{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,18]],"date-time":"2026-07-18T04:42:03Z","timestamp":1784349723593,"version":"3.55.0"},"reference-count":101,"publisher":"Public Library of Science (PLoS)","issue":"5","license":[{"start":{"date-parts":[[2022,5,4]],"date-time":"2022-05-04T00:00:00Z","timestamp":1651622400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100008982","name":"National Science Foundation","doi-asserted-by":"publisher","award":["Graduate Research Fellowship #DGE-1746060"],"award-info":[{"award-number":["Graduate Research Fellowship #DGE-1746060"]}],"id":[{"id":"10.13039\/501100008982","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["University of Arizona\u2019s Initiative for Maximizing Student Development R25 GM 062584"],"award-info":[{"award-number":["University of Arizona\u2019s Initiative for Maximizing Student Development R25 GM 062584"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007899","name":"University of Arizona","doi-asserted-by":"crossref","award":["BIO5 Accelerate for Success, Core Facilities Pilot Program"],"award-info":[{"award-number":["BIO5 Accelerate for Success, Core Facilities Pilot Program"]}],"id":[{"id":"10.13039\/100007899","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100007899","name":"University of Arizona","doi-asserted-by":"crossref","award":["Marshall Foundation Dissertation Scholarship"],"award-info":[{"award-number":["Marshall Foundation Dissertation Scholarship"]}],"id":[{"id":"10.13039\/100007899","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100007899","name":"university of arizona","doi-asserted-by":"crossref","award":["Undergraduate Biology Research Program, the Border Latino and American Indian Summer Exposure to Research program, the Neuroscience and Cognitive Science Program, and the Honors College"],"award-info":[{"award-number":["Undergraduate Biology Research Program, the Border Latino and American Indian Summer Exposure to Research program, the Neuroscience and Cognitive Science Program, and the Honors College"]}],"id":[{"id":"10.13039\/100007899","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R21NS123512"],"award-info":[{"award-number":["R21NS123512"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Deterioration in the quality of a person\u2019s voice and speech is an early marker of Parkinson\u2019s disease (PD). In humans, the neural circuit that supports vocal motor control consists of a cortico-basal ganglia-thalamo-cortico loop. The basal ganglia regions, striatum and globus pallidus, in this loop play a role in modulating the acoustic features of vocal behavior such as loudness, pitch, and articulatory rate. In PD, this area is implicated in pathogenesis. In animal models of PD, the accumulation of toxic aggregates containing the neuronal protein alpha-synuclein (\u03b1syn) in the midbrain and striatum result in limb and vocal motor impairments. It has been challenging to study vocal impairments given the lack of well-defined cortico-basal ganglia circuitry for vocalization in rodent models. Furthermore, whether deterioration of voice quality early in PD is a direct result of \u03b1syn-induced neuropathology is not yet known. Here, we take advantage of the well-characterized vocal circuits of the adult male zebra finch songbird to experimentally target a song-dedicated pathway, the anterior forebrain pathway, using an adeno-associated virus expressing the human wild-type \u03b1syn gene,<jats:italic>SNCA<\/jats:italic>. We found that overexpression of \u03b1syn in this pathway coincides with higher levels of insoluble, monomeric \u03b1syn compared to control finches. Impairments in song production were also detected along with shorter and poorer quality syllables, which are the most basic unit of song. These vocal changes are similar to the vocal abnormalities observed in individuals with PD.<\/jats:p>","DOI":"10.1371\/journal.pone.0265604","type":"journal-article","created":{"date-parts":[[2022,5,4]],"date-time":"2022-05-04T17:26:02Z","timestamp":1651685162000},"page":"e0265604","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":16,"title":["Vocal changes in a zebra finch model of Parkinson\u2019s disease characterized by alpha-synuclein overexpression in the song-dedicated anterior forebrain pathway"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3760-7370","authenticated-orcid":true,"given":"Cesar A.","family":"Medina","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eddie","family":"Vargas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie J.","family":"Munger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0371-0342","authenticated-orcid":true,"given":"Julie