Neural and behavioral substrates of subtypes of Parkinson’s disease
Identifieur interne : 000324 ( Pmc/Curation ); précédent : 000323; suivant : 000325Neural and behavioral substrates of subtypes of Parkinson’s disease
Auteurs : Ahmed Moustafa [États-Unis, Australie] ; Michele Poletti [Italie]Source :
- Frontiers in Systems Neuroscience ; 2013.
Abstract
Parkinson’s disease (PD) is a neurological disorder, associated with rigidity, bradykinesia, and resting tremor, among other motor symptoms. In addition, patients with PD also show cognitive and psychiatric dysfunction, including dementia, mild cognitive impairment (MCI), depression, hallucinations, among others. Interestingly, the occurrence of these symptoms—motor, cognitive, and psychiatric—vary among individuals, such that a subgroup of PD patients might show some of the symptoms, but another subgroup does not. This has prompted neurologists and scientists to subtype PD patients depending on the severity of symptoms they show. Neural studies have also mapped different motor, cognitive, and psychiatric symptoms in PD to different brain networks. In this review, we discuss the neural and behavioral substrates of most common subtypes of PD patients, that are related to the occurrence of: (a) resting tremor (vs. nontremor-dominant); (b) MCI; (c) dementia; (d) impulse control disorders (ICD); (e) depression; and/or (f) hallucinations. We end by discussing the relationship among subtypes of PD subgroups, and the relationship among motor, cognitive, psychiatric factors in PD.
Url:
DOI: 10.3389/fnsys.2013.00117
PubMed: 24399940
PubMed Central: 3872046
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Neural and behavioral substrates of subtypes of Parkinson’s disease</title><author><name sortKey="Moustafa, Ahmed A" sort="Moustafa, Ahmed A" uniqKey="Moustafa A" first="Ahmed" last="Moustafa">Ahmed Moustafa</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Veterans Affairs, New Jersey Health Care System</institution><country>East Orange, NJ, USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Social Sciences and Psychology and Marcs Institute for Brain and Behaviour, University of Western Sydney</institution><country>Sydney, NSW, Australia</country></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author><author><name sortKey="Poletti, Michele" sort="Poletti, Michele" uniqKey="Poletti M" first="Michele" last="Poletti">Michele Poletti</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Mental Health and Pathological Addiction, AUSL of Reggio Emilia</institution><country>Reggio Emilia, Italy</country></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24399940</idno><idno type="pmc">3872046</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3872046</idno><idno type="RBID">PMC:3872046</idno><idno type="doi">10.3389/fnsys.2013.00117</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">000324</idno><idno type="wicri:Area/Pmc/Curation">000324</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Neural and behavioral substrates of subtypes of Parkinson’s disease</title><author><name sortKey="Moustafa, Ahmed A" sort="Moustafa, Ahmed A" uniqKey="Moustafa A" first="Ahmed" last="Moustafa">Ahmed Moustafa</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Veterans Affairs, New Jersey Health Care System</institution><country>East Orange, NJ, USA</country></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>School of Social Sciences and Psychology and Marcs Institute for Brain and Behaviour, University of Western Sydney</institution><country>Sydney, NSW, Australia</country></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author><author><name sortKey="Poletti, Michele" sort="Poletti, Michele" uniqKey="Poletti M" first="Michele" last="Poletti">Michele Poletti</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Mental Health and Pathological Addiction, AUSL of Reggio Emilia</institution><country>Reggio Emilia, Italy</country></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author></analytic><series><title level="j">Frontiers in Systems Neuroscience</title><idno type="e-ISSN">1662-5137</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>Parkinson’s disease (PD) is a neurological disorder, associated with rigidity, bradykinesia, and resting tremor, among other motor symptoms. In addition, patients with PD also show cognitive and psychiatric dysfunction, including dementia, mild cognitive impairment (MCI), depression, hallucinations, among others. Interestingly, the occurrence of these symptoms—motor, cognitive, and psychiatric—vary among individuals, such that a subgroup of PD patients might show some of the symptoms, but another subgroup does not. This has prompted neurologists and scientists to subtype PD patients depending on the severity of symptoms they show. Neural studies have also mapped different motor, cognitive, and psychiatric symptoms in PD to different brain networks. In this review, we discuss the neural and behavioral substrates of most common subtypes of PD patients, that are related to the occurrence of: (a) resting tremor (vs. nontremor-dominant); (b) MCI; (c) dementia; (d) impulse control disorders (ICD); (e) depression; and/or (f) hallucinations. 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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">24399940</article-id><article-id pub-id-type="pmc">3872046</article-id><article-id pub-id-type="doi">10.3389/fnsys.2013.00117</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>Neural and behavioral substrates of subtypes of Parkinson’s disease</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Moustafa</surname><given-names>Ahmed A.</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="author-notes" rid="fn001"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Poletti</surname><given-names>Michele</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Department of Veterans Affairs, New Jersey Health Care System</institution><country>East Orange, NJ, USA</country></aff><aff id="aff2"><sup>2</sup><institution>School of Social Sciences and Psychology and Marcs Institute for Brain and Behaviour, University of Western Sydney</institution><country>Sydney, NSW, Australia</country></aff><aff id="aff3"><sup>3</sup><institution>Department of Mental Health and Pathological Addiction, AUSL of Reggio Emilia</institution><country>Reggio Emilia, Italy</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Alon Korngreen, Bar-Ilan University, Israel</p></fn><fn fn-type="edited-by"><p>Reviewed by: Nicola B. Mercuri, University of Rome, Italy; Gabriella Santangelo, Second University of Naples, Italy</p></fn><corresp id="fn001">*Correspondence: Ahmed A. Moustafa, School of Social Sciences and Psychology and Marcs Institute for Brain and Behaviour, University of Western Sydney, Room no. 24.1.58, Locked Bag 1797, Sydney, NSW 2751, Australia e-mail: <email xlink:type="simple">a.moustafa@uws.edu.au</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>24</day><month>12</month><year>2013</year></pub-date><pub-date pub-type="collection"><year>2013</year></pub-date><volume>7</volume><elocation-id>117</elocation-id><history><date date-type="received"><day>15</day><month>10</month><year>2013</year></date><date date-type="accepted"><day>05</day><month>12</month><year>2013</year></date></history><permissions><copyright-statement>Copyright © 2013 Moustafa and Poletti.