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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Dopamine imbalance in Huntington's disease: a mechanism for the lack of behavioral flexibility</title><author><name sortKey="Chen, Jane Y" sort="Chen, Jane Y" uniqKey="Chen J" first="Jane Y." last="Chen">Jane Y. Chen</name></author><author><name sortKey="Wang, Elizabeth A" sort="Wang, Elizabeth A" uniqKey="Wang E" first="Elizabeth A." last="Wang">Elizabeth A. Wang</name></author><author><name sortKey="Cepeda, Carlos" sort="Cepeda, Carlos" uniqKey="Cepeda C" first="Carlos" last="Cepeda">Carlos Cepeda</name></author><author><name sortKey="Levine, Michael S" sort="Levine, Michael S" uniqKey="Levine M" first="Michael S." last="Levine">Michael S. Levine</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23847463</idno><idno type="pmc">3701870</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3701870</idno><idno type="RBID">PMC:3701870</idno><idno type="doi">10.3389/fnins.2013.00114</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">000330</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000330</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Dopamine imbalance in Huntington's disease: a mechanism for the lack of behavioral flexibility</title><author><name sortKey="Chen, Jane Y" sort="Chen, Jane Y" uniqKey="Chen J" first="Jane Y." last="Chen">Jane Y. Chen</name></author><author><name sortKey="Wang, Elizabeth A" sort="Wang, Elizabeth A" uniqKey="Wang E" first="Elizabeth A." last="Wang">Elizabeth A. Wang</name></author><author><name sortKey="Cepeda, Carlos" sort="Cepeda, Carlos" uniqKey="Cepeda C" first="Carlos" last="Cepeda">Carlos Cepeda</name></author><author><name sortKey="Levine, Michael S" sort="Levine, Michael S" uniqKey="Levine M" first="Michael S." last="Levine">Michael S. Levine</name></author></analytic><series><title level="j">Frontiers in Neuroscience</title><idno type="ISSN">1662-4548</idno><idno type="eISSN">1662-453X</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Dopamine (DA) plays an essential role in the control of coordinated movements. Alterations in DA balance in the striatum lead to pathological conditions such as Parkinson's and Huntington's diseases (HD). HD is a progressive, invariably fatal neurodegenerative disease caused by a genetic mutation producing an expansion of glutamine repeats and is characterized by abnormal dance-like movements (chorea). The principal pathology is the loss of striatal and cortical projection neurons. Changes in brain DA content and receptor number contribute to abnormal movements and cognitive deficits in HD. In particular, during the early hyperkinetic stage of HD, DA levels are increased whereas expression of DA receptors is reduced. In contrast, in the late akinetic stage, DA levels are significantly decreased and resemble those of a Parkinsonian state. Time-dependent changes in DA transmission parallel biphasic changes in glutamate synaptic transmission and may enhance alterations in glutamate receptor-mediated synaptic activity. In this review, we focus on neuronal electrophysiological mechanisms that may lead to some of the motor and cognitive symptoms of HD and how they relate to dysfunction in DA neurotransmission. Based on clinical and experimental findings, we propose that some of the behavioral alterations in HD, including reduced behavioral flexibility, may be caused by altered DA modulatory function. Thus, restoring DA balance alone or in conjunction with glutamate receptor antagonists could be a viable therapeutic approach.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Afifi, A K" uniqKey="Afifi A">A. K. Afifi</name></author><author><name sortKey="Bahuth, N B" uniqKey="Bahuth N">N. B. Bahuth</name></author><author><name sortKey="Kaelber, W W" uniqKey="Kaelber W">W. W. Kaelber</name></author><author><name sortKey="Mikhael, E" uniqKey="Mikhael E">E. Mikhael</name></author><author><name sortKey="Nassar, S" uniqKey="Nassar S">S. 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Wilson</name></author><author><name sortKey="Dani, J A" uniqKey="Dani J">J. A. Dani</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Neurosci</journal-id><journal-id journal-id-type="iso-abbrev">Front Neurosci</journal-id><journal-id journal-id-type="publisher-id">Front. Neurosci.</journal-id><journal-title-group><journal-title>Frontiers in Neuroscience</journal-title></journal-title-group><issn pub-type="ppub">1662-4548</issn><issn pub-type="epub">1662-453X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23847463</article-id><article-id pub-id-type="pmc">3701870</article-id><article-id pub-id-type="doi">10.3389/fnins.2013.00114</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>Dopamine imbalance in Huntington's disease: a mechanism for the lack of behavioral flexibility</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Chen</surname><given-names>Jane Y.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Elizabeth A.</given-names></name></contrib><contrib contrib-type="author"><name><surname>Cepeda</surname><given-names>Carlos</given-names></name></contrib><contrib contrib-type="author"><name><surname>Levine</surname><given-names>Michael S.</given-names></name><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref></contrib></contrib-group><aff><institution>Intellectual and Developmental Disabilities Research Center, Semel Institute for Neuroscience and Human Behavior and the Brain Research Institute, David Geffen School of Medicine, University of California Los Angeles</institution><country>Los Angeles, CA, USA</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Giselle Petzinger, University of Southern California, USA</p></fn><fn fn-type="edited-by"><p>Reviewed by: Krishna P. Miyapuram, University of Trento, Italy; John P. Walsh, University of Southern California, USA</p></fn><corresp id="fn001">*Correspondence: Michael S. Levine, Intellectual and Developmental Disabilities Research Center, Semel Institute for Neuroscience and Human Behavior, School of Medicine, University of California Los Angeles, Room 58-258, 760 Westwood Plaza, Los Angeles, CA 90095, USA e-mail: <email xlink:type="simple">mlevine@mednet.ucla.edu</email></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Frontiers in Decision Neuroscience, a specialty of Frontiers in Neuroscience.</p></fn></author-notes><pub-date pub-type="epub"><day>04</day><month>7</month><year>2013</year></pub-date><pub-date pub-type="collection"><year>2013</year></pub-date><volume>7</volume><elocation-id>114</elocation-id><history><date date-type="received"><day>08</day><month>3</month><year>2013</year></date><date date-type="accepted"><day>13</day><month>6</month><year>2013</year></date></history><permissions><copyright-statement>Copyright © 2013 Chen, Wang, Cepeda and Levine.</copyright-statement><copyright-year>2013</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, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.</license-p></license></permissions><abstract><p>Dopamine (DA) plays an essential role in the control of coordinated movements. Alterations in DA balance in the striatum lead to pathological conditions such as Parkinson's and Huntington's diseases (HD). HD is a progressive, invariably fatal neurodegenerative disease caused by a genetic mutation producing an expansion of glutamine repeats and is characterized by abnormal dance-like movements (chorea). The principal pathology is the loss of striatal and cortical projection neurons. Changes in brain DA content and receptor number contribute to abnormal movements and cognitive deficits in HD. In particular, during the early hyperkinetic stage of HD, DA levels are increased whereas expression of DA receptors is reduced. In contrast, in the late akinetic stage, DA levels are significantly decreased and resemble those of a Parkinsonian state. Time-dependent changes in DA transmission parallel biphasic changes in glutamate synaptic transmission and may enhance alterations in glutamate receptor-mediated synaptic activity. In this review, we focus on neuronal electrophysiological mechanisms that may lead to some of the motor and cognitive symptoms of HD and how they relate to dysfunction in DA neurotransmission. Based on clinical and experimental findings, we propose that some of the behavioral alterations in HD, including reduced behavioral flexibility, may be caused by altered DA modulatory function. Thus, restoring DA balance alone or in conjunction with glutamate receptor antagonists could be a viable therapeutic approach.