E.","family":"Miller","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,5,4]]},"reference":[{"key":"pone.0265604.ref001","article-title":"Neuropathology and neurochemistry of nonmotor symptoms in Parkinson\u2019s disease","author":"I. Ferrer","year":"2011","journal-title":"Parkinson\u2019s Disease"},{"key":"pone.0265604.ref002","article-title":"Classic and new animal models of Parkinson\u2019s disease","author":"J. Blesa","year":"2012","journal-title":"J Biomed Biotech"},{"issue":"5321","key":"pone.0265604.ref003","doi-asserted-by":"crossref","first-page":"2045","DOI":"10.1126\/science.276.5321.2045","article-title":"Mutation in the \u03b1-synuclein gene identified in families with Parkinson\u2019s disease","volume":"276","author":"M. H. Polymeropoulos","year":"1997","journal-title":"Science"},{"issue":"6645","key":"pone.0265604.ref004","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1038\/42166","article-title":"\u03b1-Synuclein in Lewy bodies","volume":"388","author":"M. G. Spillantini","year":"1997","journal-title":"Nature"},{"issue":"4","key":"pone.0265604.ref005","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1152\/physrev.00022.2010","article-title":"What genetics tells us about the causes and mechanisms of Parkinson\u2019s disease","volume":"91","author":"O. Corti","year":"2011","journal-title":"Physiological Reviews"},{"issue":"3","key":"pone.0265604.ref006","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1097\/MOO.0b013e3282febd3a","article-title":"Speech and swallowing disorders in Parkinson disease","volume":"16","author":"S. Sapir","year":"2008","journal-title":"Current Opin in Otolaryngology & Head and Neck Surgery"},{"issue":"4","key":"pone.0265604.ref007","first-page":"1330","article-title":"Multiple factors are involved in the dysarthria associated with Parkinson\u2019s disease: a review with implications for clinical practice and research","volume":"57","author":"S. Sapir","year":"2014","journal-title":"JSLHR"},{"issue":"4","key":"pone.0265604.ref008","first-page":"631","article-title":"Clear Speech Variants: An acoustic study in Parkinson\u2019s Disease","volume":"59","author":"J. Lam","year":"2016","journal-title":"JSLHR"},{"issue":"1","key":"pone.0265604.ref009","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.bandc.2004.05.002","article-title":"Variability in fundamental frequency during speech in prodromal and incipient Parkinson\u2019s disease: A longitudinal case study","volume":"56","author":"B. Harel","year":"2004","journal-title":"Brain and Cognition"},{"issue":"5","key":"pone.0265604.ref010","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1002\/mds.22430","article-title":"Progression of dysprosody in Parkinson\u2019s disease over time\u2014a longitudinal study","volume":"24","author":"S. Skodda","year":"2009","journal-title":"Movement Disorders"},{"issue":"No. 03","key":"pone.0265604.ref011","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1055\/s-0033-1358367","article-title":"Early identification and treatment of communication and swallowing deficits in Parkinson disease","volume":"Vol. 34","author":"M. R. Ciucci","year":"2013","journal-title":"Sem in Speech and Language"},{"issue":"3","key":"pone.0265604.ref012","doi-asserted-by":"crossref","first-page":"2171","DOI":"10.1121\/1.4816541","article-title":"Imprecise vowel articulation as a potential early marker of Parkinson\u2019s disease: Effect of speaking task","volume":"134","author":"J. Rusz","year":"2013","journal-title":"JASA"},{"issue":"7","key":"pone.0265604.ref013","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1002\/mds.21996","article-title":"Speech rate and rhythm in Parkinson\u2019s disease","volume":"23","author":"S. Skodda","year":"2008","journal-title":"Movement disorders: official journal of the Movement Disorder Society"},{"key":"pone.0265604.ref014","unstructured":"Rusz, J., Cmejla, R., Ruzickova, H., Klempir, J., Majerova, V., Picmausova, J. et al. Acoustic markers of speech degradation in early untreated Parkinson\u2019s disease. European Acoustics Association. 2011; ISBN: 978-84-694-1520-7, ISSN: 221-376."