers in Systems Neuroscience</journal-title></journal-title-group><issn pub-type="epub">1662-5137</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24523677</article-id><article-id pub-id-type="pmc">3906602</article-id><article-id pub-id-type="doi">10.3389/fnsys.2014.00005</article-id><article-categories><subj-group subj-group-type="heading"><subject>Neuroscience</subject><subj-group><subject>Review Article</subject></subj-group></subj-group></article-categories><title-group><article-title>The thalamostriatal system in normal and diseased states</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Smith</surname><given-names>Yoland</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Galvan</surname><given-names>Adriana</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ellender</surname><given-names>Tommas J.</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Doig</surname><given-names>Natalie</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Villalba</surname><given-names>Rosa M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Huerta-Ocampo</surname><given-names>Icnelia</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wichmann</surname><given-names>Thomas</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bolam</surname><given-names>J. Paul</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Yerkes National Primate Research Center, Emory University</institution><country>Atlanta, GA, USA</country></aff><aff id="aff2"><sup>2</sup><institution>Department of Neurology, Emory University</institution><country>Atlanta, GA, USA</country></aff><aff id="aff3"><sup>3</sup><institution>Udall Center of Excellence for Parkinson’s Disease, Emory University</institution><country>Atlanta, GA, USA</country></aff><aff id="aff4"><sup>4</sup><institution>Department of Pharmacology, MRC Anatomical Neuropharmacology Unit</institution><country>Oxford, UK</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Hagai Bergman, The Hebrew University, Israel</p></fn><fn fn-type="edited-by"><p>Reviewed by: Jose L. Lanciego, University of Navarra, Spain; Antonio Pisani, Università di Roma “Tor Vergata”, Italy</p></fn><corresp id="fn001">*Correspondence: Yoland Smith, Yerkes National Primate Research Center, Emory University, 954, Gatewood Road NE, Atlanta, GA 30329, USA e-mail: <email xlink:type="simple">ysmit01@emory.edu</email></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to the journal Frontiers in Systems Neuroscience.</p></fn></author-notes><pub-date pub-type="epub"><day>30</day><month>1</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>8</volume><elocation-id>5</elocation-id><history><date date-type="received"><day>12</day><month>11</month><year>2013</year></date><date date-type="accepted"><day>11</day><month>1</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 Smith, Galvan, Ellender, Doig, Villalba, Huerta-Ocampo, Wichman and Bolam.</copyright-statement><copyright-year>2014</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Because of our limited knowledge of the functional role of the thalamostriatal system, this massive network is often ignored in models of the pathophysiology of brain disorders of basal ganglia origin, such as Parkinson’s disease (PD). However, over the past decade, significant advances have led to a deeper understanding of the anatomical, electrophysiological, behavioral and pathological aspects of the thalamostriatal system. The cloning of the vesicular glutamate transporters 1 and 2 (vGluT1 and vGluT2) has provided powerful tools to differentiate thalamostriatal from corticostriatal glutamatergic terminals, allowing us to carry out comparative studies of the synaptology and plasticity of these two systems in normal and pathological conditions. Findings from these studies have led to the recognition of two thalamostriatal systems, based on their differential origin from the caudal intralaminar nuclear group, the center median/parafascicular (CM/Pf) complex, or other thalamic nuclei. The recent use of optogenetic methods supports this model of the organization of the thalamostriatal systems, showing differences in functionality and glutamate receptor localization at thalamostriatal synapses from Pf and other thalamic nuclei. At the functional level, evidence largely gathered from thalamic recordings in awake monkeys strongly suggests that the thalamostriatal system from the CM/Pf is involved in regulating alertness and switching behaviors. Importantly, there is evidence that the caudal intralaminar nuclei and their axonal projections to the striatum partly degenerate in PD and that CM/Pf deep brain stimulation (DBS) may be therapeutically useful in several movement disorders.</p></abstract><kwd-group><kwd>thalamus</kwd><kwd>Parkinson’s disease</kwd><kwd>intralaminar nuclei</kwd><kwd>glutamate</kwd><kwd>vesicular glutamate transporter</kwd><kwd>attention</kwd><kwd>striatum</kwd><kwd>Tourette’s syndrome</kwd></kwd-group><counts><fig-count count="6"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="203"></ref-count><page-count count="18"></page-count><word-count count="14461"></word-count></counts></article-meta></front><body><sec id="s1"><title>Introduction</title><p>Although the evolution of the thalamus and striatum pre-dates the expansion of the cerebral cortex (Butler, <xref rid="B25" ref-type="bibr">1994</xref>; Reiner, <xref rid="B146" ref-type="bibr">2010</xref>; Stephenson-Jones et al., <xref rid="B175" ref-type="bibr">2011</xref>), our knowledge about the functional anatomy and behavioral role of the connections between them is minimal compared to the amount of information that has been gathered about the corticostriatal system (Kemp and Powell, <xref rid="B90" ref-type="bibr">1971</xref>; Alexander et al., <xref rid="B5" ref-type="bibr">1986</xref>; Parent and Hazrati, <xref rid="B135" ref-type="bibr">1995</xref>). However, significant progress has been made in our understanding of the anatomical and functional organization of the thalamostriatal system since its first description in the early 1940’s (Vogt and Vogt, <xref rid="B194" ref-type="bibr">1941</xref>; Cowan and Powell, <xref rid="B34" ref-type="bibr">1956</xref>). Research in the last decade has resulted in a much better understanding of various aspects of the synaptic properties of the thalamostriatal projection(s), and their potential roles in cognition. Furthermore, evidence that the center median/parafascicular (CM/Pf) complex, the main source of thalamostriatal connections, is severely degenerated in Parkinson’s disease (PD), combined with the fact that lesion or deep brain stimulation (DBS) of this nuclear group alleviates some of the motor and non-motor symptoms of Tourette’s syndrome (TS) and PD, has generated significant interest in these projections. In this review, we will discuss these topics and provide an overview of our current knowledge of the functional anatomy, synaptology, and physiology of the mammalian thalamostriatal system, as well as the involvement of these projections in disease processes. Because of space limitation, we will focus mostly on recent developments in this field. Readers are referred to previous reviews for additional information and a broader coverage of the early literature on the thalamostriatal projections (Groenewegen and Berendse, <xref rid="B61" ref-type="bibr">1994</xref>; Parent and Hazrati, <xref rid="B135" ref-type="bibr">1995</xref>; Mengual et al., <xref rid="B122" ref-type="bibr">1999</xref>; Haber and Mcfarland, <xref rid="B64" ref-type="bibr">2001</xref>; Van der Werf et al., <xref rid="B180" ref-type="bibr">2002</xref>; Kimura et al., <xref rid="B93" ref-type="bibr">2004</xref>; Smith et al., <xref rid="B170" ref-type="bibr">2004</xref>, <xref rid="B169" ref-type="bibr">2009</xref>, <xref rid="B167" ref-type="bibr">2010</xref>, <xref rid="B171" ref-type="bibr">2011</xref>; McHaffie et al., <xref rid="B120" ref-type="bibr">2005</xref>; Haber and Calzavara, <xref rid="B63" ref-type="bibr">2009</xref>; Halliday, <xref rid="B66" ref-type="bibr">2009</xref>; Minamimoto et al., <xref rid="B126" ref-type="bibr">2009</xref>; Sadikot and Rymar, <xref rid="B155" ref-type="bibr">2009</xref>; Galvan and Smith, <xref rid="B55" ref-type="bibr">2011</xref>; Bradfield et al., <xref rid="B21" ref-type="bibr">2013b</xref>).</p></sec><sec id="s2"><title>Thalamostriatal circuitry and synaptic connectivity</title><sec id="s2-1"><title>Functionally segregated basal ganglia-thalamostriatal circuits through the center median/parafascicular (CM/Pf) complex</title><p>Although the thalamostriatal system originates from most thalamic nuclei, the CM/Pf (or the Pf in rodents) is the main source of thalamostriatal projections in primates and non-primates (Smith and Parent, <xref rid="B168" ref-type="bibr">1986</xref>; Berendse and Groenewegen, <xref rid="B14" ref-type="bibr">1990</xref>; Francois et al., <xref rid="B49" ref-type="bibr">1991</xref>; Sadikot et al., <xref rid="B153" ref-type="bibr">1992a</xref>,<xref rid="B154" ref-type="bibr">b</xref>; Deschenes et al., <xref rid="B39" ref-type="bibr">1996a</xref>,<xref rid="B40" ref-type="bibr">b</xref>; Mengual et al., <xref rid="B122" ref-type="bibr">1999</xref>; McFarland and Haber, <xref rid="B118" ref-type="bibr">2000</xref>; Mcfarland and Haber, <xref rid="B119" ref-type="bibr">2001</xref>; Smith et al., <xref rid="B170" ref-type="bibr">2004</xref>, <xref rid="B169" ref-type="bibr">2009</xref>; Castle et al., <xref rid="B28" ref-type="bibr">2005</xref>; McHaffie et al., <xref rid="B120" ref-type="bibr">2005</xref>; Parent and Parent, <xref rid="B138" ref-type="bibr">2005</xref>; Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>; Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>). CM/Pf neurons send massive and topographically organized projections to specific regions of the dorsal striatum, but provide only minor inputs to the cerebral cortex (Sadikot et al., <xref rid="B153" ref-type="bibr">1992a</xref>; Parent and Parent, <xref rid="B138" ref-type="bibr">2005</xref>; Galvan and Smith, <xref rid="B55" ref-type="bibr">2011</xref>; Figure <xref ref-type="fig" rid="F1">1</xref>). Single cell tracing studies in monkeys have shown that more than half of all CM neurons innervate densely and focally the striatum without significant input to the cerebral cortex, while about one third innervates diffusely the cerebral cortex without significant projections to the striatum, and the remaining neurons project to both targets with a preponderance of innervation of the dorsal striatum (Parent and Parent, <xref rid="B138" ref-type="bibr">2005</xref>).