</p></abstract><kwd-group><kwd>Huntington's disease</kwd><kwd>behavioral inflexibility</kwd><kwd>dopamine</kwd><kwd>glutamate</kwd><kwd>electrophysiology</kwd></kwd-group><counts><fig-count count="1"></fig-count><table-count count="2"></table-count><equation-count count="0"></equation-count><ref-count count="214"></ref-count><page-count count="14"></page-count><word-count count="13515"></word-count></counts></article-meta></front><body><sec id="s1"><title>Introduction</title><p>Huntington's disease (HD) is an inherited, autosomal dominant, and progressive neurodegenerative disorder caused by a mutation in the huntingtin gene (<italic>HTT</italic>) resulting in an abnormally long polyglutamine (CAG >40) repeat (The Huntington's Disease Collaborative Research Group, <xref ref-type="bibr" rid="B192">1993</xref>). It is characterized by involuntary dance-like movements (chorea) in the early stages, then akinesia and dystonia in the late stages. Other symptoms include psychiatric alterations and cognitive deterioration (Bonelli and Hofmann, <xref ref-type="bibr" rid="B27">2007</xref>). Cognitive disturbances affecting learning, memory processes, as well as attention and executive function emerge early in the course of the disease and become prominent in the advanced stages (Brandt and Butters, <xref ref-type="bibr" rid="B31">1986</xref>; Peinemann et al., <xref ref-type="bibr" rid="B150">2005</xref>; Wang et al., <xref ref-type="bibr" rid="B201">2012</xref>). A juvenile form of HD also occurs, generally when the length of CAG repeats is >60. These patients develop epileptic seizures and intellectual decline associated with a more rapidly progressing course of the disease (Andrew et al., <xref ref-type="bibr" rid="B7">1993</xref>; Seneca et al., <xref ref-type="bibr" rid="B172">2004</xref>).</p><p>In HD, the most striking neuropathology is massive loss of medium-sized spiny neurons (MSNs) in the striatum (Vonsattel and Difiglia, <xref ref-type="bibr" rid="B200">1998</xref>), as well as laminar thinning and white matter loss in the cerebral cortex (Rosas et al., <xref ref-type="bibr" rid="B166">2006</xref>). Other structures such as the globus pallidus, thalamus, hypothalamus, subthalamic nucleus (STN), and substantia nigra also are affected, particularly in the later stages (Kremer et al., <xref ref-type="bibr" rid="B120">1990</xref>; Heinsen et al., <xref ref-type="bibr" rid="B92">1996</xref>; Petersen et al., <xref ref-type="bibr" rid="B154">2005</xref>). Although the symptomatology of HD is classically attributed to striatal and cortical neuronal loss, studies have demonstrated that neuronal dysfunction precedes cell death (Tobin and Signer, <xref ref-type="bibr" rid="B193">2000</xref>; Levine et al., <xref ref-type="bibr" rid="B126">2004</xref>). For example, psychiatric, cognitive, and motor symptoms can and often appear alongside cellular and synaptic alterations in the absence of neuronal loss (Vonsattel and Difiglia, <xref ref-type="bibr" rid="B200">1998</xref>).</p><p>This review examines the role of striatal dopamine (DA) in HD. We focus on neuronal electrophysiological mechanisms that may lead to some of the motor and cognitive symptoms of HD and how they relate to dysfunction in DA neurotransmission. Data from human and animal studies are reviewed with particular emphasis on alterations of the DA system and how they relate to behavioral inflexibility. The central thesis is that the major symptoms of HD can be associated with biphasic changes in DA transmission and its modulatory role on glutamate (GLU) receptor function. Thus, treatments of HD symptoms should take into account and be tailored according to the temporal progression of neurotransmitter and receptor changes. Before elaborating on these changes, we first need to understand the role of the DA system and its interactions in normal neuronal function, particularly in the striatum.</p></sec><sec><title>Striatal organization</title><p>GABAergic projection MSNs comprise 90–95% of striatal neurons (Kita and Kitai, <xref ref-type="bibr" rid="B113">1988</xref>) and receive glutamatergic inputs primarily from the cortex as well as specific thalamic nuclei (Kemp and Powell, <xref ref-type="bibr" rid="B108">1971</xref>; Smith et al., <xref ref-type="bibr" rid="B178">2004</xref>). There are two striatal projection pathways (Figure <xref ref-type="fig" rid="F1">1</xref>), each with distinct MSN populations expressing different DA receptors and neuropeptides (Graybiel, <xref ref-type="bibr" rid="B86">2000</xref>). The direct pathway consists of MSNs expressing DA D1 receptors, substance P, and dynorphin (Vincent et al., <xref ref-type="bibr" rid="B198">1982</xref>; Haber and Nauta, <xref ref-type="bibr" rid="B87">1983</xref>; Gerfen et al., <xref ref-type="bibr" rid="B81">1990</xref>). It projects monosynaptically to the substantia nigra pars reticulata and the internal segment of the globus pallidus (Albin et al., <xref ref-type="bibr" rid="B3">1989</xref>; Gerfen et al., <xref ref-type="bibr" rid="B81">1990</xref>). The indirect pathway is composed of MSNs that express D2 receptors, adenosine A<sub>2A</sub> receptors, and enkephalin (Gerfen et al., <xref ref-type="bibr" rid="B81">1990</xref>; Schiffmann and Vanderhaeghen, <xref ref-type="bibr" rid="B171">1993</xref>; Steiner and Gerfen, <xref ref-type="bibr" rid="B186">1999</xref>), and projects to the external segment of the globus pallidus (Gerfen, <xref ref-type="bibr" rid="B80">1992</xref>; Bolam et al., <xref ref-type="bibr" rid="B25">2000</xref>). The external segment of the globus pallidus, in turn, projects to the STN (Albin et al., <xref ref-type="bibr" rid="B3">1989</xref>). Electrophysiological studies using mice expressing enhanced green fluorescent protein (EGFP) in MSNs enriched with D1 or D2 DA receptors demonstrated that, although direct and indirect pathway neurons display similar basic membrane properties, indirect pathway MSNs are more excitable and thus may be more susceptible to abnormal GLU release or receptor dysfunction (Kreitzer and Malenka, <xref ref-type="bibr" rid="B119">2007</xref>; Cepeda et al., <xref ref-type="bibr" rid="B40">2008</xref>). This is partially due to a difference in dendritic surface area, where indirect pathway MSNs have fewer primary dendrites than direct pathway MSNs, suggesting that the increased excitability of indirect pathway MSNs partially results from a higher membrane input resistance due to their more compact morphology (Gertler et al., <xref ref-type="bibr" rid="B82">2008</xref>; Flores-Barrera et al., <xref ref-type="bibr" rid="B70">2010</xref>). The remaining 5–10% of striatal neurons are interneurons, which are divided into two main groups: GABAergic interneurons, which provide feedforward inhibition to MSNs (Tepper et al., <xref ref-type="bibr" rid="B191">2008</xref>); and cholinergic interneurons, which are responsible for acetylcholine levels in the striatum (Bolam et al., <xref ref-type="bibr" rid="B26">1984</xref>; Zhou et al., <xref ref-type="bibr" rid="B214">2002</xref>).</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Striatal projection pathways</bold>. In the direct “GO” pathway, MSNs expressing DA D1 receptors receive inputs from intratelencephalically projecting (IT) neurons in the cortex (Ctx) and project to the substantia nigra pars reticulata (SNr) as well as the internal segment of the globus pallidus (GPi). In the indirect “STOP” pathway, MSNs expressing DA D2 receptors receive inputs from pyramidal tract (PT) neurons in the Ctx and project to the external segment of the globus pallidus (GPe). The GPe, in turn, projects to the STN and SNr. Both D1 and D2 MSNs also receive afferents from the substantia nigra pars compacta (SNc) and thalamus (Thal).</p></caption><graphic xlink:href="fnins-07-00114-g0001"></graphic></fig><p>The striatum can also be described as a mosaic of two functionally distinct compartments. The striosome compartment is enriched with μ-opioid receptors while the surrounding extrastriosomal matrix contains neurons that express acetylcholinesterase, somatostatin, and calbindin (Gerfen, <xref ref-type="bibr" rid="B79">1984</xref>). GABAergic striosomal neurons innervate DA neurons in the substantia nigra pars compacta and reticulata, essentially forming a third striatal output pathway (Gerfen, <xref ref-type="bibr" rid="B79">1984</xref>; Jimenez-Castellanos and Graybiel, <xref ref-type="bibr" rid="B102">1989</xref>). Since interactions between striosomes and the extrastriosomal matrix are involved in drug-induced stereotypies (Saka et al., <xref ref-type="bibr" rid="B168">2004</xref>; Canales, <xref ref-type="bibr" rid="B37">2005</xref>), it has been proposed that the striosomal system may change the set point of DA neurons (Canales and Graybiel, <xref ref-type="bibr" rid="B38">2000</xref>). This, in turn, could modulate DA neurotransmission in the basal ganglia and alter the occurrence of stereotypic behaviors (Graybiel, <xref ref-type="bibr" rid="B86">2000</xref>). As discussed later, pathological changes in the striosome compartment could underlie dysregulation of DA release in the early stages of HD.