},{"key":"pone.0265604.ref015","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1016\/j.bandl.2015.04.007","article-title":"Differences in early speech patterns between Parkinson variant of multiple system atrophy and Parkinson\u2019s disease","volume":"147","author":"Y. E. Huh","year":"2015","journal-title":"Brain and Lang"},{"issue":"7","key":"pone.0265604.ref016","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1016\/j.nrleng.2014.12.014","article-title":"Speech rate in Parkinson\u2019s disease: A controlled study","volume":"31","author":"F. Mart\u00ednez-S\u00e1nchez","year":"2016","journal-title":"Neurolog\u00eda (English Edition)"},{"key":"pone.0265604.ref017","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.bandl.2017.05.001","article-title":"Longitudinal decline in speech production in Parkinson\u2019s disease spectrum disorders","volume":"171","author":"S. Ash","year":"2017","journal-title":"Brain and Lang"},{"issue":"2","key":"pone.0265604.ref018","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.bbr.2007.02.020","article-title":"Qualitative changes in ultrasonic vocalization in rats after unilateral dopamine depletion or haloperidol: a preliminary study","volume":"182","author":"M. R. Ciucci","year":"2017","journal-title":"Behav Brain Res"},{"issue":"2","key":"pone.0265604.ref019","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1037\/a0014593","article-title":"Reduction of dopamine synaptic activity: degradation of 50-kHz ultrasonic vocalization in rats","volume":"123","author":"M. R. Ciucci","year":"2009","journal-title":"Behav Neurosci"},{"key":"pone.0265604.ref020","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/j.bbr.2015.05.042","article-title":"Relationships among rat ultrasonic vocalizations, behavioral measures of striatal dopamine loss, and striatal tyrosine hydroxylase immunoreactivity at acute and chronic time points following unilateral 6-hydroxydopamine-induced dopamine depletion","volume":"291","author":"L. M. Grant","year":"2015a","journal-title":"Behav Brain Res"},{"issue":"11","key":"pone.0265604.ref021","doi-asserted-by":"crossref","first-page":"1713","DOI":"10.1002\/jnr.23625","article-title":"Evidence for early and progressive ultrasonic vocalization and oromotor deficits in a PINK1 gene knockout rat model of Parkinson\u2019s disease","volume":"93","author":"L. M. Grant","year":"2015b","journal-title":"J Neurosci Res"},{"key":"pone.0265604.ref022","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.neuroscience.2018.02.027","article-title":"Quantitative analysis of catecholamines in the Pink1\u2212\/\u2212 rat model of early-onset Parkinson\u2019s disease","volume":"379","author":"C. A. Kelm-Nelson","year":"2018","journal-title":"Neurosci"},{"issue":"6","key":"pone.0265604.ref023","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1007\/s00455-018-9896-5","article-title":"Pink1\u2212\/\u2212 rats show early-onset swallowing deficits and correlative brainstem pathology","volume":"33","author":"K. P. Cullen","year":"2018","journal-title":"Dysphagia"},{"issue":"5","key":"pone.0265604.ref024","first-page":"1326","article-title":"Laryngeal muscle biology in the Pink1\u2212\/\u2212 rat model of Parkinson disease","volume":"126","author":"T. J. Glass","year":"2019","journal-title":"JApplied Physiol"},{"issue":"8","key":"pone.0265604.ref025","doi-asserted-by":"crossref","first-page":"e0220734","DOI":"10.1371\/journal.pone.0220734","article-title":"Intervention changes acoustic peak frequency and mesolimbic neurochemistry in the Pink1-\/-rat model of Parkinson disease","volume":"14","author":"S. A. Stevenson","year":"2019","journal-title":"PLOS ONE"},{"issue":"11","key":"pone.0265604.ref026","doi-asserted-by":"crossref","first-page":"e81426","DOI":"10.1371\/journal.pone.0081426","article-title":"Morphological and behavioral impact of AAV2\/5-mediated overexpression of human wildtype \u03b1-synuclein in the rat nigrostriatal system","volume":"8","author":"S. E. Gombash","year":"2013","journal-title":"PLOS ONE"},{"issue":"2","key":"pone.0265604.ref027","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1037\/a0035965","article-title":"Vocalization deficits in mice over-expressing \u03b1-synuclein, a model of pre-manifest Parkinson\u2019s disease","volume":"128","author":"L. M. Grant","year":"2014","journal-title":"Behav Neurosci"},{"key":"pone.0265604.ref028","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/j.nbd.2015.06.003","article-title":"Intrastriatal injection of pre-formed mouse \u03b1-synuclein fibrils into rats triggers \u03b1-synuclein pathology and bilateral nigrostriatal degeneration","volume":"82","author":"K. L. Paumier","year":"2015","journal-title":"Neurobiol. Dis"},{"issue":"7","key":"pone.0265604.ref029","doi-asserted-by":"crossref","first-page":"925","DOI":"10.3390\/brainsci11070925","article-title":"Rat Models Of Vocal Deficits in Parkinson\u2019s Disease","volume":"11","author":"M.D. Krasko","year":"2021","journal-title":"Brain Sciences"},{"issue":"3","key":"pone.0265604.ref030","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1155\/1999\/327643","article-title":"Speech