</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Summary of the anatomical, functional and pathological characteristics that differentiate thalamostriatal projections from the CM/Pf vs. other thalamic nuclei (i.e., non CM/Pf)</bold>.</p></caption><graphic xlink:href="fnsys-08-00005-g0001"></graphic></fig><p>Based on its preferential targeting of specific functional territories, the primate CM/Pf complex is divided into five major sub-regions: (1) the rostral third of Pf which innervates mainly the nucleus accumbens; (2) the caudal two thirds of Pf which project to the caudate nucleus; (3) the dorsolateral extension of Pf (Pfdl) which targets selectively the anterior putamen; (4) the medial two thirds of CM (CMm) which innervates the post-commissural putamen; and (5) the lateral third of CM (CMl) which is the source of inputs the primary motor cortex (M1). Through these projections, the CM/Pf gains access to the entire striatal complex, thereby making the CM/Pf-striatal system a functionally organized network that may broadly affect motor and non-motor basal ganglia functions (Smith et al., <xref rid="B170" ref-type="bibr">2004</xref>, <xref rid="B169" ref-type="bibr">2009</xref>, <xref rid="B167" ref-type="bibr">2010</xref>; Galvan and Smith, <xref rid="B55" ref-type="bibr">2011</xref>). In rodents, the lateral part of Pf is considered to be the homologue of the primate CM and projects mainly to the sensorimotor region (i.e., the dorsolateral part) of the caudate-putamen complex, whereas the medial rodent Pf displays strong similarities with the primate Pf, projecting to associative and limbic striatal regions of the striatum (Groenewegen and Berendse, <xref rid="B61" ref-type="bibr">1994</xref>).</p></sec><sec id="s2-2"><title>Thalamostriatal systems from non-center median/parafascicular (CM/Pf) thalamic nuclei</title><p>In addition to the CM/Pf complex, thalamostriatal projections originate from several other rostral intralaminar and non-intralaminar thalamic nuclei. In primates and non-primates, the rostral intralaminar nuclei (central lateral, paracentral, central medial), the mediodorsal nucleus (MD), the pulvinar, the lateral posterior nucleus, the medial posterior nucleus, midline, anterior and the ventral motor nuclear group are prominent sources of thalamostriatal projections to the caudate nucleus and putamen (Royce, <xref rid="B149" ref-type="bibr">1978</xref>; Beckstead, <xref rid="B13" ref-type="bibr">1984</xref>; Smith and Parent, <xref rid="B168" ref-type="bibr">1986</xref>; Groenewegen and Berendse, <xref rid="B61" ref-type="bibr">1994</xref>; Smith et al., <xref rid="B170" ref-type="bibr">2004</xref>, <xref rid="B169" ref-type="bibr">2009</xref>; Alloway et al., <xref rid="B6" ref-type="bibr">2014</xref>). In contrast to the projections from the CM/Pf complex, these nuclei send major projections to the cerebral cortex, while contributing a modest or sparse innervation of the dorsal and ventral striatum (Royce, <xref rid="B150" ref-type="bibr">1983</xref>; Macchi et al., <xref rid="B113" ref-type="bibr">1984</xref>; Deschenes et al., <xref rid="B39" ref-type="bibr">1996a</xref>,<xref rid="B40" ref-type="bibr">b</xref>; Smith et al., <xref rid="B170" ref-type="bibr">2004</xref>, <xref rid="B169" ref-type="bibr">2009</xref>; Figure <xref ref-type="fig" rid="F1">1</xref>). In rats, the topography of these projections corresponds to the functionally segregated organization of the striatum, so that sensorimotor-, associative- and limbic-related thalamic nuclei innervate functionally corresponding regions of the dorsal and ventral striatum (Berendse and Groenewegen, <xref rid="B14" ref-type="bibr">1990</xref>, <xref rid="B15" ref-type="bibr">1991</xref>; Groenewegen and Berendse, <xref rid="B61" ref-type="bibr">1994</xref>). Although such detailed analyses have not been done in primates (except for projections from the ventral anterior/ventral lateral (VA/VL) complex), evidence from retrograde and anterograde labeling studies indicate that the primate non-CM/Pf thalamostriatal projections also display a strict functional topography (Parent et al., <xref rid="B136" ref-type="bibr">1983</xref>; Smith and Parent, <xref rid="B168" ref-type="bibr">1986</xref>; Fenelon et al., <xref rid="B48" ref-type="bibr">1991</xref>; McFarland and Haber, <xref rid="B118" ref-type="bibr">2000</xref>; Mcfarland and Haber, <xref rid="B119" ref-type="bibr">2001</xref>). The thalamostriatal projections from the ventral motor thalamic nuclei have received particular attention in these studies. It appears that projections from the pars oralis of the VL (VLo), the main recipient of sensorimotor internal globus pallidus (GPi) outflow, terminate preferentially in the post-commissural putamen, whereas projections from the magnocellular division of the VA, the principal target of the substantia nigra pars reticulata (SNr) and associative GPi outflow, innervate the caudate nucleus (Mcfarland and Haber, <xref rid="B119" ref-type="bibr">2001</xref>). Within striatal territories, VA/VL projections terminate in a patchy manner in the striatum, indicating that additional organizational principles may be at work that have not yet been elucidated (Groenewegen and Berendse, <xref rid="B61" ref-type="bibr">1994</xref>; McFarland and Haber, <xref rid="B118" ref-type="bibr">2000</xref>; Mcfarland and Haber, <xref rid="B119" ref-type="bibr">2001</xref>; Smith et al., <xref rid="B170" ref-type="bibr">2004</xref>, <xref rid="B169" ref-type="bibr">2009</xref>; Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>).</p><p>Through the use of trans-synaptic viral tracing studies, Strick and colleagues have suggested that thalamostriatal projections from the VL and other intralaminar thalamic nuclei that receive cerebellar outflow from the dentate nucleus may be the underlying connections through which the cerebellum communicates with the basal ganglia (Bostan and Strick, <xref rid="B18" ref-type="bibr">2010</xref>; Bostan et al., <xref rid="B17" ref-type="bibr">2010</xref>, <xref rid="B19" ref-type="bibr">2013</xref>). Dysfunctions of these cerebello-thalamo-basal ganglia interactions may underlie some aspects of the pathophysiology of dystonia and other movement disorders (Jinnah and Hess, <xref rid="B86" ref-type="bibr">2006</xref>; Neychev et al., <xref rid="B133" ref-type="bibr">2008</xref>; Calderon et al., <xref rid="B26" ref-type="bibr">2011</xref>).</p></sec><sec id="s2-3"><title>The superior colliculus: A potential driver of the thalamostriatal system in mammals</title><p>Anatomical studies have suggested that additional sub-cortical tecto-basal ganglia loops exist that connect the superficial and deep layers of the superior colliculus with specific thalamic nuclei, which then gain access to the basal ganglia circuitry via thalamostriatal connections (McHaffie et al., <xref rid="B120" ref-type="bibr">2005</xref>; Redgrave et al., <xref rid="B144" ref-type="bibr">2010</xref>). The existence of these connections could resolve some of the fundamental issues associated with short-latency responses to biologically salient stimuli (Smith et al., <xref rid="B171" ref-type="bibr">2011</xref>; Alloway et al., <xref rid="B6" ref-type="bibr">2014</xref>). As discussed in more detail below, Pf neurons exhibit short-latency excitatory responses to salient stimuli. Redgrave and colleagues have suggested that the superior colliculus (optic tectum in lower species) displays the evolutionary profile, anatomical connectivity and physiological features that would allow it to mediate such effects upon thalamic neurons (McHaffie et al., <xref rid="B120" ref-type="bibr">2005</xref>; Redgrave et al., <xref rid="B144" ref-type="bibr">2010</xref>). The basal ganglia and the superior colliculus are neural structures that appeared early (>400 million years ago) and have been highly conserved throughout the evolution of the vertebrate brain (Reiner, <xref rid="B146" ref-type="bibr">2010</xref>; Stephenson-Jones et al., <xref rid="B175" ref-type="bibr">2011</xref>), thereby suggesting that they are part of fundamental processing units that play basic functions in mammalian behavior. The superior colliculus has direct access to primary sensory information, and studies have shown that stimuli associated with positive or negative outcomes activate different sub-regions of this nucleus that engage various tecto-thalamo-striatal loops (Redgrave et al., <xref rid="B143" ref-type="bibr">1999</xref>; Alloway et al., <xref rid="B6" ref-type="bibr">2014</xref>). Through these loops, the primary sensory events could be rapidly transmitted to the striatum and affect the basal ganglia circuitry which, in turn, could lead to basal ganglia-mediated disinhibition of different sub-regions of the superior colliculus that could help select and reinforce some sensory stimuli over others (Redgrave et al., <xref rid="B143" ref-type="bibr">1999</xref>), most likely through regulation of corticostriatal plasticity via dopaminergic and cholinergic intrastriatal mechanisms (Ding et al., <xref rid="B42" ref-type="bibr">2010</xref>; Smith et al., <xref rid="B171" ref-type="bibr">2011</xref>). Through these processes, the short-latency sensory-driven activity in the superior colliculus could be used by the basal ganglia to reinforce the development of novel habits or procedures (Redgrave et al., <xref rid="B144" ref-type="bibr">2010</xref>; Smith et al., <xref rid="B171" ref-type="bibr">2011</xref>).