</p></sec><sec><title>Modulatory role of DA in the brain</title><p>The modulatory effects of DA are better understood if considered as a representation of an inverted “U” shaped function. This concept suggests that too much or too little DA perturbs cognitive function (Williams and Castner, <xref ref-type="bibr" rid="B210">2006</xref>; Vijayraghavan et al., <xref ref-type="bibr" rid="B197">2007</xref>). Furthermore, maximum efficiency in behavioral and cognitive performance is a result of maintaining an optimal DA level, where imbalances cause decreased efficiency (Dickinson and Elvevag, <xref ref-type="bibr" rid="B62">2009</xref>). As an extension, we can say that in the dorsal striatum, increases or decreases in DA alter motor behavior.</p><p>One of the main functions of DA in the brain is to enhance the signal-to-noise ratio. This can be achieved by at least 3 different mechanisms: (1) DA can modulate neuronal firing in a selective manner. For example, studies in awake rats show that iontophoresis of DA induces excitation of motor-related, and inhibition of non-motor-related neurons (Pierce and Rebec, <xref ref-type="bibr" rid="B156">1995</xref>). Also, the effect of D1 agonists on neuronal firing can be excitatory or inhibitory depending on the membrane potential of the cell. At hyperpolarized potentials, D1 receptor activation is inhibitory, whereas at depolarized potentials, it is excitatory (Hernandez-Lopez et al., <xref ref-type="bibr" rid="B93">1997</xref>). (2) DA affects responses evoked by GLU in a differential manner. Responses evoked by activation of α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionic acid (AMPA) receptors are reduced by DA, whereas responses evoked by activation of N-methyl-D-aspartate (NMDA) receptors are increased by DA (Cepeda et al., <xref ref-type="bibr" rid="B41">1993</xref>; Levine et al., <xref ref-type="bibr" rid="B127">1996</xref>; Cepeda and Levine, <xref ref-type="bibr" rid="B45">1998</xref>). In general, activation of D1 receptors enhances GLU responses whereas activation of D2 receptors decreases these responses (Cepeda et al., <xref ref-type="bibr" rid="B41">1993</xref>). (3) DA also can select excitatory inputs to the striatum (Flores-Hernandez et al., <xref ref-type="bibr" rid="B72">1997</xref>) and thus act as a filter for less active inputs (Bamford et al., <xref ref-type="bibr" rid="B17">2004</xref>). These effects are probably mediated by presynaptic D2 receptors located on corticostriatal GLU terminals (Cepeda et al., <xref ref-type="bibr" rid="B43">2001</xref>). DA modulation of neurotransmitter release also is influenced by endocannabinoid production and retrograde activation of presynaptic corticostriatal CB1 receptors (Maejima et al., <xref ref-type="bibr" rid="B129">2001</xref>; Patel et al., <xref ref-type="bibr" rid="B148">2003</xref>; Kreitzer and Malenka, <xref ref-type="bibr" rid="B118">2005</xref>).</p></sec><sec><title>DA and behavioral inflexibility</title><p>Behavioral inflexibility is defined as a failure to shift between behaviors and the inability to adapt behavior to changes in environmental stimuli. Lack of behavioral flexibility depends on the inability to stop ongoing behaviors and is mediated by a discrete cortico-basal ganglia circuit (Aron and Poldrack, <xref ref-type="bibr" rid="B13">2006</xref>; Aron et al., <xref ref-type="bibr" rid="B12">2007</xref>). Although behavioral routines are often stereotyped through learning and result in habit formation, extremely repetitive behaviors (stereotypies) appear to be prominent symptoms in various neuropsychiatric disorders and addiction. These range from impaired behavioral inhibition in attention deficit/hyperactivity disorder and inability to suppress emotions in autism spectrum disorders, to repetitive twitches or vocalizations in Tourette's syndrome, movement fixation in obsessive-compulsive disorder, punding due to over-medication of Parkinson's disease patients, and may include some of the involuntary movements in HD. Despite the wide range of behavioral phenotypes in these disorders, central features of these behaviors are DA-dependent and related to striatal dysfunction (Frank et al., <xref ref-type="bibr" rid="B73">2004</xref>; Beste et al., <xref ref-type="bibr" rid="B21">2010</xref>).</p><p>Changes in the DA system have long been implicated in human cognitive inflexibility. However, patients with DA impairments do not show deficits on all tasks that assess cognitive flexibility. Specifically, DA function in the striatum involves set-shifting between object features but is not involved in shifting between abstract rules (Cools et al., <xref ref-type="bibr" rid="B49">2006</xref>; Dang et al., <xref ref-type="bibr" rid="B58">2012</xref>). Patients with disorders of the basal ganglia, such as in Parkinson's Disease or HD, routinely show cognitive inflexibility as demonstrated by impaired performance on the Wisconsin Card Sorting Test and attentional set-shifting tests (Owen et al., <xref ref-type="bibr" rid="B145">1993</xref>; Lawrence et al., <xref ref-type="bibr" rid="B123">1996</xref>).</p><p>In the striatum, different subregions are involved in specific behavioral strategies and learning. Rats with lesions of the lateral striatum have deficits in motor skill learning and arbitrary stimulus-response associations (Reading et al., <xref ref-type="bibr" rid="B163">1991</xref>; Devan et al., <xref ref-type="bibr" rid="B61">1999</xref>), whereas those with lesions of the medial striatum have impairments in spatial and reversal learning (Whishaw et al., <xref ref-type="bibr" rid="B209">1987</xref>; Pisa and Cyr, <xref ref-type="bibr" rid="B158">1990</xref>). Furthermore, the medial striatum plays a role in switching between navigational strategies in response to changes in the environment (Mizumori et al., <xref ref-type="bibr" rid="B138">2000</xref>). The dorsomedial striatum also is necessary for maintaining and executing a new strategy. Failure to maintain a proper response pattern by shifting strategies results in behavioral inflexibility (Ragozzino, <xref ref-type="bibr" rid="B161">2007</xref>). Additionally, reversal learning and trait impulsivity in mice is associated with DA receptor density in the midbrain (Dalley et al., <xref ref-type="bibr" rid="B57">2007</xref>; Lee et al., <xref ref-type="bibr" rid="B124">2009</xref>). Taken together, these studies indicate that the striatum and DA neurotransmission play a crucial role in determining behavioral flexibility.</p><p>Stereotypies in rodents are an extreme form of behavioral inflexibility that manifest as rigid, repetitive movements. These include excessive grooming, sniffing, rearing, as well as locomotion, and may be more manifest during social isolation and stress (Ridley, <xref ref-type="bibr" rid="B165">1994</xref>). Stereotypies present as behavioral abnormalities with little flexibility and high repetition, often similar to addictive states. Drugs that act on the DA system can produce stereotyped behaviors in a dose-dependent manner. For example, low doses of amphetamine and cocaine induce repetitive locomotion while high doses cause more focal stereotypy, such as sniffing and grooming (Cooper and Dourish, <xref ref-type="bibr" rid="B50">1990</xref>). Striatal cocaine administration also results in impaired reversal learning (Stalnaker et al., <xref ref-type="bibr" rid="B185">2009</xref>), further indicating that aberrant DA transmission results in behavioral inflexibility. The intensity of drug-induced stereotypies is determined by striatal DA, where rats with high extracellular DA levels demonstrate complex stereotypic behavior, including syntactic grooming (Berridge et al., <xref ref-type="bibr" rid="B20">2005</xref>). In fact, robust stereotypies in rats similar to those induced by amphetamine and cocaine can be induced by striatal infusions of D1 and D2 receptor agonists (Waszczak et al., <xref ref-type="bibr" rid="B206">2002</xref>).