</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 (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>Parkinson’s disease (PD) is a neurological disorder, associated with rigidity, bradykinesia, and resting tremor, among other motor symptoms. In addition, patients with PD also show cognitive and psychiatric dysfunction, including dementia, mild cognitive impairment (MCI), depression, hallucinations, among others. Interestingly, the occurrence of these symptoms—motor, cognitive, and psychiatric—vary among individuals, such that a subgroup of PD patients might show some of the symptoms, but another subgroup does not. This has prompted neurologists and scientists to subtype PD patients depending on the severity of symptoms they show. Neural studies have also mapped different motor, cognitive, and psychiatric symptoms in PD to different brain networks. In this review, we discuss the neural and behavioral substrates of most common subtypes of PD patients, that are related to the occurrence of: (a) resting tremor (vs. nontremor-dominant); (b) MCI; (c) dementia; (d) impulse control disorders (ICD); (e) depression; and/or (f) hallucinations. We end by discussing the relationship among subtypes of PD subgroups, and the relationship among motor, cognitive, psychiatric factors in PD.</p></abstract><kwd-group><kwd>Parkinson’s disease</kwd><kwd>tremor</kwd><kwd>dementia</kwd><kwd>mild cognitive impairment</kwd><kwd>hallucinations</kwd><kwd>depression</kwd><kwd>impulse control disorders</kwd></kwd-group><counts><fig-count count="0"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="176"></ref-count><page-count count="11"></page-count><word-count count="10624"></word-count></counts></article-meta></front><body><sec id="s1"><title>Introduction</title><p>Parkinson’s disease (PD) is a neurodegenerative disorder characterized by motor (bradykinesia, rigidity and resting tremor) and non-motor symptoms, such as cognitive impairment, autonomic, affective and behavioral disturbances (Jankovic, <xref ref-type="bibr" rid="B69">2008</xref>). The complex clinical picture of motor and non-motor symptoms is not only different between PD patients, but is also changing along the course of disease progression in each patient. The neurodegenerative nature of PD and its pharmacological management are involved in this clinical heterogeneity. PD is characterized by a progressive widespread diffusion of the Lewy body neuropathology from subcortical to cortical structures (Braak et al., <xref ref-type="bibr" rid="B19">2003</xref>); therefore at different disease stages PD patients present different loads of Lewy body neuropathology and different involvements of subcortical and cortical structures. Moreover, drugs used to manage clinical symptoms, as dopaminergic drugs (Bonuccelli and Pavese, <xref ref-type="bibr" rid="B17">2006</xref>; Poewe et al., <xref ref-type="bibr" rid="B114">2010</xref>) have motor and non-motor effects that change along disease progression (Poletti and Bonuccelli, <xref ref-type="bibr" rid="B116">2013</xref>).</p><p>Classifications of PD into different subtypes have been proposed to reduce the heterogeneity of clinical features associated with PD, and thus better investigate their neural correlates and provide better treatment options. Two approaches are used to achieve these classifications: empirically assigned or data-driven (Marras and Lang, <xref ref-type="bibr" rid="B93">2013</xref>). Empirically assigned classifications of specific clinical motor and non-motor symptoms in PD patients (e.g., rigidity, cognitive impairment, psychosis, impulse control disorder (ICD), autonomic dysfunction) compare samples of patients with vs. without the investigated clinical symptom; for example, on the basis of the predominant motor symptoms as indicated by the Unified Parkinson’s Disease Rating Scale (UPDRS) motor subscores, PD patients were categorized into patients with predominant postural instability and gait difficulty and patients with predominant tremor (Jankovic et al., <xref ref-type="bibr" rid="B70">1990</xref>). On the other hand, the data-driven approach searches for variables that group together each subtype without a-priori hypothesis; for example the cluster analysis of Lewis et al. (<xref ref-type="bibr" rid="B89">2005</xref>) identified four subtypes of PD patients: (1) young onset; (2) non-tremor dominant with cognitive impairment and depression; (3) rapid progression without cognitive impairment; and (4) tremor dominant.</p><p>The empirically assigned and the data-driven classification approaches may identify partially overlapping subtypes (van Rooden et al., <xref ref-type="bibr" rid="B156">2010</xref>), as in the case of the motor subtypes proposed by Jankovic et al. (<xref ref-type="bibr" rid="B70">1990</xref>) and clusters proposed by Lewis et al. (<xref ref-type="bibr" rid="B89">2005</xref>). These approaches have been attempted for motor, cognitive and psychopathological features of PD patients, while, they have not been attempted on findings of neuropathological and neuroimaging assessments.</p><p>A recent comparison of the empirically assigned and data driven classification approaches (Marras and Lang, <xref ref-type="bibr" rid="B93">2013</xref>) underlined how the former has the advantages of small number of subtypes, ease of implementation and assignment of patients to one or another subtype; on the contrary clusters derived from the data-driven approach are inherently more complicated, incorporating more variables that are often not regularly measured in clinical practice, increasing the difficulty to assign some patients to subtypes.