</p></sec><sec id="s2-4"><title>Synaptic organization and prevalence of thalamostriatal vs. corticostriatal terminals</title><p>Anterograde tracing studies in several species have shown that the thalamostriatal projections give rise to asymmetric (or Gray’s Type 1) synapses. In rodents, the principal synaptic target of most non-CM/Pf thalamostriatal projections are dendritic spines of striatal medium spiny neurons (MSNs), a pattern of synaptic connectivity similar to the corticostriatal system (Kemp and Powell, <xref rid="B90" ref-type="bibr">1971</xref>; Dube et al., <xref rid="B45" ref-type="bibr">1988</xref>; Xu et al., <xref rid="B198" ref-type="bibr">1991</xref>; Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>; Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>; Figures <xref ref-type="fig" rid="F1">1</xref>, <xref ref-type="fig" rid="F2">2</xref>). In contrast, striatal afferents from CM/Pf (or Pf in rodents) establish asymmetric synapses principally with dendritic shafts of MSNs (Dube et al., <xref rid="B45" ref-type="bibr">1988</xref>; Sadikot et al., <xref rid="B154" ref-type="bibr">1992b</xref>; Smith et al., <xref rid="B166" ref-type="bibr">1994</xref>; Sidibe and Smith, <xref rid="B162" ref-type="bibr">1996</xref>; Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>, <xref rid="B141" ref-type="bibr">2008</xref>; Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>) and several types of striatal interneurons including cholinergic interneurons (Meredith and Wouterlood, <xref rid="B123" ref-type="bibr">1990</xref>; Lapper and Bolam, <xref rid="B107" ref-type="bibr">1992</xref>; Sidibe and Smith, <xref rid="B163" ref-type="bibr">1999</xref>) and parvalbumin-positive GABA interneurons (Rudkin and Sadikot, <xref rid="B152" ref-type="bibr">1999</xref>; Sidibe and Smith, <xref rid="B163" ref-type="bibr">1999</xref>; Figure <xref ref-type="fig" rid="F1">1</xref>). Overall, 70–90% of CM/Pf (or Pf) terminals form axo-dendritic synapses in the rat and monkey striatum (Dube et al., <xref rid="B45" ref-type="bibr">1988</xref>; Sadikot et al., <xref rid="B154" ref-type="bibr">1992b</xref>; Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>; Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>). However, single cell filling studies have revealed that the pattern of synaptic connection of individual Pf neurons is highly variable in rats. For instance, some Pf neurons were found to be the sources of terminals that terminate almost exclusively on dendritic spines, whereas others predominantly target dendritic shafts (Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>). It is not known whether these neurons represent functionally different subpopulations of Pf-striatal cells.</p><fig id="F2" position="float"><label>Figure 2</label><caption><p><bold>Differential pattern of activity and synaptic connectivity of CM/Pf vs. non-CM/Pf thalamostriatal terminals. (A)</bold> Thalamostriatal neurons of the central lateral nucleus (non-CM/Pf) have a compact bushy dendritic arbor. They tend to fire brief bursts of spikes at high frequency (2–5 spikes at ~150 Hz) in time with the active part of the cortical slow oscillation, reminiscent of low-threshold Ca<sup>2+</sup> spike bursts. At the ultrastructural level, terminals from the central lateral nucleus almost exclusively target spines in the striatum. <bold>(B)</bold> Thalamostriatal neurons of the parafascicular nucleus have a reticular dendritic arbor with long and infrequently branching dendrites. They also tend to fire bursts of action potentials in time with the active part of the cortical slow oscillation, but the burst spike frequency is significantly lower and more variable than those of central lateral neurons. At the ultrastructural level, terminals from the parafascicular nucleus predominantly target the dendritic shafts of striatal neurons (see Lacey et al., <xref rid="B104" ref-type="bibr">2005</xref>, <xref rid="B103" ref-type="bibr">2007</xref> for more details). <bold>(C)</bold> Histogram showing the frequency of axo-dendritic vs. axo-spinous synapses formed by anterogradely labeled boutons from various thalamic nuclei and the primary motor cortex (M1) in the rat striatum. Note the striking difference in the pattern of synaptic connectivity of terminals from Pf vs. other thalamic nuclei (see Raju et al., <xref rid="B142" ref-type="bibr">2006</xref> for more details). Abbreviations: AV: Anteroventral nucleus; CL: Central lateral nucleus; LD: Laterodorsal nucleus; MD: Mediodorsal nucleus; M1: Primary motor cortex; Pf: Parafascicular nucleus; VA/VL: Ventral anterior/ventral lateral nucleus.</p></caption><graphic xlink:href="fnsys-08-00005-g0002"></graphic></fig><p>The cloning of the vesicular glutamate transporters 1 or 2 (vGluT1 or vGluT2) (Fremeau et al., <xref rid="B50" ref-type="bibr">2001</xref>, <xref rid="B51" ref-type="bibr">2004</xref>) and the demonstration that these transporters are differentially expressed in corticostriatal (vGluT1-positive) or thalamostriatal (vGluT2-positive) terminals (but see Barroso-Chinea et al., <xref rid="B204" ref-type="bibr">2008</xref>) have helped with the assessment of the relative prevalence, and the characterization of the synaptic connectivity of corticostriatal and thalamostriatal terminals in rodents and nonhuman primates. These studies showed that 95% of all vGluT1-positive corticostriatal projections terminate on dendritic spines of striatal neurons, and 5% on dendrites in both rodents and primates. This pattern is different from that of vGluT2-containing thalamostriatal boutons. For instance, only 50–65% (depending on the striatal region) of vGluT2-containing terminals contact dendritic spines in monkeys, while the remaining form asymmetric synapses with dendritic shafts (Raju et al., <xref rid="B141" ref-type="bibr">2008</xref>). In rats, as many as 80% of vGluT2-positive terminals form axo-spinous synapses in the striatum (Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>; Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>). Whether these differences in the proportion of vGluT2 terminals in contact with striatal spines represent a genuine species difference in the microcircuitry of the thalamostriatal system between primates and non-primates remain to be determined.</p><p>It is also important to note that the synaptic connectivity of vGluT2-containing terminals differs between the patch/striosome and the matrix compartments of the striatum in rats. While the ratio of axo-spinous and axo-dendritic synapses for vGluT2-immunoreactive terminals is 90:10 in the patch compartment, it is about 55:45 in the matrix (Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>; Figure <xref ref-type="fig" rid="F1">1</xref>). The fact that the massive thalamostriatal projection from Pf, a predominant source of axo-dendritic glutamatergic synapses, terminates exclusively in the striatal matrix accounts for this difference in the overall synaptology of vGluT2-containing terminals between the two striatal compartments (Herkenham and Pert, <xref rid="B76" ref-type="bibr">1981</xref>; Sadikot et al., <xref rid="B154" ref-type="bibr">1992b</xref>; Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>). Evidence that activity imbalances between the patch/striosome and matrix compartments may be involved in various basal ganglia disorders (Crittenden and Graybiel, <xref rid="B36" ref-type="bibr">2011</xref>) highlights the potential significance of this compartmental segregation of CM/Pf inputs to the mammalian striatum. In contrast to vGluT2, the pattern of synaptic innervation of corticostriatal vGluT1-positive terminals does not differ between patch/striosome and matrix compartments (Raju et al., <xref rid="B142" ref-type="bibr">2006</xref>).</p><p>The use of vGluT1 and vGluT2 also allowed the quantification of the relative prevalence of cortical and thalamic terminals in the rat and monkey striatum. In the monkey post-commissural putamen, ~50% of putative glutamatergic terminals (i.e., those forming asymmetric synapses) express vGluT1, ~25% contain vGluT2 and ~25% do not display immunoreactivity for either vGluT1 or vGluT2 (Raju et al., <xref rid="B141" ref-type="bibr">2008</xref>). In rats, the differences in the prevalence of vGluT1 over vGluT2 terminals is not as striking (35% vGluT1 vs. 25% vGluT2 in rats), and the percentage of putative glutamatergic terminals unlabeled for either transporter subtype is higher (~40%) than in monkeys (Kaneko and Fujiyama, <xref rid="B88" ref-type="bibr">2002</xref>; Fujiyama et al., <xref rid="B53" ref-type="bibr">2004</xref>; Lacey et al., <xref rid="B104" ref-type="bibr">2005</xref>; Fujiyama et al., <xref rid="B54" ref-type="bibr">2006</xref>; Huerta-Ocampo et al., <xref rid="B80" ref-type="bibr">2013</xref>). It remains unclear whether the large proportion of putative glutamatergic terminals that are not immunopositive for vGluT1 or vGluT2 are simply cortical and thalamic boutons that express undetectable levels of vGluT1 or vGluT2, whether they express other, yet unidentified, vGluT(s) or whether they are non-glutamatergic.