</p><p>It would be misleading, however, to think that only DA alterations are involved in behavioral inflexibility. In fact, the capacity for attentional shifts and inhibition of ongoing motor activity by salient stimuli seems to depend on thalamostriatal inputs onto cholinergic interneurons (Ding et al., <xref ref-type="bibr" rid="B64">2010</xref>). These aspiny interneurons have rich terminal connections and are implicated in stereotypic behavior as well as associative learning (Aosaki et al., <xref ref-type="bibr" rid="B9">1994</xref>, <xref ref-type="bibr" rid="B10">2010</xref>). For example, striatal application of the muscarinic receptor antagonist pirenzepine impairs reversal learning, indicating that these cholinergic receptors play a role in the shifting of response patterns (Tzavos et al., <xref ref-type="bibr" rid="B194">2004</xref>). Thus, cholinergic interneurons may also play an important role in the loss of cognitive and behavioral flexibility in pathological conditions including HD.</p></sec><sec><title>DA alterations in huntington's disease</title><p>Alterations in DA function play a significant role in the motor and cognitive symptoms of HD. Here we will discuss changes in DA transmission that may underlie the neuropathological changes in HD. There is evidence from studies in HD patients that increased DA release induces chorea while a reduction in DA leads to akinesia (Bird, <xref ref-type="bibr" rid="B23">1980</xref>; Spokes, <xref ref-type="bibr" rid="B182">1980</xref>), thus giving rise to the biphasic movement symptoms of early and late HD. The idea that aberrant DA signaling underlies behavioral abnormalities was first proposed as a predictive test when asymptomatic offspring of individuals with HD developed dyskinesias in response to levodopa (L-DOPA) administration (Klawans et al., <xref ref-type="bibr" rid="B116">1970</xref>). The hypothesis was that stimulation of DA receptors was involved in the production of dyskinesias as a basic mechanism of chorea. Early studies indicating an involvement of the DA nigrostriatal pathway in HD demonstrated increased levels of DA in postmortem brains of HD patients and showed that DA-depleting agents and DA receptor agonists can be used with therapeutic benefit (Bird, <xref ref-type="bibr" rid="B23">1980</xref>; Spokes, <xref ref-type="bibr" rid="B182">1980</xref>). Later, neurochemical studies of HD patients suggested that increased DA occurs in the early stages of the disease (Garrett and Soares-Da-Silva, <xref ref-type="bibr" rid="B78">1992</xref>) while postmortem studies of late-stage HD patients showed reduced levels of caudate DA and homovanillic acid, the principal DA metabolite (Bernheimer et al., <xref ref-type="bibr" rid="B19">1973</xref>; Kish et al., <xref ref-type="bibr" rid="B112">1987</xref>). Thus, it was thought that DA levels in HD may show biphasic, time-dependent changes, with early increases followed by late decreases (Table <xref ref-type="table" rid="T1">1</xref>).</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>DA in human HD and animal models</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="1" colspan="1"></th><th align="left" rowspan="1" colspan="1"><bold>Early stage</bold></th><th align="left" rowspan="1" colspan="1"><bold>Late stage</bold></th></tr></thead><tbody><tr><td align="left" colspan="3" rowspan="1"><bold>HUMAN HD</bold></td></tr><tr><td align="left" rowspan="2" colspan="1">DA levels in striatum</td><td align="left" valign="top" rowspan="1" colspan="1">Increased</td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Garrett and Soares-Da-Silva, <xref ref-type="bibr" rid="B78">1992</xref></td><td align="left" valign="top" rowspan="1" colspan="1">Bernheimer et al., <xref ref-type="bibr" rid="B19">1973</xref>; Kish et al., <xref ref-type="bibr" rid="B112">1987</xref></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">DA receptor density</td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Joyce et al., <xref ref-type="bibr" rid="B106">1988</xref>; Richfield et al., <xref ref-type="bibr" rid="B164">1991</xref>; Van Oostrom et al., <xref ref-type="bibr" rid="B195">2009</xref></td><td align="left" valign="top" rowspan="1" colspan="1">Antonini et al., <xref ref-type="bibr" rid="B8">1996</xref>; Weeks et al., <xref ref-type="bibr" rid="B207">1996</xref></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">DAT</td><td align="left" valign="top" rowspan="1" colspan="1">Not determined</td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td></tr><tr><td rowspan="1" colspan="1"></td><td align="left" valign="top" rowspan="1" colspan="1">Backman et al., <xref ref-type="bibr" rid="B16">1997</xref>; Ginovart et al., <xref ref-type="bibr" rid="B83">1997</xref>; Suzuki et al., <xref ref-type="bibr" rid="B188">2001</xref></td></tr><tr><td align="left" colspan="3" rowspan="1"><bold>ANIMAL MODELS</bold></td></tr><tr><td align="left" valign="top" rowspan="3" colspan="1">DA levels</td><td align="left" valign="top" rowspan="1" colspan="1">Increased<sup>*</sup></td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><sup>*</sup>tgHD rat model</td><td align="left" valign="top" rowspan="2" colspan="1">Hickey et al., <xref ref-type="bibr" rid="B94">2002</xref>; Johnson et al., <xref ref-type="bibr" rid="B103">2006</xref>; Callahan and Abercrombie, <xref ref-type="bibr" rid="B36">2011</xref></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Jahanshahi et al., <xref ref-type="bibr" rid="B99">2010</xref></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">DA receptors</td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td><td align="left" valign="top" rowspan="1" colspan="1">Decreased</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Cha et al., <xref ref-type="bibr" rid="B46">1998</xref>; Bibb et al., <xref ref-type="bibr" rid="B22">2000</xref>; Ariano et al., <xref ref-type="bibr" rid="B11">2002</xref>; Petersen et al., <xref ref-type="bibr" rid="B153">2002b</xref></td><td align="left" valign="top" rowspan="1" colspan="1">Pouladi et al., <xref ref-type="bibr" rid="B159">2012</xref></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">DAT</td><td align="left" valign="top" rowspan="1" colspan="1">Not determined</td><td align="left" valign="top" rowspan="1" colspan="1">Not determined</td></tr></tbody></table></table-wrap><p>During the early phase of HD, neuropathological studies have shown that discrete islands of neuronal loss and astrocytosis appear in the striosomes almost exclusively, whereas in the late phase, cell loss increasingly occurs in the matrix compartment (Hedreen and Folstein, <xref ref-type="bibr" rid="B91">1995</xref>). As MSNs from the striosomes project to the substantia nigra pars compacta, it may be that early degeneration of these inhibitory neurons produces hyperactivity of the DA pathway, contributing to chorea and other early clinical manifestations of HD. Studies using positron emission tomography, autoradiography, and markers for pre- and postsynaptic neurons have observed reduced striatal D1 and D2 DA receptor density, even in asymptomatic HD patients, further indicating that DA signaling is disrupted early in HD (Joyce et al., <xref ref-type="bibr" rid="B106">1988</xref>; Richfield et al., <xref ref-type="bibr" rid="B164">1991</xref>; Van Oostrom et al., <xref ref-type="bibr" rid="B195">2009</xref>). These observations have been confirmed by imaging studies, which reported reduced striatal D1 and D2 receptors in both HD patients and asymptomatic HD mutation carriers (Antonini et al., <xref ref-type="bibr" rid="B8">1996</xref>; Weeks et al., <xref ref-type="bibr" rid="B207">1996</xref>). There also is a progressive reduction of D1 and D2 receptor binding in the temporal and frontal cortices (Ginovart et al., <xref ref-type="bibr" rid="B83">1997</xref>; Pavese et al., <xref ref-type="bibr" rid="B149">2003</xref>). Striatal and cortical loss of DA receptors in presymptomatic and early stage HD patients have been correlated with early cognitive decline, which may reflect altered synaptic plasticity and lead to deficits in cognitive processes such as attention, executive function, learning, and memory (Backman and Farde, <xref ref-type="bibr" rid="B15">2001</xref>).</p><p>Studies also have examined DA transporter (DAT) density as both an index of DA neurotransmission and a correlate of clinical status (Hwang and Yao, <xref ref-type="bibr" rid="B97">2011</xref>). DAT is a key regulator of DA receptor stimulation and, in turn, affects locomotion and cognitive function. DA transmission is initiated by DA release from the presynaptic terminal and is terminated by its reuptake through DAT. In fact, postmortem analyses of brains from HD patients have shown reduced striatal DAT binding and reduced levels of vesicular monoamine transporter type-2, which is used to estimate the extent of DA innervation (Backman et al., <xref ref-type="bibr" rid="B16">1997</xref>; Ginovart et al., <xref ref-type="bibr" rid="B83">1997</xref>; Suzuki et al., <xref ref-type="bibr" rid="B188">2001</xref>). This indicates that the reduction in DAT binding likely results from a loss of DA nigrostriatal terminals, consistent with the view that the dystonic late-stage symptoms of HD may arise in part from critical reductions in DA input.