</p><p>Furthermore the empirically assigned classification is probably more informative on the pathophysiology of specific PD symptoms but it could also hamper a global view on complex clinical patterns of motor and non-motor symptoms that characterize PD patients. Since data driven subtypes reviewed elsewhere (van Rooden et al., <xref ref-type="bibr" rid="B156">2010</xref>), this review aims at presenting an overview of some of the main PD subtypes derived from the empirically assigned classification; we briefly present their neural and behavioral correlates to show how these subtypes may correlate with each other. For this purpose in the next sections we describe the following subtypes: motor (postural instability and gait difficulty vs. tremor) and non-motor symptoms (mild cognitive impairment (MCI) vs. dementia; with/without ICD, depression, or hallucinations). Next, we briefly discuss existing data on how these subtypes correlate with each other.</p></sec><sec id="s2"><title>Cognitive subtypes in PD: from mild cognitive impairment to dementia</title><p>Since the early clinical stages, PD patients present an increased risk of cognitive impairment, with prevalences of MCI ranging from 14.8–18.9% in newly diagnosed drug-naïve patients (Aarsland et al., <xref ref-type="bibr" rid="B2">2009</xref>, <xref ref-type="bibr" rid="B3">2010</xref>; Poletti et al., <xref ref-type="bibr" rid="B117">2012a</xref>,<xref ref-type="bibr" rid="B120">b</xref>), up to a 50% and 5 years after clinical diagnosis (Broeders et al., <xref ref-type="bibr" rid="B20">2013</xref>).</p><p>MCI may be diagnosed when a neuropsychological impairment is demonstrated by performances 1–2 standard deviations below appropriate norms in at least two tests of the same cognitive domain (MCI single domain; for example dysexecutive MCI when only the executive domain is impaired; amnestic MCI when only episodic memory is impaired) or in at least one test in two different cognitive domains (MCI multiple domains: for example executive and episodic memory domains or executive and visuospatial domains are impaired) and there is a preserved functional level in everyday activities, not considering difficulties related to the motor symptoms (Litvan et al., <xref ref-type="bibr" rid="B90">2012</xref>).</p><p>In the early clinical stage, cognitive impairment in PD is primarily characterized by deficits if executive functions, caused by loss of dopaminergic neurons in the nigrostriatal pathway (Kish et al., <xref ref-type="bibr" rid="B76">1988</xref>) and resulting in the reduction of dopamine levels in the striatum. This dopamine reduction negatively impacts the functioning of the dorsolateral frontostriatal loop (linking dorsolateral prefrontal cortex, dorsolateral caudate nucleus of the striatum, dorsomedial globus pallidus and thalamus), which is mainly involved in of executive functions such as working memory, planning and set-shifting (Alexander et al., <xref ref-type="bibr" rid="B5">1986</xref>) and dopaminergic drugs have a beneficial effects on these functions in the early stages of disease by impacting striatal dopamine levels (Cools, <xref ref-type="bibr" rid="B27">2006</xref>).</p><p>The presence of MCI since the early PD stages is associated not only with the frontostriatal deficit but also with an early involvement of parietal and occipital cortices (Pappata et al., <xref ref-type="bibr" rid="B110">2011</xref>); this finding have been consistently reported in patients with MCI by structural neuroimaging studies, detecting atrophic changes in a number of cortical regions, including occipital, parietal, medial temporal and prefrontal cortices (Song et al., <xref ref-type="bibr" rid="B148">2011</xref>; Weintraub et al., <xref ref-type="bibr" rid="B172">2011a</xref>; Lee et al., <xref ref-type="bibr" rid="B80">2012a</xref>) and cortical hypometabolism in frontostriatal loops and parietal and occipital regions (Nobili et al., <xref ref-type="bibr" rid="B105">2011</xref>; Ekman et al., <xref ref-type="bibr" rid="B40">2012</xref>; Garcia-Garcia et al., <xref ref-type="bibr" rid="B54">2012</xref>; Nagano-Saito et al., <xref ref-type="bibr" rid="B103">2013</xref>).</p><p>Advanced PD stages, usually presenting dementia in 75–80% of patients (Aarsland et al., <xref ref-type="bibr" rid="B1">2003</xref>; Williams-Gray et al., <xref ref-type="bibr" rid="B176">2013</xref>), are characterized by widespread cortical and subcortical atrophic changes (Burton et al., <xref ref-type="bibr" rid="B23">2004</xref>; Nagano-Saito et al., <xref ref-type="bibr" rid="B104">2005</xref>; Summerfield et al., <xref ref-type="bibr" rid="B152">2005</xref>; Beyer et al., <xref ref-type="bibr" rid="B15">2007</xref>; Weintraub et al., <xref ref-type="bibr" rid="B173">2011b</xref>; Melzer et al., <xref ref-type="bibr" rid="B96">2012</xref>) and more severe temporal, parietal and occipital hypometabolism in comparison with MCI patients (Garcia-Garcia et al., <xref ref-type="bibr" rid="B54">2012</xref>).</p><p>In sum, the cognitive profile of PD is usually characterized by an early executive impairment, a sign of nigrostriatal degeneration, and subsequently by impairment of visuospatial functions, memory and/or language, a sign of cortical diffusion of Lewy body pathology, evidenced by cortical atrophy and hypometabolismml: this second feature in particular, in comparison with the first one, is associated with an increased risk of developing MCI and subsequently dementia (Jellinger, <xref ref-type="bibr" rid="B71">2013</xref>; Kehagia et al., <xref ref-type="bibr" rid="B74">2013</xref>).</p></sec><sec id="s3"><title>Tremor vs. non-tremor in PD</title><p>As discussed above, PD involves a spectrum of motor symptoms that include akinesia, bradykinesia, and resting tremor, among others. Few studies categorize the patients into different subgroups, depending on the motor symptoms they present. This usually involves dividing the patients into a tremor-dominant and non-tremor-dominant groups, with the latter is either patients with predominant akinesia, bradykinesia, or postural instability and gait symptoms (Jankovic et al., <xref ref-type="bibr" rid="B70">1990</xref>; Zaidel et al., <xref ref-type="bibr" rid="B180">2009</xref>; Mure et al., <xref ref-type="bibr" rid="B102">2011</xref>; Schillaci et al., <xref ref-type="bibr" rid="B134">2011</xref>; Lee et al., <xref ref-type="bibr" rid="B81">2012b</xref>; Wylie et al., <xref ref-type="bibr" rid="B177">2012</xref>). Bradykinesia, and postural instability and gait dysfunction are more common in patients with a rapid disease progression compared with PD patients with a slower progression rate (Jankovic et al., <xref ref-type="bibr" rid="B70">1990</xref>).