</p></sec><sec id="s2-5"><title>Thalamic inputs to direct vs. indirect pathway neurons</title><p>The striatum comprises two main populations of output neurons characterized by their differential dopamine receptors and neuropeptides expression (D1/substance P/dynorphin or D2/enkephalin) (Gerfen, <xref rid="B56" ref-type="bibr">1984</xref>). These so-called “direct” and “indirect pathway” MSNs receive synaptic inputs from the thalamus and the cerebral cortex (Somogyi et al., <xref rid="B172" ref-type="bibr">1981</xref>; Hersch et al., <xref rid="B77" ref-type="bibr">1995</xref>; Sidibe and Smith, <xref rid="B163" ref-type="bibr">1999</xref>; Lanciego et al., <xref rid="B105" ref-type="bibr">2004</xref>; Lei et al., <xref rid="B110" ref-type="bibr">2004</xref>, <xref rid="B109" ref-type="bibr">2013</xref>; Huerta-Ocampo et al., <xref rid="B80" ref-type="bibr">2013</xref>). In rats, the proportion of thalamic (vGluT2-positive) or cortical (vGluT1-positive) terminals in contact with direct or indirect pathway MSNs is very similar when considered as a population (Doig et al., <xref rid="B44" ref-type="bibr">2010</xref>; Lei et al., <xref rid="B109" ref-type="bibr">2013</xref>), but the total number of cortical terminals is higher than the number of thalamic boutons in contact with <italic>individual</italic> MSNs (Huerta-Ocampo et al., <xref rid="B80" ref-type="bibr">2013</xref>). Tract-tracing studies in monkeys suggested that afferents from the CM preferentially innervate direct pathway MSNs in the putamen (Sidibe and Smith, <xref rid="B162" ref-type="bibr">1996</xref>). However, because the CM/Pf (or Pf in rodents) has a unique pattern of synaptic connectivity in the striatum compared with other thalamic nuclei (Figures <xref ref-type="fig" rid="F1">1</xref>, <xref ref-type="fig" rid="F2">2</xref>), and because axonal tracers labeled only a subset of CM terminals in this study, the potentially preferential innervation of direct pathway neurons needs to be further assessed using vGluT2 or other more general marker of the CM/Pf-striatal system.</p><p>The convergence of thalamic and cortical inputs upon single MSNs is consistent with <italic>in vivo</italic> and <italic>in vitro</italic> electrophysiological analyses showing that single direct or indirect pathway neurons respond to both cortical and thalamic stimulation in rodents (Kocsis and Kitai, <xref rid="B95" ref-type="bibr">1977</xref>; Vandermaelen and Kitai, <xref rid="B181" ref-type="bibr">1980</xref>; Ding et al., <xref rid="B43" ref-type="bibr">2008</xref>; Ellender et al., <xref rid="B47" ref-type="bibr">2011</xref>, <xref rid="B46" ref-type="bibr">2013</xref>; Huerta-Ocampo et al., <xref rid="B80" ref-type="bibr">2013</xref>). Recent studies have suggested that thalamic inputs may gate corticostriatal transmission via regulation of striatal cholinergic interneurons, and that this interaction may modulate behavioral switching and attentional set-shifting (Kimura et al., <xref rid="B93" ref-type="bibr">2004</xref>; Ding et al., <xref rid="B42" ref-type="bibr">2010</xref>; Smith et al., <xref rid="B171" ref-type="bibr">2011</xref>; Sciamanna et al., <xref rid="B158" ref-type="bibr">2012</xref>; Bradfield et al., <xref rid="B20" ref-type="bibr">2013a</xref>,<xref rid="B21" ref-type="bibr">b</xref>).</p></sec><sec id="s2-6"><title>Relationships between thalamic or cortical terminals and dopaminergic or histaminergic afferents</title><p>The modulation of excitatory inputs from the cerebral cortex by dopaminergic afferents from the substantia nigra pars compacta is central to our understanding of the functional properties of the basal ganglia. The post-synaptic cortical-induced excitatory responses are modulated by dopamine acting through a wide variety of pre- and/or post-synaptic mechanisms dependent on the type and localization of dopamine receptors and the physiological state of striatal MSNs (Gonon, <xref rid="B59" ref-type="bibr">1997</xref>; Reynolds et al., <xref rid="B147" ref-type="bibr">2001</xref>; Cragg and Rice, <xref rid="B35" ref-type="bibr">2004</xref>; Surmeier et al., <xref rid="B177" ref-type="bibr">2007</xref>; Rice and Cragg, <xref rid="B148" ref-type="bibr">2008</xref>; Ma et al., <xref rid="B112" ref-type="bibr">2012</xref>). Although the regulatory effects of dopamine on thalamic glutamatergic transmission have not been directly assessed, the similarity between the overall pattern of synaptic connectivity of non-CM/Pf thalamic and cortical terminals with MSNs (Moss and Bolam, <xref rid="B129" ref-type="bibr">2008</xref>) suggests that these two pathways may be regulated in the same manner by nigrostriatal dopamine afferents (Figure <xref ref-type="fig" rid="F1">1</xref>). The dopaminergic modulation of corticostriatal transmission relies in part on the synaptic convergence of dopaminergic and cortical synapses on individual spines of striatal MSNs (Freund et al., <xref rid="B52" ref-type="bibr">1984</xref>; Bolam and Smith, <xref rid="B16" ref-type="bibr">1990</xref>; Smith et al., <xref rid="B166" ref-type="bibr">1994</xref>) and/or pre-synaptic dopamine-mediated regulation of glutamate release from neighboring cortical terminals (Surmeier et al., <xref rid="B177" ref-type="bibr">2007</xref>). Our recent quantitative ultrastructural analyses of rat tissue immunolabelled to reveal both dopaminergic axons and cortical (vGluT1-positive) or thalamic (vGluT2-positive) terminals in rats showed that both glutamatergic systems display the same structural relationships with dopaminergic afferents, i.e., all thalamic and cortical glutamatergic terminals are located within 1 µm of a dopaminergic synapse suggesting that synaptically released and spilled over dopamine may modulate most glutamatergic terminals in the rodent striatum (Arbuthnott et al., <xref rid="B9" ref-type="bibr">2000</xref>; Arbuthnott and Wickens, <xref rid="B8" ref-type="bibr">2007</xref>; Moss and Bolam, <xref rid="B129" ref-type="bibr">2008</xref>; Rice and Cragg, <xref rid="B148" ref-type="bibr">2008</xref>; but see Xu et al., <xref rid="B199" ref-type="bibr">2012</xref>). However, it is unclear whether this general concept of interaction between dopaminergic and thalamostriatal afferents also applies to CM/Pf-striatal terminals that form axo-dendritic synapses. In light of our previous tracing studies which showed that axo-dendritic thalamic inputs from CM and dopaminergic terminals do not display significant structural relationships on the dendritic surface of striatal neurons (Smith et al., <xref rid="B166" ref-type="bibr">1994</xref>), it is likely that the interactions between dopaminergic afferents and CM/Pf or non-CM/Pf thalamostriatal synapses differ (Figure <xref ref-type="fig" rid="F1">1</xref>).</p><p>Glutamatergic inputs from the cerebral cortex and thalamus to both direct and indirect pathway MSNs are also modulated pre-synaptically by histamine (Ellender et al., <xref rid="B47" ref-type="bibr">2011</xref>). Histaminergic projections to the striatum that originate in the hypothalamus negatively modulate corticostriatal and thalamostriatal transmission through histamine H3 receptors.</p></sec></sec><sec id="s3"><title>Afferent connections of center median/parafascicular (CM/Pf)</title><p>In addition to the massive GABAergic projections from the GPi and SNr (see above), the CM receives inputs from motor, premotor and somatosensory cortices (Mehler, <xref rid="B121" ref-type="bibr">1966</xref>; Kuypers and Lawrence, <xref rid="B102" ref-type="bibr">1967</xref>; Kunzle, <xref rid="B98" ref-type="bibr">1976</xref>, <xref rid="B99" ref-type="bibr">1978</xref>; Catsman-Berrevoets and Kuypers, <xref rid="B29" ref-type="bibr">1978</xref>; DeVito and Anderson, <xref rid="B41" ref-type="bibr">1982</xref>), while the Pf is the main target of the frontal and supplementary eye fields (Huerta et al., <xref rid="B79" ref-type="bibr">1986</xref>; Leichnetz and Goldberg, <xref rid="B111" ref-type="bibr">1988</xref>) and associative areas of the parietal cortex (Ipekchyan, <xref rid="B85" ref-type="bibr">2011</xref>). The CM/Pf complex also receives significant afferents from various subcortical sources, including the superior colliculus (Grunwerg et al., <xref rid="B62" ref-type="bibr">1992</xref>; Redgrave et al., <xref rid="B144" ref-type="bibr">2010</xref>), the pedunculopontine tegmental nucleus (Pare et al., <xref rid="B134" ref-type="bibr">1988</xref>; Parent et al., <xref rid="B137" ref-type="bibr">1988</xref>; Barroso-Chinea et al., <xref rid="B12" ref-type="bibr">2011</xref>), the cerebellum (Royce et al., <xref rid="B151" ref-type="bibr">1991</xref>; Ichinohe et al., <xref rid="B82" ref-type="bibr">2000</xref>), the raphe nuclei, the locus coeruleus (Lavoie and Parent, <xref rid="B108" ref-type="bibr">1991</xref>; Royce et al., <xref rid="B151" ref-type="bibr">1991</xref>; Vertes et al., <xref rid="B182" ref-type="bibr">2010</xref>), and from the mesencephalic, pontine and medullary reticular formation (Comans and Snow, <xref rid="B30" ref-type="bibr">1981</xref>; Steriade and Glenn, <xref rid="B176" ref-type="bibr">1982</xref>; Hallanger et al., <xref rid="B65" ref-type="bibr">1987</xref>; Cornwall and Phillipson, <xref rid="B33" ref-type="bibr">1988</xref>; Vertes and Martin, <xref rid="B183" ref-type="bibr">1988</xref>; Royce et al., <xref rid="B151" ref-type="bibr">1991</xref>; Newman and Ginsberg, <xref rid="B132" ref-type="bibr">1994</xref>).</p></sec><sec id="s4"><title>Physiology of the thalamostriatal projections</title><sec id="s4-1"><title><italic>In vivo</italic> recording studies</title><p>Experiments to study the role of the projections from the CM/Pf to the striatum date back to the 1970s. These studies described that electrical stimulation of the intralaminar nuclei induces short-latency excitatory post-synaptic potentials (EPSPs) in anesthetized cats and rats (Kocsis and Kitai, <xref rid="B95" ref-type="bibr">1977</xref>; Vandermaelen and Kitai, <xref rid="B181" ref-type="bibr">1980</xref>), confirming the existence of a direct glutamatergic thalamostriatal connection. Later, Wilson and colleagues demonstrated that these responses occurred in striatal MSNs (Wilson et al., <xref rid="B195" ref-type="bibr">1983</xref>) and in cholinergic interneurons (Wilson et al., <xref rid="B196" ref-type="bibr">1990</xref>). In addition to short-latency EPSPs, both types of neurons also showed prolonged inhibitions, or long-latency excitations (Wilson et al., <xref rid="B195" ref-type="bibr">1983</xref>, <xref rid="B196" ref-type="bibr">1990</xref>), indicating that the thalamic stimulation also engaged polysynaptic pathways.