</p></sec><sec><title>DA in animal models of HD</title><p>Animal models of HD have been available for more than 30 years, beginning with the first neurotoxin-based models in which chemically-induced striatal lesions reproduced HD neuropathology, providing insights into the mechanisms underlying striatal cell death (Difiglia, <xref ref-type="bibr" rid="B63">1990</xref>; Brouillet et al., <xref ref-type="bibr" rid="B32">1999</xref>). After the discovery of the HD gene, transgenic and knock-in rodent models were generated. These better replicated the processes and mechanisms underlying the slow development of the human disease far beyond endpoint analyses. We have previously reviewed the phenotypic properties of a number of these models (Cepeda et al., <xref ref-type="bibr" rid="B42">2010</xref>; Raymond et al., <xref ref-type="bibr" rid="B162">2011</xref>). Here, we will briefly describe those that have been used for electrophysiological studies examining DA neurotransmission.</p><p>The most widely used mouse model for electrophysiology is the R6/2 line, a transgenic fragment model expressing exon 1 of <italic>HTT</italic> with ~150 CAG repeats (Mangiarini et al., <xref ref-type="bibr" rid="B130">1996</xref>). R6/2 mice display a very rapidly progressing phenotype, similar to the juvenile form of HD in humans. In these mice, overt symptoms begin to appear at 5–7 weeks of age and become fully manifest after 8 weeks. The R6/1 transgenic mouse model, with ~110 CAG repeats and less mutant <italic>HTT</italic> expression than the R6/2, displays similar phenotypic alterations but in a more protracted form (Mangiarini et al., <xref ref-type="bibr" rid="B130">1996</xref>). HD mouse models with full-length mutant <italic>HTT</italic> include the yeast artificial chromosome model with 128 CAG repeats (YAC128) and the bacterial artificial chromosome model with 97 CAG/CAA repeats (BACHD) (Slow et al., <xref ref-type="bibr" rid="B176">2003</xref>; Gray et al., <xref ref-type="bibr" rid="B85">2008</xref>). These models show a longer development of the HD phenotype and thus are generally studied at the early (1.5–2 months of age) and late stages (12 months of age), corresponding roughly to periods of hyperkinesia and hypokinesia, respectively. In contrast to transgenic mice where the mutant <italic>HTT</italic> is randomly inserted into the mouse genome, knock-in mouse models have the CAG expansion inserted into the mouse huntingtin gene, which allows gene expression in its appropriate genomic and protein context (Menalled, <xref ref-type="bibr" rid="B134">2005</xref>). The transgenic rat model of HD (tgHD) carries a truncated huntingtin cDNA fragment with 51 CAG repeats (Von Horsten et al., <xref ref-type="bibr" rid="B199">2003</xref>). The tgHD model and most knock-in mouse models also manifest a slow progression of the HD phenotype.</p><p>There is evidence that DA release is reduced in transgenic mouse models in the late stages of the disease, consistent with what is proposed to occur in human HD. There is a progressive reduction in striatal DA levels in both R6/2 and YAC128 mice concomitant with motor abnormalities (Hickey et al., <xref ref-type="bibr" rid="B94">2002</xref>; Johnson et al., <xref ref-type="bibr" rid="B103">2006</xref>; Callahan and Abercrombie, <xref ref-type="bibr" rid="B36">2011</xref>). Furthermore, motorically asymptomatic R6/2 mice show a significant reduction in DA metabolites by 4 weeks of age (Mochel et al., <xref ref-type="bibr" rid="B139">2011</xref>). Deficits in DA levels and/or release have been attributed to either impaired vesicle loading or a reduction in DA reserve pool vesicles available for mobilization (Suzuki et al., <xref ref-type="bibr" rid="B188">2001</xref>; Ortiz et al., <xref ref-type="bibr" rid="B143">2010</xref>). The tgHD rat model displays an increase in striatal DA levels and DA neurons at the early symptomatic stage in two main sources of striatal DA input, the substantia nigra pars compacta and the ventral tegmental area (Jahanshahi et al., <xref ref-type="bibr" rid="B99">2010</xref>). However, these rats also show impaired DA release dynamics, as demonstrated by a reduction in evoked release of DA (Ortiz et al., <xref ref-type="bibr" rid="B144">2012</xref>). Since these results from animal models are not entirely consistent, future studies on DA release dynamics in HD will be needed to parse out changes in DA levels that occur in the early and late disease stages (Table <xref ref-type="table" rid="T1">1</xref>).</p><p>In agreement with analyses of HD patients, striatal D1 and D2 receptors also are compromised in HD mouse models. Striatal D1 and D2 receptor binding is reduced early, with deficiencies in DA signaling seen in R6/2 and R6/1 mice (Cha et al., <xref ref-type="bibr" rid="B46">1998</xref>; Bibb et al., <xref ref-type="bibr" rid="B22">2000</xref>; Ariano et al., <xref ref-type="bibr" rid="B11">2002</xref>; Petersen et al., <xref ref-type="bibr" rid="B152">2002a</xref>). Significant reductions also are seen in mRNA levels of striatal D1 and D2 receptors in late stage YAC128 mice, but not in BACHD mice (Pouladi et al., <xref ref-type="bibr" rid="B159">2012</xref>). It is unclear why these differences occur between the two full-length models.</p><p>The traditional view of behavioral abnormalities in HD proposes that hyperkinetic choreic movements in the early stages result from initial dysfunction of D2-enriched indirect pathway MSNs, while hypokinesia during the late stages is a consequence of further defects in D1-enriched direct pathway MSNs (Spektor et al., <xref ref-type="bibr" rid="B180">2002</xref>). This view has been challenged by recent data obtained in experimental mouse models of HD (YAC128 and BACHD) crossed with mice expressing EGFP in direct and indirect pathway neurons. In the early hyperkinetic stage (1.5 months of age), direct pathway MSNs receive more excitatory inputs than control animals, whereas indirect pathway MSNs are not as affected. In contrast, in the late hypokinetic stage (12 months of age) both pathways receive less excitatory inputs compared to controls (André et al., <xref ref-type="bibr" rid="B6">2011b</xref>; Galvan et al., <xref ref-type="bibr" rid="B77">2012</xref>).</p><p>DAT dysregulation also may mediate key alterations in DA neurotransmission and behavior in HD mouse models. A marked reduction of DAT immunoreactivity is observed in the striatum of R6/2 mice (Stack et al., <xref ref-type="bibr" rid="B184">2007</xref>). DAT knock-out mice present not only neuropathological but also behavioral hallmarks of HD, i.e., elevated striatal extracellular DA levels, selective MSN degeneration, and locomotor hyperactivity (Giros et al., <xref ref-type="bibr" rid="B84">1996</xref>; Jones et al., <xref ref-type="bibr" rid="B104">1998</xref>; Cyr et al., <xref ref-type="bibr" rid="B55">2006</xref>; Crook and Housman, <xref ref-type="bibr" rid="B52">2012</xref>). Additionally, studies of DAT knock-out mice crossed with a knock-in mouse model of HD demonstrate an increase in stereotypic behavior that emerges at 6 months of age before returning to baseline by 12 months. Wild-type mice crossed with these knock-in HD mice merely demonstrate a similar but less pronounced biphasic pattern of locomotor alteration (Cyr et al., <xref ref-type="bibr" rid="B55">2006</xref>). Thus, it can be concluded that enhanced DA transmission in HD mice exacerbates the behavioral phenotype of the disease.</p></sec><sec><title>DA and synaptic plasticity in HD</title><p>Striatal long-term depression (LTD), a long-lasting decrease in the efficacy of GLU synapses, can be induced through high frequency afferent stimulation or sustained postsynaptic membrane depolarization paired with activation of presynaptic metabotropic GLU receptors (Calabresi et al., <xref ref-type="bibr" rid="B35">1994</xref>; Kreitzer and Malenka, <xref ref-type="bibr" rid="B118">2005</xref>). Additionally, acetylcholine and activation of DA D2 and endocannabinoid CB1 receptors is necessary for LTD induction (Wang et al., <xref ref-type="bibr" rid="B205">2006</xref>; Singla et al., <xref ref-type="bibr" rid="B175">2007</xref>). Induction of striatal long-term potentiation (LTP), a long-lasting increase in the efficacy of GLU synapses, requires activation of DA D1, NMDA, and muscarinic acetylcholine receptors (Calabresi et al., <xref ref-type="bibr" rid="B34">1999</xref>; Kerr and Wickens, <xref ref-type="bibr" rid="B109">2001</xref>). LTD is more easily induced in the dorsolateral and caudal striatum while LTP is more prevalent in the dorsomedial and rostral striatum (Partridge et al., <xref ref-type="bibr" rid="B147">2000</xref>; Spencer and Murphy, <xref ref-type="bibr" rid="B181">2000</xref>; Smith et al., <xref ref-type="bibr" rid="B177">2001</xref>).