</p><p>Studies have generally shown that PD patients with tremor are usually less cognitively impaired than PD patients with akinesia or gait dysfunction (Burn et al., <xref ref-type="bibr" rid="B22">2006</xref>; Lyros et al., <xref ref-type="bibr" rid="B91">2008</xref>; Oh et al., <xref ref-type="bibr" rid="B107">2009</xref>; Domellof et al., <xref ref-type="bibr" rid="B38">2011</xref>). For example, Vakil and Herishanu-Naaman (<xref ref-type="bibr" rid="B155">1998</xref>) found that tremor-dominant patients are less impaired at procedural learning tasks than akinesia-dominant patients. Studies also showed that PD patients with tremor are less impaired than PD patients with other motor subtypes on perceptual tasks, including peripheral vision and visual processing speed (Seichepine et al., <xref ref-type="bibr" rid="B138">2011</xref>). Interestingly, we also found that akinesia-dominant patients were more impaired than tremor-dominant patients at various working memory (Moustafa et al., <xref ref-type="bibr" rid="B101">2013a</xref>) and learning (Moustafa et al., <xref ref-type="bibr" rid="B100">2013b</xref>) measures. Prior studies have reported significant correlations between bradykinesia severity and cognitive measures in newly diagnosed PD patients (Domellof et al., <xref ref-type="bibr" rid="B38">2011</xref>; Poletti et al., <xref ref-type="bibr" rid="B120">2012b</xref>). For example, Domellof et al. (<xref ref-type="bibr" rid="B38">2011</xref>) found that bradykinesia scores correlate with Wisconsin Card Sorting Test, digit span, and Trail Making Test performance. Along the same lines, (Poletti et al., <xref ref-type="bibr" rid="B117">2012a</xref>,<xref ref-type="bibr" rid="B120">b</xref>) reported a correlation between bradykinesia and Trail Making Test as well as achieved category in the Modified Card Sorting Test.</p><p>This pattern of results also applies to psychiatric symptoms. One neuropsychological study found that unlike tremor-dominant patients, PD patients with non-tremor symptoms show increased rates of depression, apathy, and hallucinations (Reijnders et al., <xref ref-type="bibr" rid="B127">2009</xref>). Further, neuropsychological studies found depression is more common in akinesia-dominant patients than tremor patients (Starkstein et al., <xref ref-type="bibr" rid="B149">1998</xref>). Recently, a neuropsychological study found that unlike patients with dominant tremor symptoms, patients with postural instability and gait deficits show more impulsive behavior (Wylie et al., <xref ref-type="bibr" rid="B177">2012</xref>). Clinical and neuropsychological studies also suggest that the severity of akinesia symptoms is a risk factor for the development of dementia and MCI in PD patients (Poletti et al., <xref ref-type="bibr" rid="B118">2011</xref>; Poletti and Bonuccelli, <xref ref-type="bibr" rid="B116">2013</xref>).</p><p>For more than two decades, it has been shown that patient with dominant akinesia show more neural damage than PD patients with dominant tremor (Paulus and Jellinger, <xref ref-type="bibr" rid="B111">1991</xref>). Recent neuropsychological studies showed that non-tremor symptoms in PD, including postural instability and gait deficits, are associated with grey matter degeneration (Rosenberg-Katz et al., <xref ref-type="bibr" rid="B129">2013</xref>). Other neuropsychological and animal studies suggest that akinesia and bradykinesia are arguably associated with basal ganglia (and corticostriatal circuits) dysfunction, while tremor is perhaps associated with cerebellar, thalamic, and subthalamic nucleus abnormalities (Kassubek et al., <xref ref-type="bibr" rid="B73">2002</xref>; Probst-Cousin et al., <xref ref-type="bibr" rid="B123">2003</xref>; Weinberger et al., <xref ref-type="bibr" rid="B170">2009</xref>; Zaidel et al., <xref ref-type="bibr" rid="B180">2009</xref>; Mure et al., <xref ref-type="bibr" rid="B102">2011</xref>). For example, Schillaci et al. (<xref ref-type="bibr" rid="B134">2011</xref>) found that PD patients with akinesia and rigidity as the predominant symptoms have significantly more widespread dopamine loss in the striatum than PD patients with tremor as the predominant symptom(also see Eggers et al., <xref ref-type="bibr" rid="B39">2011</xref>). These results support a relationship between motor variables (including akinesia and bradykinesia) and cognitive performance in PD patients.</p></sec><sec id="s4"><title>Impulse control disorders in PD</title><p>Dopaminergic medications, especially some dopamine agonists, can trigger ICDs, such as hypersexuality, hobbyism, dopamine dysregulation syndrome, binge eating and pathological gambling, in a considerable subpopulation of PD patients (Dodd et al., <xref ref-type="bibr" rid="B37">2005</xref>; Voon et al., <xref ref-type="bibr" rid="B164">2007</xref>). It is also important to note that ICDs can be caused by other factors beside the administration of dopaminergic medications. For example, few studies reported the occurrence of ICDs in drug-naïve PD patients (Antonini et al., <xref ref-type="bibr" rid="B8">2011</xref>). Interestingly, studies also report that some PD patients present either with single or multiple ICDs, and that each of these subgroups have a different cognitive and neural profile (Vitale et al., <xref ref-type="bibr" rid="B160">2011</xref>). Further, few studies have investigated the prevalence and predictors of ICDs. For example, it was reported that alexithymia is a predictor of ICDs in PD patients (Goerlich-Dobre et al., <xref ref-type="bibr" rid="B57">2013</xref>). It was also found that frontal executive function is a predictor of the occurrence of pathological gambling (Santangelo et al., <xref ref-type="bibr" rid="B133">2009b</xref>).</p><p>Prior studies show that ICDs are observed more often in patients on D2 dopamine agonists (Weintraub et al., <xref ref-type="bibr" rid="B174">2006</xref>; Voon and Fox, <xref ref-type="bibr" rid="B161">2007</xref>) It is suggested that patients vulnerable to ICDs have a lower D2 receptor density, even before onset of PD (Dagher and Robbins, <xref ref-type="bibr" rid="B32">2009</xref>). The density of D2 receptors might further decreases in these vulnerable patients by overstimulation of ventral striatal D2 receptors in PD and increases the rate of ICDs in such vulnerable patients. Other studies suggest that binding to dopamine D3 receptors is responsible for the occurrence of ICDs (Vilas et al., <xref ref-type="bibr" rid="B159">2012</xref>). A recent study found that patients with ICDs were more likely to be on antidepressant medications and had more motor complications than those without ICDs (Mack et al., <xref ref-type="bibr" rid="B92">2013</xref>). In addition to dopaminergic medications, studies also show that ICDs can be caused by deep brain stimulation of the subthalamic nucleus (Frank et al., <xref ref-type="bibr" rid="B51">2007</xref>; Callesen et al., <xref ref-type="bibr" rid="B25">2013a</xref>; but also see Santangelo et al., <xref ref-type="bibr" rid="B130">2013</xref>). Studies also show that cognitive behavioral therapy can ameliorate ICDs in PD patients (Okai et al., <xref ref-type="bibr" rid="B108">2013</xref>).