</p><p>In more recent studies in awake monkeys, we carried out extracellular recordings in the striatum during electrical stimulation of the CM/Pf complex (Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref>; Figure <xref ref-type="fig" rid="F3">3</xref>). We found that striatal cells did not respond to single-pulse stimulation, but that many neurons showed long-latency (tens of milliseconds) responses to burst stimulation (100 Hz, 1 s) of the CM/Pf. While phasically active neurons (PANs), which likely correspond to striatal MSNs, responded mainly with increases in firing, tonically active striatal neurons (TANs, likely to be cholinergic interneurons) often showed combinations of increases and decreases in firing (Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref>; Figure <xref ref-type="fig" rid="F3">3</xref>). Both types of responses were most likely generated by activation of the intrastriatal circuitry. As mentioned above, anatomical observations support the idea that CM/Pf terminals contact both striatal GABAergic and cholinergic elements in primates and non-primates (Sidibe and Smith, <xref rid="B163" ref-type="bibr">1999</xref>), and that cholinergic interneurons receive GABAergic synaptic inputs from collaterals of direct and indirect pathway MSNs (Gonzales et al., <xref rid="B60" ref-type="bibr">2013</xref>). These collaterals may mediate the decreases in firing after the activation of the presumably excitatory thalamostriatal projections.</p><fig id="F3" position="float"><label>Figure 3</label><caption><p><bold>Electrophysiological responses of striatal neurons to electrical stimulation of CM in awake monkeys.</bold> Electrical stimulation (100 Hz, 100 pulses-shaded area) of CM evokes responses in PANs (putatively MSNs) and TANs (putatively cholinergic interneurons) in awake rhesus monkeys. <bold>(A)</bold> Example of a PAN responding with increased firing to electrical CM stimulation. <bold>(B)</bold> Example of a TAN responding with a brief decrease followed by an increase in firing to CM stimulation. The histograms and rasters are aligned to the start of stimulation trains. <bold>(C)</bold> Summary of responses. The majority of PANs display increases or decreases in firing rate, while most TANs present combinatory (increases and decreases) responses following CM stimulation (see Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref> for more details).</p></caption><graphic xlink:href="fnsys-08-00005-g0003"></graphic></fig><p>The eventual effects of CM stimulation on the striatal circuitry may depend on the experimental conditions chosen. For instance, pharmacological stimulation of the Pf in rats, or electrical stimulation of the CM/Pf in monkeys, was shown to reduce striatal acetylcholine levels, an effect that can be reversed by intrastriatal administration of GABA<sub>A</sub> receptor antagonists (Zackheim and Abercrombie, <xref rid="B201" ref-type="bibr">2005</xref>; Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref>). The reduction in acetylcholine levels could be explained assuming that the thalamic activation drives intrastriatal GABAergic neurons that then secondarily inhibit cholinergic interneurons. However, other studies showed that electrical stimulation of Pf increased the level of acetylcholine in the rat striatum (Consolo et al., <xref rid="B31" ref-type="bibr">1996a</xref>) in an NMDA-receptor dependent manner.</p></sec><sec id="s4-2"><title><italic>In vitro</italic> recordings in brain slices</title><p>A new rat brain slice preparation that partly preserved thalamostriatal axons (Smeal et al., <xref rid="B164" ref-type="bibr">2007</xref>) has enabled studies of the chemical and functional properties of thalamostriatal synapses and the potential relationships between thalamostriatal and corticostriatal systems in normal state (Ding et al., <xref rid="B43" ref-type="bibr">2008</xref>; Smeal et al., <xref rid="B165" ref-type="bibr">2008</xref>). Using this preparation, the ratio of NMDA/non-NMDA glutamatergic receptors was found to be higher at thalamic than cortical synapses (Ding et al., <xref rid="B43" ref-type="bibr">2008</xref>; Smeal et al., <xref rid="B165" ref-type="bibr">2008</xref>), an observation that extends earlier neurochemical studies in adult rats (Baldi et al., <xref rid="B11" ref-type="bibr">1995</xref>; Consolo et al., <xref rid="B31" ref-type="bibr">1996a</xref>,<xref rid="B32" ref-type="bibr">b</xref>). This slice preparation has also lead to additional data suggesting that the thalamostriatal system gates corticostriatal signaling via activation of striatal cholinergic interneurons, and that this functional interaction might be altered in mouse model of dystonia (Ding et al., <xref rid="B43" ref-type="bibr">2008</xref>; Sciamanna et al., <xref rid="B158" ref-type="bibr">2012</xref>). However, it is a limitation of this preparation that thalamostriatal projections from CM/Pf cannot be distinguished from those originating in other parts of the thalamus.</p><p>The introduction of optogenetic methods helped to further characterize the properties of specific thalamostriatal synapses in rats (Ellender et al., <xref rid="B46" ref-type="bibr">2013</xref>). Thus, neurons in the central lateral nucleus (CL) have bushy, frequently branching, dendrites and, under anesthesia, fire action potentials in the form of low-threshold Ca<sup>2+</sup> spike bursts, while Pf neurons have long, infrequently branching dendrites and give rise to action potentials that are only rarely in the form of low-threshold bursts (Lacey et al., <xref rid="B103" ref-type="bibr">2007</xref>; Figure <xref ref-type="fig" rid="F2">2</xref>). In the striatum, thalamostriatal terminals from the CL terminate almost exclusively on dendritic spines, while Pf boutons target predominantly dendritic shafts (Figure <xref ref-type="fig" rid="F2">2</xref>). <italic>In vitro</italic> optogenetic activation of the different pathways combined with whole-cell, patch-clamp recordings of direct or indirect pathway MSNs in adult mice (Ellender et al., <xref rid="B46" ref-type="bibr">2013</xref>) revealed that stimulation of CL synapses leads to large amplitude, predominantly AMPA-receptor mediated, excitatory responses that display short-term facilitation. In contrast, stimulation of Pf synapses gives rise to small amplitude responses that display short-term depression and are largely mediated by post-synaptic NMDA receptors (Ellender et al., <xref rid="B46" ref-type="bibr">2013</xref>; Figure <xref ref-type="fig" rid="F4">4</xref>). The high frequency Ca<sup>2+</sup> spike bursts in CL neurons together with the synaptic properties of CL thalamostriatal synapses suggests that thalamic inputs from CL are well suited to driving MSNs to depolarization and hence firing (Ellender et al., <xref rid="B46" ref-type="bibr">2013</xref>). In contrast, the firing characteristics and properties of Pf neurons and their thalamostriatal synapses suggest that these are better suited to exert modulatory effects on striatal MSNs, which could be in the form of facilitating Ca<sup>2+</sup>-dependent processes. Furthermore, pairing Pf pre-synaptic stimulation with action potentials in MSNs leads to NMDA receptor- and Ca<sup>2+</sup>-dependent long-term depression at these synapses (Ellender et al., <xref rid="B46" ref-type="bibr">2013</xref>; Figure <xref ref-type="fig" rid="F4">4</xref>).</p><fig id="F4" position="float"><label>Figure 4</label><caption><p><bold>Electrophysiological responses of striatal MSNs to optogenetic activation of thalamostriatal terminals from CL or Pf in mice. (A)</bold> Channelrhodopsin-2 (ChR2) was delivered to either the CL or Pf thalamic nucleus using a stereotaxic injection of adeno-associated virus containing the double-floxed sequence for ChR2-YFP in CAMKII-cre mice. This approach enabled expression of ChR2 in the excitatory thalamic neurons of either the CL or Pf nucleus including in their axonal arbor. Thalamic axons expressing ChR2-YFP were readily visible in acute striatal slices and this method allowed for activation of only those synapses originating from neurons from the injected thalamic nucleus by illumination of these slices with blue (473 nm) laser or LED light. <bold>(B)</bold> Whole-cell patch-clamp recordings of striatal MSNs showed that activation of CL synapses led to consistently larger post-synaptic responses than activation of Pf synapses. <bold>(C)</bold> Detailed investigation of the glutamate receptor-mediated currents revealed the CL synapses exhibit predominantly AMPA receptor-mediated currents in response to light activation and the Pf synapses exhibit predominantly NMDA receptor-mediated currents. <bold>(D)</bold> The short term plastic properties of these synapses were investigated by repetitive activation of the synapses in close succession. This revealed that inputs from CL exhibit short term facilitation, in which the response to the second activation has a larger amplitude than the response to the first activation, whereas inputs from Pf exhibit short term depression. <bold>(E)</bold> The long term plastic properties of these synapses were investigated using a spike timing-dependent plasticity protocol, consisting of the pairing of optical activation of a pre-synaptic thalamic input with a post-synaptic action potential in a MSN. This protocol induced a clear long term depression of synaptic efficacy at Pf synapses, but no plasticity was observed at CL synapses. The same observation was made using either a pre-post or post-pre pairing, with only the pre-post pairing shown for clarity (see Ellender et al., <xref rid="B46" ref-type="bibr">2013</xref> for more details).