</p><p>The 3-nitropropionic acid (3-NP) toxin model shows an increase in NMDA receptor-dependent LTP at cortico-striatal synapses (Akopian et al., <xref ref-type="bibr" rid="B2">2008</xref>). This form of LTP is mediated by D1 receptors and can be reversed by exogenous addition of DA or a D2 receptor agonist. In genetic HD mouse models, DA levels and receptor numbers are altered, resulting in impaired synaptic plasticity. Furthermore, R6/2 mice display a significant reduction in D1-receptor mediated LTP in the striatum (Kung et al., <xref ref-type="bibr" rid="B121">2007</xref>). Impaired LTP in the medial prefrontal cortex of presymptomatic R6/1 mice can be reversed by D1 receptor agonists (Dallerac et al., <xref ref-type="bibr" rid="B56">2011</xref>). Additionally, layer II/III cells in the perirhinal cortex of symptomatic R6/1 mice are unable to support LTD, which may be a result of reductions in D2 receptor activation (Cummings et al., <xref ref-type="bibr" rid="B54">2006</xref>). Paired-pulse profiles, which are measures of short-term plasticity, are aberrant in cortical slices from R6/1 mice. Instead of exhibiting paired-pulse depression seen in control mice, mutants show a more facilitatory profile. Quinpirole, a D2 receptor agonist, produces a profile that resembles age-matched controls and restores LTD (Cummings et al., <xref ref-type="bibr" rid="B54">2006</xref>). Evidence that D1 receptor agonists rescue impaired LTP while D2 receptor agonists rescue impaired LTD show that there is much promise in therapeutics targeting DA modulation of synaptic plasticity. These are functional consequences that hold important implications for ameliorating the cognitive deficits in HD.</p><p>As cholinergic transmission and DA are involved in both LTD and LTP, disturbances of the DA-acetylcholine balance in synaptic plasticity could lead to behavioral deficits. In several HD rodent models, LTP does not occur in cholinergic interneurons. As a consequence, MSNs do not display depotentiation, a process induced by low frequency stimulation that leads to reversion of LTP and requires activation of muscarinic receptors (Picconi et al., <xref ref-type="bibr" rid="B155">2006</xref>). This lack of depotentiation may represent a synaptic mechanism for early behavioral abnormalities observed in HD (Picconi et al., <xref ref-type="bibr" rid="B155">2006</xref>).</p></sec><sec><title>DA and GLU receptor interactions in HD</title><p>Although it is unknown why MSNs preferentially degenerate in HD, one major hypothesis has been that MSNs are more susceptible to excitotoxicity. This theory posits that an excess of excitatory neurotransmitters such as GLU and/or overactivation of GLU receptors, particularly the NMDA receptor, mediate MSN neurodegeneration. Overactivity of NMDA receptors can induce cell death through sustained neuronal membrane depolarization, unchecked Ca<sup>2+</sup> influx, and/or mitochondrial dysfunction (Difiglia, <xref ref-type="bibr" rid="B63">1990</xref>; Coyle and Puttfarcken, <xref ref-type="bibr" rid="B51">1993</xref>). In addition, although DA exists in high concentrations in the striatum, studies also suggest a toxic role for DA in which cell death is accelerated through increases in free radical production (Hastings et al., <xref ref-type="bibr" rid="B90">1996</xref>; Jakel and Maragos, <xref ref-type="bibr" rid="B100">2000</xref>; Wersinger et al., <xref ref-type="bibr" rid="B208">2004</xref>; Hastings, <xref ref-type="bibr" rid="B89">2009</xref>). In striatal cultures derived from R6/2 mice, MSNs undergo DA-mediated oxidative stress and apoptosis (Petersen et al., <xref ref-type="bibr" rid="B151">2001</xref>). Further, DAT knock-out mice are hypersensitive to 3-NP striatal damage (Fernagut et al., <xref ref-type="bibr" rid="B68">2002</xref>).</p><p>DA and GLU neurotransmission are intimately intertwined. Understanding this interplay could help elucidate the cause of biphasic DA changes in human HD. In animal models of HD, biphasic changes in corticostriatal GLU transmission are characterized by initial increases in GLU synaptic activity followed by later decreases (Klapstein et al., <xref ref-type="bibr" rid="B115">2001</xref>; Cepeda et al., <xref ref-type="bibr" rid="B44">2003</xref>; Joshi et al., <xref ref-type="bibr" rid="B105">2009</xref>; André et al., <xref ref-type="bibr" rid="B5">2011a</xref>). Early increases in GLU are associated with cortical hyperexcitability (Cepeda et al., <xref ref-type="bibr" rid="B44">2003</xref>; Spampanato et al., <xref ref-type="bibr" rid="B179">2008</xref>; Cummings et al., <xref ref-type="bibr" rid="B53">2009</xref>) and loss of D2 receptors contributes to increased synaptic activity. Stimulation of corticostriatal neurons has been shown to activate DA release in the striatum (Nieoullon et al., <xref ref-type="bibr" rid="B142">1978</xref>). In addition, DA neurons that modulate GLU release in the corticostriatal pathway are subject to afferent GLU regulation, which is suggested by the presence of GLU receptors on DA neurons (Meltzer et al., <xref ref-type="bibr" rid="B133">1997</xref>). There is substantial evidence for a direct cortico-nigral projection (Afifi et al., <xref ref-type="bibr" rid="B1">1974</xref>; Kornhuber et al., <xref ref-type="bibr" rid="B117">1984</xref>; Naito and Kita, <xref ref-type="bibr" rid="B141">1994</xref>) and work in rodents demonstrates that this pathway both directly and indirectly regulates the firing pattern of DA neurons (Maurice et al., <xref ref-type="bibr" rid="B131">1999</xref>; Sesack and Carr, <xref ref-type="bibr" rid="B173">2002</xref>). Other studies indicate that stimulation of GLU receptors on DA neurons increases DA release in both the substantia nigra and in DA innervated areas (Mintz et al., <xref ref-type="bibr" rid="B137">1986</xref>; Kalivas et al., <xref ref-type="bibr" rid="B107">1989</xref>; Murase et al., <xref ref-type="bibr" rid="B140">1993</xref>). Thus, if DA neuron firing is regulated by frontal cortical neurons, the activity of which is upregulated in early HD, the biphasic trends of DA levels in early and late human HD may be correlated with the biphasic changes of GLU release by cortical afferents. This indicates that biphasic changes in DA levels during early and late HD parallel changes occurring in GLU transmission.</p><p>In forebrain neurons, which receive both DA and GLU input, a diminished signal-to-noise ratio can impair both motor and cognitive functions (Kiyatkin and Rebec, <xref ref-type="bibr" rid="B114">1996</xref>). Furthermore, a reduction in DA diminishes the strength of the GLU signal above background activity (Kiyatkin and Rebec, <xref ref-type="bibr" rid="B114">1996</xref>). Recently, Hong and Rebec (<xref ref-type="bibr" rid="B95">2012</xref>) developed a theoretical framework suggesting that inflexibility rather than inconsistency is the more relevant problem to explain changes during aging and neurodegeneration. Dysfunction in the DA and GLU systems restricts their ability to modulate neural noise. With aging and neurodegeneration, the range over which DA and GLU can be modulated is decreased, leading to dysfunctional neuronal communication, increased neural noise, and inflexibility in brain activity (Hong and Rebec, <xref ref-type="bibr" rid="B95">2012</xref>). Increased neural noise is evident in HD, appearing as a decrease in burst activity and a loss of correlation in the firing patterns of pairs of neurons in the striatum of HD mice (Miller et al., <xref ref-type="bibr" rid="B136">2008</xref>). As a consequence, behavioral adaptations in response to environmental challenges are reduced.</p><p>DA and GLU signaling pathways can synergistically enhance MSN sensitivity to huntingtin toxicity. Studies demonstrate that this deleterious process occurs through D1 but not D2 receptor activation (Tang et al., <xref ref-type="bibr" rid="B189">2007</xref>; Paoletti et al., <xref ref-type="bibr" rid="B146">2008</xref>) and are in agreement with previous studies demonstrating that DA and D1 receptor agonists enhance excitotoxicity (Cepeda and Levine, <xref ref-type="bibr" rid="B45">1998</xref>; McLaughlin et al., <xref ref-type="bibr" rid="B132">1998</xref>). D1 receptor-mediated potentiation of NMDA responses, which holds key functional consequences in HD, has been verified in the cortex and striatum (Cepeda et al., <xref ref-type="bibr" rid="B41">1993</xref>; Wang and O'donnell, <xref ref-type="bibr" rid="B203">2001</xref>; Flores-Hernandez et al., <xref ref-type="bibr" rid="B71">2002</xref>). For example, D1 receptor-induced cell death in MSNs of knock-in HD mice is increased with pretreatment with NMDA when compared with cells from wild-type mice (Paoletti et al., <xref ref-type="bibr" rid="B146">2008</xref>). In neurons from YAC128 mice or Q111 knock-in mice, the convergence of DA and GLU signaling pathways leads to Ca<sup>2+</sup> overload, resulting in excitotoxic processes such as induction of mitochondrial depolarization and caspase activation (Cepeda et al., <xref ref-type="bibr" rid="B43">2001</xref>; Zeron et al., <xref ref-type="bibr" rid="B213">2002</xref>, <xref ref-type="bibr" rid="B212">2004</xref>; Tang et al., <xref ref-type="bibr" rid="B189">2007</xref>; Paoletti et al., <xref ref-type="bibr" rid="B146">2008</xref>).