</p><p>ICDs in PD is also associated with cognitive and psychiatric symptoms. Unlike patients without ICDs, PD with ICDs show increased discounting in delay discounting tasks (Housden et al., <xref ref-type="bibr" rid="B67">2010</xref>; Voon et al., <xref ref-type="bibr" rid="B165">2010b</xref>; Leroi et al., <xref ref-type="bibr" rid="B87">2013</xref>), increased reward learning (Voon et al., <xref ref-type="bibr" rid="B162">2011</xref>), and impairment performing the Iowa gambling task (Gescheidt et al., <xref ref-type="bibr" rid="B55">2012</xref>). Studies have also shown that PD patients with ICDs are more impaired than patients without ICDs on working memory (Djamshidian et al., <xref ref-type="bibr" rid="B36">2010</xref>; Voon et al., <xref ref-type="bibr" rid="B163">2010a</xref>), but they did not differ on executive functioning (Siri et al., <xref ref-type="bibr" rid="B145">2010</xref>). A recent study also showed that PD patients with ICDs are more impaired at planning and set-shifting tasks than patients without ICDs (Vitale et al., <xref ref-type="bibr" rid="B160">2011</xref>), although the study did not include a healthy control group. Another study showed ICDs in PD are associated with executive dysfunction (Voon et al., <xref ref-type="bibr" rid="B165">2010b</xref>) and working memory impairment (Voon et al., <xref ref-type="bibr" rid="B162">2011</xref>). Further, it was found that PD patients with the hypersexuality subtype show more impairment on the Stroop task than patients with pathological gambling (Vitale et al., <xref ref-type="bibr" rid="B160">2011</xref>), suggesting that the different impulsive behaviors are associated with different behavioral, and potential neural, profile. Studies also found that ICDs in PD are associated with depression and irritability (Pontone et al., <xref ref-type="bibr" rid="B122">2006</xref>).</p><p>Neural studies have implicated cortical and subcortical structure for the occurrence of ICDs in PD. Many studies show that the underlying neural substrates of ICDs in PD are mostly the ventral striatum, including the nucleus accumbens (Cools et al., <xref ref-type="bibr" rid="B29">2007</xref>; Dagher and Robbins, <xref ref-type="bibr" rid="B32">2009</xref>; Steeves et al., <xref ref-type="bibr" rid="B150">2009</xref>; Voon et al., <xref ref-type="bibr" rid="B163">2010a</xref>). For example, using PET imaging, Steeves et al. (<xref ref-type="bibr" rid="B150">2009</xref>) found greater decreases in binding potential in the ventral striatum in PD patients on dopamine agonists with pathological gambling. Additionally, (Voon et al., <xref ref-type="bibr" rid="B163">2010a</xref>,<xref ref-type="bibr" rid="B165">b</xref>) reported impaired dopamine signaling in ventral striatal blood oxygen level dependent (BOLD) in PD patients with ICDs. It has been suggested that restoration of dopamine transmission in the dorsal striatum might lead to overdosing of the ventral striatum which results in excessive dopamine receptor stimulation in the ventral striatum (Swainson et al., <xref ref-type="bibr" rid="B153">2000</xref>; Cools et al., <xref ref-type="bibr" rid="B28">2001</xref>) that induce ICDs in some subjects (Cools et al., <xref ref-type="bibr" rid="B181">2003</xref>; Dagher and Robbins, <xref ref-type="bibr" rid="B32">2009</xref>). A recent study showed that increase of striatal dopamine might lead to ICDs in PD (Voon et al., <xref ref-type="bibr" rid="B166">2013</xref>). Studies have also implicated the hippocampus in the occurrence of ICDs in PD (Calabresi et al., <xref ref-type="bibr" rid="B24">2013</xref>). Beside subcortical structures, neural studies have shown that patients with ICDs show dopamine reduction in the ventromedial prefrontal cortex (and nucleus accumbens) compared with those without ICDs (Lee et al., <xref ref-type="bibr" rid="B82">2013</xref>).</p></sec><sec id="s5"><title>Depression in PD</title><p>Depression is one of the most common non-motor symptoms in PD patients (Schrag et al., <xref ref-type="bibr" rid="B135">2007</xref>; Picillo et al., <xref ref-type="bibr" rid="B112">2009</xref>). It is estimated that roughly 40% of PD patients show depressive symptoms (Slaughter et al., <xref ref-type="bibr" rid="B146">2001</xref>; McDonald et al., <xref ref-type="bibr" rid="B95">2003</xref>; Leentjens, <xref ref-type="bibr" rid="B84">2004</xref>; Schrag et al., <xref ref-type="bibr" rid="B135">2007</xref>; clinical manifestations, etiology, and treatment of depression in PD). These depressive symptoms include social withdrawal and anhedonia (inability to experience pleasure). Depression in PD is often diagnozed as follows: patients with Beck Depression Inventory (BDI) score greater than 13/14 is considered in the depression group, while the others are in the non-depressed group (Leentjens et al., <xref ref-type="bibr" rid="B86">2000</xref>; Schrag et al., <xref ref-type="bibr" rid="B135">2007</xref>; Herzallah et al., <xref ref-type="bibr" rid="B65">2010</xref>). Furthermore, patients with major depressive disorder have a threefold higher risk to develop Parkinson’s later in life (Schuurman et al., <xref ref-type="bibr" rid="B137">2002</xref>). Like ICDs, it is well recognized that the incidence of depression among PD patients is much higher than among age-matched healthy participants (Cummings, <xref ref-type="bibr" rid="B31">1992</xref>; Veiga et al., <xref ref-type="bibr" rid="B157">2009</xref>). Selective serotonin reuptake inhibitors as well dopamine agonists, such as pramipexole and pergolide were shown to have antidepressant effects in PD depression (Picillo et al., <xref ref-type="bibr" rid="B112">2009</xref>).