</p></caption><graphic xlink:href="fnsys-08-00005-g0004"></graphic></fig></sec></sec><sec id="s5"><title>The role of the center median/parafascicular (CM/Pf) thalamostriatal system in cognition</title><p>The CM/Pf-striatal system is now thought to be critical in mediating basal ganglia responses to attention-related stimuli, and may be engaged in behavioral switching and reinforcement functions (Kimura et al., <xref rid="B93" ref-type="bibr">2004</xref>; Minamimoto et al., <xref rid="B126" ref-type="bibr">2009</xref>; Smith et al., <xref rid="B171" ref-type="bibr">2011</xref>; Bradfield et al., <xref rid="B20" ref-type="bibr">2013a</xref>).</p><sec id="s5-1"><title>Responses of center median/parafascicular (CM/Pf) neurons in attention-related tasks</title><p>Because the intralaminar nuclei receive massive ascending projections from the reticular formation and various brainstem regions (see above), and have long been known as the source(s) of widely distributed “nonspecific” thalamocortical projections, these thalamic nuclei are considered part of the ascending “reticular activating system” that regulates arousal and attention (as reviewed in Van der Werf et al., <xref rid="B180" ref-type="bibr">2002</xref>). In line with this concept, functional imaging studies in humans demonstrated a significant increase of activity in CM/Pf during processing of attention-related stimuli (Kinomura et al., <xref rid="B94" ref-type="bibr">1996</xref>; Hulme et al., <xref rid="B81" ref-type="bibr">2010</xref>; Metzger et al., <xref rid="B124" ref-type="bibr">2010</xref>). More recent observations in primates showed that CM and Pf neurons respond to behaviorally salient visual, auditory and somatosensory stimuli (Matsumoto et al., <xref rid="B116" ref-type="bibr">2001</xref>; Minamimoto and Kimura, <xref rid="B127" ref-type="bibr">2002</xref>; Minamimoto et al., <xref rid="B125" ref-type="bibr">2005</xref>; Figure <xref ref-type="fig" rid="F5">5</xref>). In these studies, the response latencies of Pf neurons were much shorter than those of CM neurons (Figure <xref ref-type="fig" rid="F5">5</xref>). Compatible with the view that responses of CM/Pf neurons to external events are related to attention, the initially vigorous responses fade quickly upon repeated stimulus presentation if stimuli were not followed by reward, and, thus, lose their salience (Matsumoto et al., <xref rid="B116" ref-type="bibr">2001</xref>; Minamimoto and Kimura, <xref rid="B127" ref-type="bibr">2002</xref>; Kimura et al., <xref rid="B93" ref-type="bibr">2004</xref>; Minamimoto et al., <xref rid="B125" ref-type="bibr">2005</xref>). Acute pharmacological inactivation of Pf in monkeys disrupts attention processing more efficiently than CM inactivation (Minamimoto and Kimura, <xref rid="B127" ref-type="bibr">2002</xref>). The functional responses of CM/Pf neurons to attention-related stimuli thus suggest a role of the CM/Pf-striatal system in cognition, most particularly related to attention shifting, behavior switching and reinforcement processes (Matsumoto et al., <xref rid="B116" ref-type="bibr">2001</xref>; Minamimoto and Kimura, <xref rid="B127" ref-type="bibr">2002</xref>; Kimura et al., <xref rid="B93" ref-type="bibr">2004</xref>; Minamimoto et al., <xref rid="B125" ref-type="bibr">2005</xref>; Smith et al., <xref rid="B171" ref-type="bibr">2011</xref>; Bradfield et al., <xref rid="B20" ref-type="bibr">2013a</xref>,<xref rid="B21" ref-type="bibr">b</xref>). There is also evidence that sensory-responsive CM neurons may be involved in mechanisms needed for decision-making and biasing actions (Minamimoto et al., <xref rid="B125" ref-type="bibr">2005</xref>).</p><fig id="F5" position="float"><label>Figure 5</label><caption><p><bold>Sensory responses of two types of CM/Pf neurons, and a striatal TAN recorded during the presentation of a stimulus with or without reward (WR vs. WOR).</bold> The spike rasters and histograms are aligned to the time of presentation of the stimulus. <bold>(A<sub>1</sub>)</bold> Representative activity of a CM neuron with long-latency facilitation (LLF) following stimulus presentation. <bold>(A<sub>2</sub>)</bold> Activity of a Pf neuron showing short-latency facilitation (SLF) after stimulus. <bold>(A<sub>3</sub>)</bold> Activity of a TAN. Note that thalamic responses occur in both WR and WOR tasks, whereas TAN responses occur only in the WR task. <bold>(B)</bold> Localization of LLF and SLF neurons in the monkey CM/Pf complex. Note the complete segregation of these two populations of neurons in CM or Pf. <bold>(C)</bold> Application of the GABA<sub>A</sub> receptor agonist muscimol in CM/Pf alters the pattern of responses of striatal TANs to the presentation of reward-related sensory stimuli in awake monkeys, The rasters and histograms on the right demonstrate that the pauses in the TAN responses are abolished after application of muscimol in CM/Pf (reproduced with permission from Matsumoto et al., <xref rid="B116" ref-type="bibr">2001</xref>).</p></caption><graphic xlink:href="fnsys-08-00005-g0005"></graphic></fig><p>Additional evidence for a “cognitive” role of the CM/Pf projections to the striatum comes from studies in mice in which selective immunotoxin lesions or pharmacological inactivation of the Pf-striatal projection, impair performance in a discrimination learning task (Brown et al., <xref rid="B23" ref-type="bibr">2010</xref>; Kato et al., <xref rid="B89" ref-type="bibr">2011</xref>). Furthermore, recent evidence indicates the Pf projection to the posterior dorsomedial striatum is involved in regulating the interaction between new and previously learned stimuli (Bradfield et al., <xref rid="B20" ref-type="bibr">2013a</xref>,<xref rid="B21" ref-type="bibr">b</xref>). It is noteworthy that neither lesion nor pharmacological inactivation of CM/Pf in monkeys or rodents lead to motor impairments (Matsumoto et al., <xref rid="B116" ref-type="bibr">2001</xref>; Minamimoto and Kimura, <xref rid="B127" ref-type="bibr">2002</xref>; Brown et al., <xref rid="B23" ref-type="bibr">2010</xref>; Kato et al., <xref rid="B89" ref-type="bibr">2011</xref>).</p></sec><sec id="s5-2"><title>Center median/parafascicular (CM/Pf)-striatal system regulation of striatal cholinergic interneurons</title><p>Reward-associated events evoke pause responses in striatal TANs (which are likely to be cholinergic interneurons) (Goldberg and Reynolds, <xref rid="B58" ref-type="bibr">2011</xref>). These responses are regulated in part by the CM/Pf-striatal system, because they are almost completely abolished by chemical inactivation of the CM/Pf complex in monkeys (Matsumoto et al., <xref rid="B116" ref-type="bibr">2001</xref>; Figure <xref ref-type="fig" rid="F5">5</xref>). Furthermore, the removal of Pf inputs to cholinergic interneurons reduces the firing rate of these neurons and produces an enduring deficit in goal-directed learning (Bradfield et al., <xref rid="B20" ref-type="bibr">2013a</xref>). These observations are consistent with the fact that cholinergic interneurons receive synaptic inputs from CM/Pf (Lapper and Bolam, <xref rid="B107" ref-type="bibr">1992</xref>; Sidibe and Smith, <xref rid="B163" ref-type="bibr">1999</xref>), that CM stimulation strongly affects TAN activity patterns (Wilson et al., <xref rid="B196" ref-type="bibr">1990</xref>; Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref>) and that CM/Pf alterations affect striatal acetylcholine release (Consolo et al., <xref rid="B31" ref-type="bibr">1996a</xref>,<xref rid="B32" ref-type="bibr">b</xref>; Zackheim and Abercrombie, <xref rid="B201" ref-type="bibr">2005</xref>; Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref>). As mentioned above, several mechanisms have been proposed to explain how activation of the glutamatergic CM/Pf-striatal projection evokes inhibitions or pauses in TAN firing, including the involvement of intercalated GABAergic and dopaminergic elements, as well as intrinsic properties of cholinergic interneurons (Ding et al., <xref rid="B42" ref-type="bibr">2010</xref>; Goldberg and Reynolds, <xref rid="B58" ref-type="bibr">2011</xref>; Sciamanna et al., <xref rid="B158" ref-type="bibr">2012</xref>; Threlfell et al., <xref rid="B179" ref-type="bibr">2012</xref>).</p></sec></sec><sec id="s6"><title>Degeneration of the thalamostriatal system in Parkinson’s disease (PD)</title><p>Postmortem studies have shown that 30–40% of CM/Pf neurons are lost in PD patients with mild motor deficits, and that the extent of CM/Pf degeneration does not further progress with the severity of the Parkinsonian motor signs (Xuereb et al., <xref rid="B200" ref-type="bibr">1991</xref>; Heinsen et al., <xref rid="B72" ref-type="bibr">1996</xref>; Henderson et al., <xref rid="B73" ref-type="bibr">2000a</xref>,<xref rid="B74" ref-type="bibr">b</xref>,<xref rid="B75" ref-type="bibr">2005</xref>; Brooks and Halliday, <xref rid="B22" ref-type="bibr">2009</xref>; Halliday, <xref rid="B66" ref-type="bibr">2009</xref>). We have recently found a similarly robust loss of CM/Pf neurons in monkeys that were chronically treated with low doses of the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP), even in motor asymptomatic animals with minimal nigrostriatal dopaminergic denervation (Villalba et al., <xref rid="B188" ref-type="bibr">2014</xref>; Figure <xref ref-type="fig" rid="F6">6</xref>). In PD patients and MPTP-treated monkeys, this thalamic degeneration predominantly affects CM/Pf (Henderson et al., <xref rid="B73" ref-type="bibr">2000a</xref>,<xref rid="B74" ref-type="bibr">b</xref>; Villalba et al., <xref rid="B188" ref-type="bibr">2014</xref>), although significant neuronal loss was also reported in the parataenial, cucullar and central lateral nuclei of PD patients (Halliday, <xref rid="B66" ref-type="bibr">2009</xref>). In the brain of PD patients, α-synuclein deposition was found in the latter three nuclei, but not as much in CM/Pf (Brooks and Halliday, <xref rid="B22" ref-type="bibr">2009</xref>). Parvalbumin-negative neurons are particularly affected in CM (Halliday, <xref rid="B66" ref-type="bibr">2009</xref>). It is noteworthy that robust CM/Pf neuronal loss is not only found in PD, but has also been found in other neurodegenerative diseases, including progressive supranuclear palsy and Huntington’s disease (Heinsen et al., <xref rid="B72" ref-type="bibr">1996</xref>; Henderson et al., <xref rid="B73" ref-type="bibr">2000a</xref>,<xref rid="B74" ref-type="bibr">b</xref>). The cellular properties of CM/Pf neurons needs to be studied in more detail to determine the potential factors that make them more sensitive to degeneration than other thalamic cells in these diseases (see also below).