</p><p>While D1-NMDA receptor activation is thought to be neurotoxic, activation of D2 receptors reduces NMDA receptor responses and thus may be neuroprotective (Lee et al., <xref ref-type="bibr" rid="B125">2002</xref>; Bozzi and Borrelli, <xref ref-type="bibr" rid="B30">2006</xref>; Blanke and Vandongen, <xref ref-type="bibr" rid="B24">2009</xref>). For example, activation of D2 receptors by quinpirole reduces the toxicity of both NMDA and kainic acid in rat striatal neurons (Cepeda and Levine, <xref ref-type="bibr" rid="B45">1998</xref>), as well as in mesencephalic and cortical neurons (Sawada et al., <xref ref-type="bibr" rid="B170">1998</xref>; Kihara et al., <xref ref-type="bibr" rid="B110">2002</xref>). However, an exclusive role for D1 receptor activation in mediating MSN degeneration is contradicted by evidence that blocking D2 receptor stimulation significantly reverses DA potentiation of mutant huntingtin-induced MSN cell death (Charvin et al., <xref ref-type="bibr" rid="B48">2005</xref>). As cultured striatal neurons can be protected by antagonism of D1 and D2 receptors, it is possible that both D1 and D2 receptor activation might contribute to neurotoxicity (Davis et al., <xref ref-type="bibr" rid="B59">2002</xref>; Bozzi and Borrelli, <xref ref-type="bibr" rid="B30">2006</xref>). Thus, the exact nature of DA and NMDA interactions are dynamic and complex, indicating a need for further investigation into the differential effects of D1 and D2 activation on GLU signaling in the HD striatum.</p></sec><sec><title>DA agonists and antagonists as treatments for HD</title><p>Since the abnormalities in the DA system appear to underlie many of the behavioral symptoms of HD, DA agonists, antagonists, and/or stabilizers may provide potential treatment options (Table <xref ref-type="table" rid="T2">2</xref>). Conceptually, DA stabilizers (or partial agonists) increase or decrease DA receptor activity depending on the level of DA tone. HD patients treated with aripiprazole, a partial D2 receptor agonist, demonstrate improvements in chorea, but not cognitive function (Brusa et al., <xref ref-type="bibr" rid="B33">2009</xref>). A recent phase 3 clinical trial of the DA stabilizer pridopidine demonstrated improvements in hand movements, gait, and balance of HD patients as defined by the unified HD rating scale (De Yebenes et al., <xref ref-type="bibr" rid="B60">2011</xref>). Although these changes fell short of the primary efficacy threshold, the slight improvements in motor dysfunction without any deleterious side effects suggest that treatments targeted toward DA imbalance may have therapeutic benefits.</p><table-wrap id="T2" position="float"><label>Table 2</label><caption><p><bold>Available and potential treatments</bold>.</p></caption><table frame="hsides" rules="groups"><tbody><tr><td align="left" colspan="2" rowspan="1"><bold>HUMAN HD</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Tetrabenazine</td><td align="left" valign="top" rowspan="1" colspan="1">Well-supported antichoreatic effects but frequent adverse reactions limit its usefulness (Huntington Study Group, <xref ref-type="bibr" rid="B96">2006</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D2 antagonists</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>Haloperidol</italic>: a traditional D2 antagonist; improves chorea, but does not increase functional capacity (Bonelli and Wenning, <xref ref-type="bibr" rid="B28">2006</xref>). <italic>Olanzapine and risperidone</italic>: atypical antipsychotic drugs with D2 antagonist properties; improve chorea and behavioral disturbances (Squitieri et al., <xref ref-type="bibr" rid="B183">2001</xref>; Duff et al., <xref ref-type="bibr" rid="B65">2008</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D2 agonists</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>Bromocriptine</italic>: effects are both positive and negative (Frattola et al., <xref ref-type="bibr" rid="B75">1977</xref>; Caraceni et al., <xref ref-type="bibr" rid="B39">1980</xref>). <italic>Lisuride</italic>: limited positive effects (Caraceni et al., <xref ref-type="bibr" rid="B39">1980</xref>; Frattola et al., <xref ref-type="bibr" rid="B74">1983</xref>). <italic>Aripiprazole</italic>: a partial D2 agonist; improves chorea but not cognitive function (Brusa et al., <xref ref-type="bibr" rid="B33">2009</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Other DA drugs</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>Pridopidine</italic>: a DA stabilizer; produces slight improvements in motor dysfunction (De Yebenes et al., <xref ref-type="bibr" rid="B60">2011</xref>). <italic>L-DOPA</italic>: possibly useful for treatment of rigidity (Racette and Perlmutter, <xref ref-type="bibr" rid="B160">1998</xref>).</td></tr><tr><td align="left" colspan="2" rowspan="1"><bold>ANIMAL MODELS</bold></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Tetrabenazine</td><td align="left" valign="top" rowspan="1" colspan="1">Alleviates motor alterations and reduces striatal loss in both early and late stages (Tang et al., <xref ref-type="bibr" rid="B189">2007</xref>; Wang and Morris, <xref ref-type="bibr" rid="B204">2010</xref>; André et al., <xref ref-type="bibr" rid="B5">2011a</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D1 antagonist</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>SCH23390</italic>: rescues electrophysiological changes in excitatory and inhibitory synaptic transmission in direct pathway MSNs (André et al., <xref ref-type="bibr" rid="B5">2011a</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D1 agonist</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>SKF38393</italic>: reverses impaired LTP in the medial prefrontal cortex of presymptomatic R6/1 mice (Dallerac et al., <xref ref-type="bibr" rid="B56">2011</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D2 antagonist</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>Haloperidol</italic>: early and chronic treatment significantly reduces striatal toxicity in the tgHD rat model (Charvin et al., <xref ref-type="bibr" rid="B47">2008</xref>).</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">D2 agonist</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>Quinpirole</italic>: restores the ability of transgenic cortical slices to support LTD (Cummings et al., <xref ref-type="bibr" rid="B54">2006</xref>).</td></tr></tbody></table></table-wrap><p>Current treatment options for HD are limited and confined to antidopaminergic agents for motor symptoms while there are virtually no therapeutics for cognitive deterioration (Venuto et al., <xref ref-type="bibr" rid="B196">2012</xref>). Additionally, clinical results of these treatments seem contradictory, possibly reflecting the dynamic and time-dependent changes that occur in the DA system as the disease progresses (Mochel et al., <xref ref-type="bibr" rid="B139">2011</xref>). For example, both D2 agonists and antagonists have demonstrated clinical benefits for improvement of HD motor symptoms (Tedroff et al., <xref ref-type="bibr" rid="B190">1999</xref>; Haskins and Harrison, <xref ref-type="bibr" rid="B88">2000</xref>; Brusa et al., <xref ref-type="bibr" rid="B33">2009</xref>). Conventional antipsychotic drugs, such as the D2 antagonist haloperidol, are used in clinical practice, but they do not improve functional capacity (Bonelli and Wenning, <xref ref-type="bibr" rid="B28">2006</xref>). Atypical antipsychotic drugs with D2 antagonist properties such as olanzapine, risperidone, quetiapine, and ziprasidone, can improve chorea and impact a larger range of behavioral disturbances with a reduced risk of side effects (Squitieri et al., <xref ref-type="bibr" rid="B183">2001</xref>; Bonelli et al., <xref ref-type="bibr" rid="B29">2003</xref>; Alpay and Koroshetz, <xref ref-type="bibr" rid="B4">2006</xref>; Duff et al., <xref ref-type="bibr" rid="B65">2008</xref>). D2 agonists like bromocriptine and lisuride have also demonstrated therapeutic potential in HD (Frattola et al., <xref ref-type="bibr" rid="B75">1977</xref>, <xref ref-type="bibr" rid="B74">1983</xref>; Caraceni et al., <xref ref-type="bibr" rid="B39">1980</xref>).