</p><p>Research has shown that depressive symptoms in PD have a negative impact on PD patients’ quality of life (Karlsen et al., <xref ref-type="bibr" rid="B72">1999</xref>; Schrag et al., <xref ref-type="bibr" rid="B136">2000</xref>). Studies also suggest depression in PD is associated with intellectual impairment and inattention (Mayeux et al., <xref ref-type="bibr" rid="B94">1981</xref>). Furthermore, depression in PD is associated with cognitive impairment (Kuzis et al., <xref ref-type="bibr" rid="B79">1997</xref>; Bader and Hell, <xref ref-type="bibr" rid="B9">1998</xref>; Errea and Ara, <xref ref-type="bibr" rid="B41">1999</xref>). Current studies in PD patients with depression largely focus on executive functioning, working memory, or memory (Kuzis et al., <xref ref-type="bibr" rid="B79">1997</xref>; Norman et al., <xref ref-type="bibr" rid="B106">2002</xref>; Kummer et al., <xref ref-type="bibr" rid="B78">2009</xref>; Santangelo et al., <xref ref-type="bibr" rid="B132">2009a</xref>). We also found that PD patients with depression were more impaired at learning tasks than PD patients without depression (Herzallah et al., <xref ref-type="bibr" rid="B65">2010</xref>).</p><p>It debated in the literature which mechanism contributes the occurrence of depression in PD, and whether depression symptoms are related to other psychiatric symptoms in PD, including apathy and anxiety. Further, it is debated whether depression in PD are related to dopamingeric dysfunction (Eskow Jaunarajs et al., <xref ref-type="bibr" rid="B43">2011</xref>). Some also argue that depressive symptoms in PD can be due to psychosocial factors or secondary to motor impairment (Aarsland et al., <xref ref-type="bibr" rid="B4">2012</xref>). Further, it is not clear which neurotransmitter system dysfunction contributes to PD depression, as many argue it could be related to dopaminergic, noradrenergic and/or serotonergic dysfunction (Aarsland et al., <xref ref-type="bibr" rid="B4">2012</xref>). It is also argued that depressive symptoms are more related to severity of motor symptoms in PD, particularly akinesia and bradykinesia (Reijnders et al., <xref ref-type="bibr" rid="B127">2009</xref>).</p><p>Neurobiological studies have also investigated the neural substrates of depression in PD. For example, imaging studies found that patients with PD who develop depression show structural changes that reflect dopaminergic dysfunction (Walter et al., <xref ref-type="bibr" rid="B168">2010</xref>). This is in agreement with case reports showing that deep brain stimulation of the substrania nigra can trigger depressive symptoms in PD (Bejjani et al., <xref ref-type="bibr" rid="B14">1999</xref>). Other neural studies suggest that while the primary neural dysfunction of PD is the dorsal striatum and its dopaminergic afferents (Kish et al., <xref ref-type="bibr" rid="B76">1988</xref>), depression in PD is associated with deficits in the ventral regions within striatum, including the nucleus accumbens (Remy et al., <xref ref-type="bibr" rid="B128">2005</xref>). Interestingly, Voon et al. (<xref ref-type="bibr" rid="B162">2011</xref>) argue that depression in PD (hypoactive state) is perhaps the antithesis of ICDs (hyperactive state). For example, research has shown that depression in PD can result from reduction of dopamine levels in the brain (Thobois et al., <xref ref-type="bibr" rid="B154">2010</xref>). This is contrasted from ICDs, which is often associated with increased dopamine levels, due mostly to the administration of dopamine agonist therapy (Voon et al., <xref ref-type="bibr" rid="B164">2007</xref>), but also see <xref ref-type="bibr" rid="B26">Callesen et al. (2013b)</xref> for evidence of association of impulsivity and depression in PD.</p><p>It is debated whether depression is caused by motor abnormalities or other neuropathology in PD. Imaging studies suggest that patients with depression who show structural abnormalities at the level of the substantia nigra are possibly at an elevated risk of later developing definite PD (Hoeppner et al., <xref ref-type="bibr" rid="B66">2009</xref>; Shen et al., <xref ref-type="bibr" rid="B140">2013</xref>). Nonmotor manifestations of PD (such as depression) are the earliest to appear (Simuni and Sethi, <xref ref-type="bibr" rid="B144">2008</xref>).</p></sec><sec id="s6"><title>Hallucinations in PD</title><p>Psychosis and visual and olfactory hallucinations occurs in approximately 20–30% of PD patients (Rabey, <xref ref-type="bibr" rid="B124">2009</xref>). In PD patients, visual hallucinations are more common than auditory or olfactory hallucinations (Diederich et al., <xref ref-type="bibr" rid="B35">2009</xref>). Psychosis is usually defined as involving one of the following symptoms: (a) illusions (misinterpretations of existing stimuli), hallucinations (defined as hallucinatory symptoms), and/or delusional symptoms. Psychosis in PD is usually confirmed using the Parkinson’s Psychosis Rating Scale (Friedberg et al., <xref ref-type="bibr" rid="B52">1998</xref>). Although it was previously found that the administration of dopaminergic drugs is the main cause of psychosis and hallucinations (Morgante et al., <xref ref-type="bibr" rid="B99">2012</xref>), recent studies additionally show that sleep disturbance, dementia, longer disease duration, and advanced stage of the disease, can also exacerbate psychotic symptoms in PD patients (Poewe, <xref ref-type="bibr" rid="B113">2003</xref>; Fenelon et al., <xref ref-type="bibr" rid="B47">2006</xref>; Fenelon, <xref ref-type="bibr" rid="B46">2008</xref>; Bannier et al., <xref ref-type="bibr" rid="B10">2012</xref>; Gibson et al., <xref ref-type="bibr" rid="B56">2013</xref>; Lee and Weintraub, <xref ref-type="bibr" rid="B83">2012</xref>; Morgante et al., <xref ref-type="bibr" rid="B99">2012</xref>). So unlike earlier clinical practice, a diagnosis of psychosis in PD is made when the patients have not had any dopaminergic medications. Among risk factors, one longitudinal study found that frontal dysfunction was also a predictor for the development of hallucinations in PD (Santangelo et al., <xref ref-type="bibr" rid="B131">2007</xref>).</p><p>Prior reports also suggest that hallucinations in PD patients are the main reason for admission to nursing homes (Diederich et al., <xref ref-type="bibr" rid="B35">2009</xref>). Psychosis in PD is also a risk factor for the occurrence of severe cognitive dysfunctions such as dementia (Factor et al., <xref ref-type="bibr" rid="B44">2003</xref>) and is associated with a diminished quality of life (Zahodne and Fernandez, <xref ref-type="bibr" rid="B179">2008</xref>; Rabey, <xref ref-type="bibr" rid="B124">2009</xref>). Prior studies have shown strong links between medication dosage, dementia, sleep disturbance, and psychosis in PD patients (Poewe, <xref ref-type="bibr" rid="B113">2003</xref>; Fenelon, <xref ref-type="bibr" rid="B46">2008</xref>; Bannier et al., <xref ref-type="bibr" rid="B10">2012</xref>; Gibson et al., <xref ref-type="bibr" rid="B56">2013</xref>).