</p><fig id="F6" position="float"><label>Figure 6</label><caption><p><bold>Loss of CM/Pf neurons in MPTP-treated monkeys. (A–G)</bold> Light micrographs of neurons in CM or Pf of control monkeys <bold>(A, D)</bold>, MPTP-treated motor symptomatic <bold>(B, E)</bold> and MPTP-treated motor asymptomatic <bold>(C, F)</bold> animals. The motor asymptomatic animals had ~40% striatal dopamine loss and did not display any Parkinsonian motor symptoms, while the motor symptomatic monkeys had more than 80% striatal dopamine loss and displayed moderate to severe Parkinsonism. Note the significant reduction in neuronal density in CM and Pf of both symptomatic and asymptomatic MPTP-treated monkeys. <bold>(G)</bold> Stereological cell counts demonstrate a significant loss of neurons in both CM and Pf of the two groups of MPTP-treated monkeys compared with controls.</p></caption><graphic xlink:href="fnsys-08-00005-g0006"></graphic></fig><p>In rodent and primate models of PD, striatal dopamine loss is associated with a loss of glutamatergic synapses (Ingham et al., <xref rid="B84" ref-type="bibr">1998</xref>; Villalba et al., <xref rid="B189" ref-type="bibr">2013</xref>), which is consistent with a loss of spines on striatal MSNs in PD postmortem material (see below). Stereological estimates of the number of glutamatergic synapses formed by vGluT1- (marker of cortical terminals) or vGluT2- (marker of thalamic terminals) containing terminals in the putamen of MPTP-treated monkeys showed that the number of vGluT2-positive terminals, but not that of vGluT1-containing boutons, is substantially reduced in Parkinsonian animals (Villalba et al., <xref rid="B189" ref-type="bibr">2013</xref>). This suggests that the loss of thalamic glutamatergic inputs to the striatum outweighs the loss of cortical terminals in MPTP-treated monkeys (Villalba et al., <xref rid="B189" ref-type="bibr">2013</xref>). Because CM/Pf inputs to striatal MSNs predominantly terminate on dendritic shafts (see above), these findings are in line with our previous studies which had demonstrated that MPTP treatment reduces the relative prevalence of vGluT2-positive axo-dendritic synapses in the putamen more strongly than that of axo-spinous synapses (Raju et al., <xref rid="B141" ref-type="bibr">2008</xref>). Together, these results support the hypothesis that the loss of CM/Pf inputs to the striatum prominently contributes to the glutamatergic deafferentation of MSNs in PD. It is not yet clear whether the loss of striatal inputs from CM/Pf also affects the glutamatergic innervation of cholinergic interneurons.</p><p>The loss of glutamatergic afferents is reflected in a profound loss of dendritic spines of striatal MSNs in PD patients (Stephens et al., <xref rid="B174" ref-type="bibr">2005</xref>; Zaja-Milatovic et al., <xref rid="B202" ref-type="bibr">2005</xref>), rodent models of PD (Ingham et al., <xref rid="B83" ref-type="bibr">1989</xref>; Day et al., <xref rid="B37" ref-type="bibr">2006</xref>; Kusnoor et al., <xref rid="B100" ref-type="bibr">2009</xref>) and in MPTP-treated monkeys (Raju et al., <xref rid="B141" ref-type="bibr">2008</xref>; Smith et al., <xref rid="B169" ref-type="bibr">2009</xref>; Villalba et al., <xref rid="B184" ref-type="bibr">2009</xref>, <xref rid="B189" ref-type="bibr">2013</xref>; Villalba and Smith, <xref rid="B185" ref-type="bibr">2010</xref>, <xref rid="B186" ref-type="bibr">2011</xref>, <xref rid="B187" ref-type="bibr">2013</xref>). In the latter studies, a 40–50% spine loss was found in the sensorimotor striatum, similar to findings in PD patients (Zaja-Milatovic et al., <xref rid="B202" ref-type="bibr">2005</xref>; Villalba et al., <xref rid="B184" ref-type="bibr">2009</xref>). The link between the aforementioned striatal glutamatergic deafferentation and spine loss remains uncertain. For instance, it remains unclear whether the CM/Pf degeneration and the resulting loss of glutamatergic inputs to the striatum contribute to the changes in the number and morphology of dendritic spines in PD. As a further complication, the use of dopaminergic drugs can also affect spine growth and morphology. Thus, a recent study showed aberrant restoration of axo-spinous synapses that affect corticostriatal, but not thalamostriatal synapses, in unilaterally 6-hydroxydopamine (OHDA)-lesioned rats that developed L-3,4-didroxyphenylalanine (L-DOPA)-induced dyskinesias (Zhang et al., <xref rid="B203" ref-type="bibr">2013</xref>), suggesting a differential impairment of the two glutamatergic systems in dyskinesia. Details about the extent of Pf neuronal loss in these animals are needed to translate these findings to human PD patients with L-DOPA-induced dyskinesia.</p><sec id="s6-1"><title>Potential reasons for center median/parafascicular (CM/Pf) neuron loss in PD</title><p>Although it remains unclear why CM/Pf neurons are particularly sensitive to neurodegeneration in PD and other disorders (Halliday et al., <xref rid="B67" ref-type="bibr">2005</xref>; Halliday, <xref rid="B66" ref-type="bibr">2009</xref>), their chemical phenotype and sensitivity to chronic MPTP administration in non-human primates (Villalba et al., <xref rid="B188" ref-type="bibr">2014</xref>) may provide clues. The CM/Pf nuclei do not carry a specifically high level of α-synuclein deposits in PD patients (Brooks and Halliday, <xref rid="B22" ref-type="bibr">2009</xref>), so that their vulnerability in PD cannot be explained by the burden of α-synuclein aggregation.</p><p>In rodents, striatal terminals from the Pf express immunoreactivity for the protein cerebellin 1, a neurochemical feature that appears to be specific for the CM/Pf-striatal system, and may also regulate the morphology of striatal spines (Kusnoor et al., <xref rid="B101" ref-type="bibr">2010</xref>). It remains to be established whether this unique molecular characteristic amongst thalamic neurons contributes to their susceptibility. It is also possible that the absence of calcium binding proteins expression in CM/Pf neurons determines their differential vulnerability. In humans, postmortem studies have shown that subpopulations of parvalbumin-containing neurons are mainly affected in Pf, while non-parvalbumin/non-calbindin neurons are more specifically targeted in CM (Henderson et al., <xref rid="B73" ref-type="bibr">2000a</xref>). In MPTP-treated animals, the degeneration of CM/Pf could instead be due to direct toxic effects of the MPTP metabolite, 1-methyl-4-phenylpyridinium (MPP+), on the thalamus, independent of its effects on the nigrostriatal system (Villalba et al., <xref rid="B188" ref-type="bibr">2014</xref>). Consistent with this possibility, injections of MPP+ into the rodent striatum resulted in a major neuronal loss in Pf, without significant effects on cortical neurons (Ghorayeb et al., <xref rid="B57" ref-type="bibr">2002</xref>).</p></sec></sec><sec id="s7"><title>The center median/parafascicular (CM/Pf) as a target of neurosurgical interventions in brain disorders</title><p>Although the physiological properties of the caudal intralaminar nuclei and their projections remain poorly characterized, these nuclei have been used as targets for surgical interventions, aimed at treating pain, seizures, impairments of consciousness, or movement disorders. We will focus our discussion on the use of neurosurgical procedures as treatment of movement disorders, because this use is most easily linked to the interactions between CM/Pf and the basal ganglia. These procedures have been used specifically in patients with disabling TS, or with PD. The mechanisms of action of CM/Pf interventions in these diseases, and the specifics of the optimal surgical approach and DBS characteristics remain matters of speculation. Furthermore, inclusion and exclusion criteria for trials of these interventions are only beginning to emerge for TS patients, while no formal criteria have yet been developed for trials in patients with PD.</p><sec id="s7-1"><title>Ablative surgeries of center median/parafascicular (CM/Pf)</title><p>Since the 1960s, unilateral or bilateral lesions of the intralaminar and medial thalamic nuclei, as well as the nucleus ventro-oralis internus (Voi) have been empirically used to treat patients with TS (see below) (Hassler and Dieckmann, <xref rid="B70" ref-type="bibr">1970</xref>, <xref rid="B71" ref-type="bibr">1973</xref>; de Divitiis et al., <xref rid="B38" ref-type="bibr">1977</xref>; Hassler, <xref rid="B69" ref-type="bibr">1982</xref>). These studies have reported impressive reductions in tic frequency in these patients, along with a lesser reversal of compulsive symptoms. The effects of CM/Pf lesions in other movement disorders (such as Parkinsonism) have not been extensively characterized. However, in rodents, Pf lesions were shown to prevent the neurochemical changes produced by dopamine denervation in different basal ganglia nuclei (Kerkerian-Le Goff et al., <xref rid="B91" ref-type="bibr">2009</xref>). Similar experiments in MPTP-treated primates have not resulted in significant anti-parkinsonian effects (Lanciego et al., <xref rid="B106" ref-type="bibr">2008</xref>).