</p><p>As the early stages of HD may reflect a hyperdopaminergic stage, drugs that reduce DA tone can be beneficial during the choreic movement phase (Mochel et al., <xref ref-type="bibr" rid="B139">2011</xref>). DA-depleting agents such as tetrabenazine (TBZ), which inhibits vesicular monoamine transporter type-2 and decreases DA content in presynaptic vesicles, have been shown to reduce chorea (Huntington Study Group, <xref ref-type="bibr" rid="B96">2006</xref>). Currently, TBZ is the only drug formally approved for treatment of Huntington's chorea by a regulatory agency (Mestre and Ferreira, <xref ref-type="bibr" rid="B135">2012</xref>).</p><p><italic>In vivo</italic> and <italic>in vitro</italic> studies of animal models support a role for DA inhibitors in protecting HD MSNs from cell death. The rationale follows and agrees with experimental and clinical findings suggesting that DA tone is elevated during the early stages of the disease. In YAC128 mice, TBZ alleviates motor deficits and reduces striatal loss in both early and late stages (Tang et al., <xref ref-type="bibr" rid="B189">2007</xref>; Wang et al., <xref ref-type="bibr" rid="B202">2010</xref>). TBZ also rescues the increased stereotypies in 1–2 month old YAC128 and BACHD mice (André et al., <xref ref-type="bibr" rid="B5">2011a</xref>). D1 receptor antagonists rescue the changes in excitatory synaptic transmission of direct pathway MSNs that occur in the early symptomatic phase of YAC128 and BACHD mice, suggesting that tonic activation of D1 receptors may underlie early dysfunction of D1 MSNs (André et al., <xref ref-type="bibr" rid="B5">2011a</xref>). Similarly, D1 receptor antagonists prevent DA/GLU-induced MSN death in YAC128 mice (Tang et al., <xref ref-type="bibr" rid="B189">2007</xref>). In a lentivirus-based rat model, striatal toxicity is reduced by early and chronic treatment with haloperidol (Charvin et al., <xref ref-type="bibr" rid="B47">2008</xref>). However, this evidence is complicated by the fact that haloperidol, a putative D2 receptor antagonist, also modulates NMDA receptor function (Fletcher and Macdonald, <xref ref-type="bibr" rid="B69">1993</xref>; Ilyin et al., <xref ref-type="bibr" rid="B98">1996</xref>; Arvanov et al., <xref ref-type="bibr" rid="B14">1997</xref>). Predictably, DA antagonists may be more beneficial when administered with other neuroprotective drugs such as memantine, a NMDA receptor antagonist, as a combination therapy (Wu et al., <xref ref-type="bibr" rid="B211">2006</xref>).</p><p>HD mouse models have demonstrated the therapeutic potential of not only DA antagonists, but also DA agonists. For example, in fully symptomatic R6/2 mice, replacement of reduced DA levels by chronic treatment with L-DOPA yields short-term improvements in the HD behavioral phenotype whereas long-term treatment impairs survival and rotarod performance (Hickey et al., <xref ref-type="bibr" rid="B94">2002</xref>). Additionally, D1 receptor agonists rescue cortical LTP impairment and deficits in synaptic plasticity of R6/1 mice (Dallerac et al., <xref ref-type="bibr" rid="B56">2011</xref>), suggesting that increasing DA levels could improve cognitive dysfunction. Since some treatments may only be suitable early or late in disease progression, effective therapies need to be temporally oriented to accommodate differential changes in DA levels throughout the course of the disease.</p></sec><sec><title>Conclusions and future directions</title><p>While the role of DA in Parkinson's disease is well-established, its role in HD is less well-understood. Although an association between chorea and excess DA levels had long been suspected, a causal link was not demonstrated until TBZ was shown to alleviate abnormal movements in HD. Other less known alterations in early symptomatic patients, such as cognitive changes, impulsivity, gambling, and hypersexuality, could also associate with perturbations of the DA system (Fedoroff et al., <xref ref-type="bibr" rid="B66">1994</xref>; Stout et al., <xref ref-type="bibr" rid="B187">2001</xref>; Rosenblatt, <xref ref-type="bibr" rid="B167">2007</xref>; Beglinger et al., <xref ref-type="bibr" rid="B18">2008</xref>; Jhanjee et al., <xref ref-type="bibr" rid="B101">2011</xref>). TBZ can treat chorea and other early symptoms by reducing DA, but it can also have deleterious effects on cognitive function. Understanding time- and region-dependent alterations in DA function throughout the course of the disease will help in discovering better therapeutic strategies. Selective manipulation of DA-producing neurons, such as using optogenetics in animal models and potentially in human patients, may open new and exciting alternatives.</p><p>While much knowledge on the role of DA in HD has been gathered in the past few years, many questions remain unanswered and should be the focus of future endeavors. The traditional view that D2 MSNs are more vulnerable in HD is beginning to change due to emerging data from experimental animal models. Based on evidence reviewed here, one may think that, in fact, D1 MSNs should be more vulnerable to the HD mutation, i.e., they become dysfunctional in the early stage of HD and D1-NMDA receptor interactions enhance neurotoxicity. Therefore, the standing question should be reformulated to ask why D1 MSNs are less susceptible in HD. Do they have a neuroprotective mechanism that D2 MSNs lack? Recent studies using mice expressing EGFP in D1 or D2 cells point in that direction. For example, fluorescence-activated cell sorting array analyses showed that the transcription factor Zfp521, which is enriched in D1 MSNs, is anti-apoptotic (Lobo et al., <xref ref-type="bibr" rid="B128">2008</xref>). Specifically, Zfp521 promotes proliferation, delays differentiation, and reduces apoptosis (Shen et al., <xref ref-type="bibr" rid="B174">2011</xref>).</p><p>Another important question is: what causes early perturbations in DA release? Is it the loss of striosome MSN projections to the substantia nigra pars compacta, increased activity along the cortico-nigral projection, or dysregulation of DA release due to loss of D2 auto-receptors? On a similar note, since there are at least two splice variants for D2 receptors, a short D2S (mostly presynaptic) and a long D2L (mostly postsynaptic) form, which one is reduced in early HD? In the striatum, DA D2 auto-receptor function is mediated by synapsin III, a phosphoprotein that is specifically involved in regulating vesicular reserve pools and DA release in the striatum (Feng et al., <xref ref-type="bibr" rid="B67">2002</xref>; Kile et al., <xref ref-type="bibr" rid="B111">2010</xref>). In brains of R6/2 mice and HD patients, there is a progressive loss of complexins, synaptic proteins similar to syntaxin III that are involved in synaptogenesis and modulate neurotransmitter release (Freeman and Morton, <xref ref-type="bibr" rid="B76">2004</xref>). If a similar reduction in synapsin III occurs, this could explain increased DA transmission in early HD and a consequent loss of behavioral flexibility. In agreement, reversal learning can be improved by increasing levels of synapsin III (Laughlin et al., <xref ref-type="bibr" rid="B122">2011</xref>). Thus far, it is unknown whether or not presynaptic D2 auto- or hetero-receptors are lost before postsynaptic receptors (Sandstrom et al., <xref ref-type="bibr" rid="B169">2010</xref>). However, selective agonists of D2 auto-receptors produce long-lasting suppression of extracellular brain DA levels <italic>in vivo</italic> and could provide promising therapeutic benefits for HD (Pifl et al., <xref ref-type="bibr" rid="B157">1988</xref>).</p><p>As shown in this review, our knowledge of changes in DA function in HD has made substantial strides, particularly after the introduction of genetic rodent models. However, many more questions remain. Answering these questions is within reach and use of these animal models should help understand the early mechanisms of striatal DA dysfunction and its role in behavioral alterations.</p><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></sec></body><back><ack><p>Supported by USPHS NS41574, a contract from CHDI Inc., and the Hereditary Disease Foundation.</p></ack><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Afifi</surname><given-names>A. K.</given-names></name><name><surname>Bahuth</surname><given-names>N. B.</given-names></name><name><surname>Kaelber</surname><given-names>W. 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