impairment in a large sample of patients with Parkinson\u2019s disease","volume":"11","author":"A. K. Ho","year":"1999","journal-title":"Behav Neurol"},{"issue":"11","key":"pone.0265604.ref031","doi-asserted-by":"crossref","first-page":"1617","DOI":"10.1038\/nn.4133","article-title":"Human mutant huntingtin disrupts vocal learning in transgenic songbirds","volume":"18","author":"W. C. Liu","year":"2015","journal-title":"Nature Neurosci"},{"key":"pone.0265604.ref032","article-title":"Dopamine regulation of human speech and bird song: A critical review","author":"K. Simonyan","year":"2012","journal-title":"Brain and Lang"},{"issue":"6215","key":"pone.0265604.ref033","doi-asserted-by":"crossref","first-page":"1256846","DOI":"10.1126\/science.1256846","article-title":"Convergent transcriptional specializations in the brains of humans and song-learning birds","volume":"346","author":"A. R. Pfenning","year":"2014","journal-title":"Science"},{"issue":"1684","key":"pone.0265604.ref034","doi-asserted-by":"crossref","first-page":"20150056","DOI":"10.1098\/rstb.2015.0056","article-title":"Brain evolution by brain pathway duplication","volume":"370","author":"M. Chakraborty","year":"2015","journal-title":"Phil. Trans. R. Soc. B"},{"issue":"3","key":"pone.0265604.ref035","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1538\/expanim.15-0008","article-title":"Songbird: a unique animal model for studying the molecular basis of disorders of vocal development and communication","volume":"64","author":"C. Mori","year":"2015","journal-title":"Experimental Animals"},{"issue":"13","key":"pone.0265604.ref036","doi-asserted-by":"crossref","first-page":"3152","DOI":"10.1523\/JNEUROSCI.5589-03.2004","article-title":"Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction","volume":"24","author":"I. Teramitsu","year":"2004","journal-title":"J Neurosci"},{"issue":"13","key":"pone.0265604.ref037","doi-asserted-by":"crossref","first-page":"3164","DOI":"10.1523\/JNEUROSCI.4369-03.2004","article-title":"FoxP2 expression in avian vocal learners and non-learners","volume":"24","author":"S. Haesler","year":"2004","journal-title":"J Neurosci"},{"issue":"12","key":"pone.0265604.ref038","doi-asserted-by":"crossref","first-page":"e321","DOI":"10.1371\/journal.pbio.0050321","article-title":"Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X","volume":"5","author":"S. Haesler","year":"2007","journal-title":"PLOS Biol"},{"issue":"11","key":"pone.0265604.ref039","doi-asserted-by":"crossref","first-page":"1995","DOI":"10.1002\/cne.22318","article-title":"Language-related Cntnap2 gene is differentially expressed in sexually dimorphic song nuclei essential for vocal learning in songbirds","volume":"518","author":"S. C. Panaitof","year":"2010","journal-title":"J Comp Neurol"},{"issue":"1","key":"pone.0265604.ref040","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1002\/cne.23394","article-title":"Distribution of language-related Cntnap2 protein in neural circuits critical for vocal learning","volume":"522","author":"M. C. Condro","year":"2014a","journal-title":"J Comp Neurol"},{"key":"pone.0265604.ref041","doi-asserted-by":"crossref","first-page":"75","DOI":"10.3819\/ccbr.2014.90003","article-title":"Recent advances in the genetics of vocal learning","volume":"9","author":"M. C. Condro","year":"2014b","journal-title":"Comparative Cognition and Behavior Reviews"},{"issue":"6","key":"pone.0265604.ref042","doi-asserted-by":"crossref","first-page":"1464","DOI":"10.1016\/j.neuron.2013.09.021","article-title":"Diminished FoxP2 levels affect dopaminergic modulation of corticostriatal signaling important to song variability","volume":"80","author":"M. Murugan","year":"2013","journal-title":"Neuron"},{"issue":"9","key":"pone.0265604.ref043","doi-asserted-by":"crossref","first-page":"2896","DOI":"10.1523\/JNEUROSCI.11-09-02896.1991","article-title":"A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning","volume":"11","author":"C. Scharff","year":"1991","journal-title":"J Neurosci"},{"issue":"2","key":"pone.0265604.ref044","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1016\/j.jchemneu.2009.07.003","article-title":"Anatomy of a songbird basal ganglia circuit essential for vocal learning and plasticity","volume":"39","author":"S. D. Gale","year":"2010","journal-title":"J Chem Neuroanatomy"},{"key":"pone.0265604.ref045","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-030-34683-6","volume-title":"The Neuroethology of