</p></sec><sec id="s7-2"><title>CM/Pf deep brain stimulation and TS</title><p>TS is a neuropsychiatric disorder of childhood onset. Patients develop rapid, stereotyped movements (tics) which typically peak in preadolescence and decline in the later teenage years. Many TS patients also suffer from psychiatric comorbidities, such as obsessive compulsive disorder, attention-deficit hyperactivity disorder, or depression. Most patients are successfully (albeit partially) treated with neuroleptics and other drugs or with behavioral therapy. However, a few patients continue to experience severe tics in adulthood. These patients are candidates for neurosurgical procedures. Although still under considerable debate, TS may be the result of abnormal GABAergic or dopaminergic transmission in the basal ganglia (see, e.g., Buse et al., <xref rid="B24" ref-type="bibr">2013</xref>; Worbe et al., <xref rid="B197" ref-type="bibr">2013</xref>), involving both motor and limbic basal ganglia-thalamocortical circuitry.</p><p>Although there is little evidence linking the pathology or functional disturbances of CM/Pf to TS, this nuclear complex has been a major focus of surgical treatment of this condition, mostly because of the early empirical evidence with ablative treatments (see above). Early investigations of the use of stimulation of CM/Pf in movement disorders were carried out in patients that were enrolled in pain treatment studies, but also suffered from movement disorders (Andy, <xref rid="B7" ref-type="bibr">1980</xref>; Krauss et al., <xref rid="B97" ref-type="bibr">2002</xref>). Significant symptomatic improvements of motor dysfunctions were reported in these studies, but the stimulation parameters were not communicated. Since then, impressive reductions in tic frequency and severity, perhaps with greater effectiveness against motor than vocal tics, have been reported, although the number of TS patients treated with CM/Pf DBS remains small (Visser-Vandewalle et al., <xref rid="B192" ref-type="bibr">2003</xref>, <xref rid="B193" ref-type="bibr">2004</xref>, <xref rid="B190" ref-type="bibr">2006</xref>; Temel and Visser-Vandewalle, <xref rid="B178" ref-type="bibr">2004</xref>; Houeto et al., <xref rid="B78" ref-type="bibr">2005</xref>; Ackermans et al., <xref rid="B3" ref-type="bibr">2006</xref>, <xref rid="B4" ref-type="bibr">2008</xref>, <xref rid="B1" ref-type="bibr">2010</xref>, <xref rid="B2" ref-type="bibr">2011</xref>; Bajwa et al., <xref rid="B10" ref-type="bibr">2007</xref>; Maciunas et al., <xref rid="B114" ref-type="bibr">2007</xref>; Servello et al., <xref rid="B159" ref-type="bibr">2008</xref>, <xref rid="B160" ref-type="bibr">2010</xref>; Shields et al., <xref rid="B161" ref-type="bibr">2008</xref>; Porta et al., <xref rid="B140" ref-type="bibr">2009</xref>; Hariz and Robertson, <xref rid="B68" ref-type="bibr">2010</xref>; Sassi et al., <xref rid="B156" ref-type="bibr">2011</xref>; Maling et al., <xref rid="B115" ref-type="bibr">2012</xref>; Savica et al., <xref rid="B157" ref-type="bibr">2012</xref>; Visser-Vandewalle and Kuhn, <xref rid="B191" ref-type="bibr">2013</xref>). The time course of tic improvement varies between individuals, ranging from immediate effects (Visser-Vandewalle et al., <xref rid="B192" ref-type="bibr">2003</xref>; Maciunas et al., <xref rid="B114" ref-type="bibr">2007</xref>) to a more protracted time course (Maciunas et al., <xref rid="B114" ref-type="bibr">2007</xref>; Servello et al., <xref rid="B159" ref-type="bibr">2008</xref>). In addition to the motor symptoms of the disease, CM/Pf DBS also effectively alleviated some of the psychiatric components of TS, including obsessive-compulsive behaviors and anxiety (Houeto et al., <xref rid="B78" ref-type="bibr">2005</xref>; Mink, <xref rid="B128" ref-type="bibr">2006</xref>; Visser-Vandewalle et al., <xref rid="B190" ref-type="bibr">2006</xref>; Neuner et al., <xref rid="B131" ref-type="bibr">2009</xref>; Krack et al., <xref rid="B96" ref-type="bibr">2010</xref>; Sassi et al., <xref rid="B156" ref-type="bibr">2011</xref>). The mechanisms of action of CM/Pf stimulation on TS signs and symptoms remain unclear, but the anatomy and potential role of the thalamostriatal system from CM/Pf in cognition, as well as functional studies indicating the key role of CM/Pf in regulating striatal cholinergic interneurons activity (see above) in animals, suggest that CM/Pf stimulation may mediate its effects through complex regulation of striatal microcircuits that influence both motor and non-motor basal ganglia-thalamocortical and thalamostriatal networks (Nanda et al., <xref rid="B130" ref-type="bibr">2009</xref>; Kim et al., <xref rid="B92" ref-type="bibr">2013</xref>).</p></sec><sec id="s7-3"><title>Center median/parafascicular (CM/Pf) DBS and Parkinson’s disease (PD)</title><p>CM/Pf DBS was found to provide significant anti-parkinsonian benefits in 6-OHDA-treated rats (Jouve et al., <xref rid="B87" ref-type="bibr">2010</xref>). CM/Pf DBS has also been used in a few PD patients. These studies have suggested that CM/Pf DBS may have anti-dyskinetic effects and reduce freezing of gait, a symptom that is not satisfactorily treated with either medications or conventional DBS approaches directed at subthalamic and pallidal targets (Caparros-Lefebvre et al., <xref rid="B27" ref-type="bibr">1999</xref>; Mazzone et al., <xref rid="B117" ref-type="bibr">2006</xref>). More recent studies have suggested that CM/Pf DBS may also reduce Parkinsonian tremor (Peppe et al., <xref rid="B139" ref-type="bibr">2008</xref>; Stefani et al., <xref rid="B173" ref-type="bibr">2009</xref>).</p></sec></sec><sec id="s8"><title>Concluding remarks and future studies</title><p>Despite significant progress in our understanding of the anatomy, physiology and pathophysiology of the thalamostriatal systems, many unresolved issues remain. The cloning of vGluT1 and vGluT2 has had a significant impact in our understanding of the anatomical and synaptic organization of the thalamostriatal systems, allowing us to further appreciate that the thalamus is a massive source of extrinsic glutamatergic inputs to the striatum that originates either in the CM/Pf nuclear complex, or in the numerous non-CM/Pf thalamic nuclei. Future studies aimed at understanding the physiological role of these multiple thalamostriatal circuits, and their functional interactions with the corticostriatal and nigrostriatal systems, are warranted to decipher the mechanisms by which these extrinsic afferents regulate basal ganglia functions.</p><p>Because of the complex relationships between the cerebral cortex, thalamus and striatum, the use of traditional stimulation or lesion methods has had a limited impact in our understanding of the physiology and synaptic properties of thalamostriatal connections. However, as presented in this review, optogenetic approaches help overcome some of these technical challenges, setting the stage for a rigorous and detailed characterization of the physiology and pathophysiology of the CM/Pf vs. non-CM/Pf-striatal systems in normal and diseased states.</p><p>The major breakthroughs that were recently made in characterizing some aspects of the role of the CM/Pf-striatal system in regulating the physiological responses of striatal cholinergic interneurons to attention-related salient sensory stimuli provide a deeper understanding of the mechanisms involved by which the basal ganglia regulate activities such as behavioral switching, attentional set-shifting and reinforcement. Because the CM/Pf-striatal system undergoes massive degeneration in PD, future studies aimed at assessing the effects of this degeneration upon attention and other basal ganglia-related cognitive functions are needed. A better understanding of the respective role played by the thalamostriatal vs. the nigrostriatal dopamine systems in the regulation of cholinergic interneuron activity is another area of great interest for future studies.</p><p>In light of neuropathology studies of the thalamus in human patients with PD (Halliday, <xref rid="B66" ref-type="bibr">2009</xref>), combined with studies in MPTP-treated non-human primates, it appears that CM/Pf neurons are particularly sensitive to degeneration in PD, neurodegenerative diseases, and neurotoxic insults. Thus, future studies aimed at elucidating the chemical, physiological and pharmacological properties of CM/Pf neurons vs. other thalamic cells are essential to determine the basis for the selective vulnerability of CM/Pf neurons in brain disorders.</p><p>Finally, another area of great interest is the use of DBS of CM/Pf in movement disorders, most particularly in TS. We need to understand better how stimulation of the thalamostriatal system from CM/Pf alleviates tics and psychiatric symptoms of this disease. Furthermore, rigorous blinded trials in a large number of patients still need to be done before this treatment can be recommended for patients with TS.</p></sec><sec><title>Conflict of interest statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Ackermans</surname><given-names>L.</given-names></name><name><surname>Duits</surname><given-names>A.</given-names></name><name><surname>Temel</surname><given-names>Y.</given-names></name><name><surname>Winogrodzka</surname><given-names>A.</given-names></name><name><surname>Peeters</surname><given-names>F.</given-names></name><name><surname>Beuls</surname><given-names>E. 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