</p><p>There have been very few studies investigating the perceptual and cognitive correlates of psychosis in PD. Studies generally report cognitive and behavioral dysfunction in PD patients with psychosis than in patients without psychosis (Baydas et al., <xref ref-type="bibr" rid="B13">2005</xref>; Shine et al., <xref ref-type="bibr" rid="B143">2011</xref>). For example, studies have shown that PD patients with hallucinations are more impaired than PD patients without hallucination on recognition memory (Barnes et al., <xref ref-type="bibr" rid="B11">2003</xref>), executive function (Grossi et al., <xref ref-type="bibr" rid="B62">2005</xref>), frontal function (as measured using the frontal assessment battery), attentional processes (Meppelink et al., <xref ref-type="bibr" rid="B97">2008</xref>), and semantic fluency (Ramirez-Ruiz et al., <xref ref-type="bibr" rid="B125">2006</xref>). Specifically, Botha and Carr (<xref ref-type="bibr" rid="B18">2012</xref>) argue that the gating of irrelevant information to working memory is the mechanism underlying the occurrence of hallucinations. Prior studies have shown that hallucinations and psychosis in PD patients are associated with visual disturbance (Gallagher and Schrag, <xref ref-type="bibr" rid="B53">2012</xref>; Shine et al., <xref ref-type="bibr" rid="B142">2012</xref>). Behavioral differences between PD patients with and without psychosis can be observed during the performance of complex perceptual tasks (Shine et al., <xref ref-type="bibr" rid="B143">2011</xref>).</p><p>Prior studies suggest that hallucinations in PD patients can be due to either cortical or subcortical atrophy (Papapetropoulos et al., <xref ref-type="bibr" rid="B109">2006</xref>). Specifically, psychosis and hallucinations can stem from dysfunction to either the prefrontal cortex (Corlett et al., <xref ref-type="bibr" rid="B30">2007</xref>; Fletcher and Frith, <xref ref-type="bibr" rid="B48">2008</xref>), basal ganglia (Frank, <xref ref-type="bibr" rid="B50">2008</xref>; Howes et al., <xref ref-type="bibr" rid="B68">2012</xref>), or hippocampal region (Bogerts et al., <xref ref-type="bibr" rid="B16">1985</xref>; Weinberger, <xref ref-type="bibr" rid="B169">1999</xref>; Goldman and Mitchell, <xref ref-type="bibr" rid="B58">2004</xref>; Keri, <xref ref-type="bibr" rid="B75">2008</xref>; Grace, <xref ref-type="bibr" rid="B61">2010</xref>). Studies also report temporal lobe dysfunction in PD patients with visual hallucination (Botha and Carr, <xref ref-type="bibr" rid="B18">2012</xref>) and also with studies showing that early onset of hallucinations in PD patients is associated with dysfunction to the parahippocampus and inferior temporal cortex (Harding et al., <xref ref-type="bibr" rid="B63">2002</xref>). It was found that carrying the<italic> APOE</italic> ∈4 allele, which is associated with a small hippocampal volume in healthy older subjects (Alexopoulos et al., <xref ref-type="bibr" rid="B6">2011</xref>), is also a risk factor for the development of psychotic episodes in PD patients (de la Fuente-Fernandez et al., <xref ref-type="bibr" rid="B33">1999</xref>; Goldman et al., <xref ref-type="bibr" rid="B59">2004</xref>; Feldman et al., <xref ref-type="bibr" rid="B45">2006</xref>).</p></sec><sec id="s7"><title>Discussion: relationships among PD subtypes</title><p>In the previous sections we briefly reviewed some clinical subtypes of PD derived from the empirically assigned classification approach, that has the advantage of describing a small number of subtypes as regards specific clinical symptoms, with ease of implementation and assignment of patients to one or another subtype. On the other hand, because of inability to investigate relationships between subtypes, this approach does not provide a global view on complex clinical patterns of motor and non-motor symptoms.</p><p>This study aimed at reviewing most common PD subtypes derived from the empirically assigned classification to attempt a possible integration of them, through the identification of their possible relationships and their possible common neuropathological causes Indeed the clinical heterogeneity of PD lead to the classification in many subtypes as regards motor symptoms (e.g., postural instability and gait difficulty vs. tremor), cognition (MCI vs. dementia), psychopathological features (e.g., with ICD vs. without ICD; with psychosis vs. without psychosis), demographic features (e.g., young onset vs. late onset) and disease features (e.g., rapid progression vs. slow progression).</p><p>A first issue involves the relationship between motor subtypes and subtypes of non-motor symptoms, in particular of the cognitive and psychopathological domains. The non-tremor dominant motor subtype usually presents a more severe clinical pattern of non-motor symptoms in comparison to the tremor dominant subtype. Since the early untreated stages of PD, this subtype is characterized by a higher risk of MCI (Poletti et al., <xref ref-type="bibr" rid="B117">2012a</xref>) and longitudinally is associated with faster motor worsening (Vu et al., <xref ref-type="bibr" rid="B167">2012</xref>), cognitive decline (Burn et al., <xref ref-type="bibr" rid="B22">2006</xref>), and higher risk of developing dementia (Alves et al., <xref ref-type="bibr" rid="B7">2006</xref>; Sollinger et al., <xref ref-type="bibr" rid="B147">2010</xref>). This subtype is also associated with an increasing risk of developing psychopathological features, including affective features such as depression and alexithymia (Starkstein et al., <xref ref-type="bibr" rid="B149">1998</xref>; Reijnders et al., <xref ref-type="bibr" rid="B127">2009</xref>; Poletti et al., <xref ref-type="bibr" rid="B118">2011</xref>; Burn et al., <xref ref-type="bibr" rid="B21">2012</xref>) and psychotic features as hallucinations (Reijnders et al., <xref ref-type="bibr" rid="B127">2009</xref>). Conversely, the tremor dominant subtype appears to be characterized by a less severe clinical picture, with a slower progression of motor and cognitive symptoms and a lower risk of developing dementia and psychopathological features. The more severe clinical picture of the non-tremor dominant PD subtypes is due to a more severe Lewy body neuropathological load, as found at the post-mortem pathological examination (Selikhova et al., <xref ref-type="bibr" rid="B139">2009</xref>) and a more severe gray matter atrophy of cortical and limbic structures, as indicated by neuroimaging studies (Rosenberg-Katz et al., <xref ref-type="bibr" rid="B129">2013</xref>).</p><p>A second issue is regarding the relationship between cognitive subtypes and psychopathological subtypes. Few empirical findings are available from studies based on the classification of cognitive subtypes: only two studies directly compared cognitive subtypes of PD patients in relation to other non-motor subtypes. One study compared 54 cognitively preserved patients, 48 PD patients with MCI and 25 PD patients with dementia (Leroi et al., <xref ref-type="bibr" rid="B88">2012</xref>). Apathy was reported in almost 50% of MCI patients and PD patients with dementia, and was the only psychopathological manifestation differentiating cognitively preserved patients from MCI patients. Moreover the prevalence of psychotic symptoms as hallucinations and delusion progressively increased according to the degree of cognitive impairment (12.9% in cognitively preserved, 16.7% in MCI and 48% in PD patients with dementia). Another study compared different subtypes of MCI (Goldman et al., <xref ref-type="bibr" rid="B60">2012</xref>) in 128 PD patients with MCI; according to the cognitive profile patients were classified as non-amnestic single domain (47.7% of the sample), amnestic multiple domain (24.2%), amnestic single domain (18.8%), and non-amnestic single domain, and executive functions and visuospatial functions were the most frequently impaired domains. In comparison to other subtypes, non-amnestic multiple domain MCI patients showed most pronounced difficulties with postural instability and gait; subtypes did not differ in relation to age, PD duration, medication use, mood or behavioral disturbances.</p><p>These few findings are in agreement with the more robust empirical literature on the classification in psychopathological subtypes, suggesting that different subtypes may present different clinical patterns along the disease course. The subtype characterized by affective features (e.g., depression, apathy and anxiety) is very common at each disease stage, because it is associated with several non-disease specific risk factors (Leentjens et al., <xref ref-type="bibr" rid="B85">2013</xref>); moreover it is also associated with the executive impairment (Poletti et al., <xref ref-type="bibr" rid="B117">2012a</xref>), and it is only partially modified by dopaminergic therapies (Eskow Jaunarajs et al., <xref ref-type="bibr" rid="B43">2011</xref>).</p><p>Different patterns characterize psychotic features as hallucinations and delusions. Hallucinations may be present in patients with MCI (Shin et al., <xref ref-type="bibr" rid="B141">2012</xref>; Hepp et al., <xref ref-type="bibr" rid="B64">2013</xref>) but are particularly prevalent in advanced PD stages, in association with dementia (Rana et al., <xref ref-type="bibr" rid="B126">2012</xref>) and with cortical atrophy at neuroimaging (Papapetropoulos et al., <xref ref-type="bibr" rid="B109">2006</xref>). Delusions also may be associated with hallucinations and dementia in advanced patients but may be present in isolation in cognitively preserved patients, probably due to the interaction between individual susceptibility (as psychiatric familial history) and dopaminergic therapy (Poletti et al., <xref ref-type="bibr" rid="B117">2012a</xref>).</p><p>ICD are more in common in patients without dementia than in patients with dementia (9.6% vs. 3.8% in a recent cross-sectional study: Poletti et al., <xref ref-type="bibr" rid="B121">2013</xref>). However, an impairment of both orbitofrontal and dorsolateral executive functions may represent a risk factor (Poletti and Bonuccelli, <xref ref-type="bibr" rid="B115">2012</xref>) and probably interplays with individual (premorbid level of impulsivity), pharmacological (dopamine agonist therapy) and disease related (striatal dopaminergic alteration) risk factors (Dagher and Robbins, <xref ref-type="bibr" rid="B32">2009</xref>).</p><p>A controversial issue involving motor, cognitive and psychopathological PD subtypes regards the possible influence of the side of motor onset. Empirical findings principally involve cognition: the side of motor onset does not influence cognition in newly diagnosed untreated patients (Erro et al., <xref ref-type="bibr" rid="B42">2013</xref>; Poletti et al., <xref ref-type="bibr" rid="B119">2013</xref>); in patients “on” dopaminergic therapy a right-side motor symptom predominance is typically associated with difficulties in tasks of language and verbal memory, whereas a left-side motor symptom predominance is typically associated with difficulties in visuospatial tasks (Verreyt et al., <xref ref-type="bibr" rid="B158">2011</xref>). More heterogeneous and controversial are findings on the role of the side of motor onset on motor subtypes (e.g., Stewart et al., <xref ref-type="bibr" rid="B151">2009</xref>; Baumann et al., <xref ref-type="bibr" rid="B12">2013</xref>) and especially on psychopathological subtypes (e.g., Foster et al., <xref ref-type="bibr" rid="B49">2011</xref>; Dewey et al., <xref ref-type="bibr" rid="B34">2012</xref>), therefore more empirical studies are needed on this issue.</p><p>Further empirical studies are also needed on other clinical features that have been scarcely investigated in relation to motor, cognitive and psychopathological subtypes. For example, data driven classification methods (van Rooden et al., <xref ref-type="bibr" rid="B156">2010</xref>) suggested that PD patients could be also classified as “rapid disease progression” vs. “slow disease progression” or according to age of PD onset (e.g., young vs. late onset); in this perspective these features could be investigated by studies based on empirically assigned classifications. Moreover also other features suggested by empirically assigned classifications, as freezing of gait and autonomic dysfunctions, should be investigated in relation to motor, cognitive and psychopathological subtypes.</p><p>In sum, all these psychopathological subtypes may be present in all disease stages, and the presence of cognitive impairment represents a risk factor for their occurrence. Overall, PD is a heterogeneous disorder encompassing many subtypes along motor, cognitive, and psychiatric dimensions. Further, as discussed here, some of these subtypes are related (e.g., isolated delusions and ICD are more common in patients without dementia while hallucinations are more common in patients with dementia).</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><ack><p>This Research is partially supported by a 2013 internal UWS Research Grant Scheme award P00021210 to Ahmed A. Moustafa.</p></ack><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Aarsland</surname><given-names>D.</given-names></name><name><surname>Andersen</surname><given-names>K.</given-names></name><name><surname>Larsen</surname><given-names>J. 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