Birdsong","author":"J. Sakata","year":"2020"},{"key":"pone.0265604.ref046","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1146\/annurev-neuro-060909-152826","article-title":"Translating Birdsong: Songbirds as a model for basic and applied medical research","volume":"36","author":"M. S. Brainard","year":"2013","journal-title":"Annual Rev Neurosci"},{"issue":"10","key":"pone.0265604.ref047","doi-asserted-by":"crossref","first-page":"e46610","DOI":"10.1371\/journal.pone.0046610","article-title":"Of Mice, Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds","volume":"7","author":"G Arriaga","year":"2012","journal-title":"PLOS ONE"},{"issue":"2","key":"pone.0265604.ref048","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/0896-6273(95)90040-3","article-title":"Characterization of a novel protein regulated during the critical period for song learning in the zebra finch","volume":"15","author":"J. M. George","year":"1995","journal-title":"Neuron"},{"issue":"3","key":"pone.0265604.ref049","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1006\/nlme.1997.3795","article-title":"Synelfin regulation during the critical period for song learning in normal and isolated juvenile zebra finches","volume":"68","author":"H. Jin","year":"1997","journal-title":"Neurobiol Learn and Mem"},{"issue":"3","key":"pone.0265604.ref050","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/j.neuron.2012.01.005","article-title":"Molecular microcircuitry underlies functional specification in a basal ganglia circuit dedicated to vocal learning","volume":"73","author":"A. T. Hilliard","year":"2012","journal-title":"Neuron"},{"key":"pone.0265604.ref051","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.bbr.2018.12.004","article-title":"Social context-dependent singing alters molecular markers of dopaminergic and glutamatergic signaling in finch basal ganglia Area X","volume":"360","author":"L.Y. So","year":"2019","journal-title":"Behav Brain Res"},{"issue":"7026","key":"pone.0265604.ref052","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1038\/nature03127","article-title":"Contributions of an avian basal ganglia\u2013forebrain circuit to real-time modulation of song","volume":"433","author":"M. H. Kao","year":"2005","journal-title":"Nature"},{"issue":"1","key":"pone.0265604.ref053","doi-asserted-by":"crossref","first-page":"e8592","DOI":"10.1371\/journal.pone.0008592","article-title":"Song practice promotes acute vocal variability at a key stage of sensorimotor learning","volume":"5","author":"J. E. Miller","year":"2010","journal-title":"PLOS ONE"},{"issue":"12","key":"pone.0265604.ref054","doi-asserted-by":"crossref","first-page":"e82327","DOI":"10.1371\/journal.pone.0082327","article-title":"A daily oscillation in the fundamental frequency and amplitude of harmonic syllables of zebra finch song","volume":"8","author":"W. E. Wood","year":"2013","journal-title":"PLOS ONE"},{"issue":"6","key":"pone.0265604.ref055","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1006\/anbe.1999.1416","article-title":"A procedure for an automated measurement of song similarity","volume":"59","author":"O. Tchernichovski","year":"2009","journal-title":"Animal Behav"},{"issue":"11","key":"pone.0265604.ref056","doi-asserted-by":"crossref","first-page":"e12599","DOI":"10.14814\/phy2.12599","article-title":"Reduced vocal variability in a zebra finch model of dopamine depletion: implications for Parkinson disease","volume":"3","author":"J. E. Miller","year":"2015","journal-title":"Physiol Rep"},{"issue":"7027","key":"pone.0265604.ref057","doi-asserted-by":"crossref","first-page":"710","DOI":"10.1038\/nature03275","article-title":"How sleep affects the developmental learning of bird song","volume":"433","author":"S. Der\u00e9gnaucourt","year":"2005","journal-title":"Nature"},{"key":"pone.0265604.ref058","doi-asserted-by":"crossref","first-page":"10237","DOI":"10.1038\/srep10237","article-title":"VoICE: A semi-automated pipeline for standardizing vocal analysis across models","volume":"5","author":"Z. D. Burkett","year":"2015","journal-title":"Scientific Rep"},{"issue":"1","key":"pone.0265604.ref059","first-page":"60","article-title":"Common terminology and acoustic measures for human voice and birdsong","volume":"62","author":"A. Badwal","year":"2018","journal-title":"JSLHR"},{"issue":"4","key":"pone.0265604.ref060","doi-asserted-by":"crossref","first-page":"2015","DOI":"10.1152\/jn.90415.2008","article-title":"Birdsong decreases protein levels of FoxP2, a molecule required for human speech","volume":"100","author":"J. E. Miller","year":"2008","journal-title":"J Neurophysiol"},{"issue":"1","key":"pone.0265604.ref061","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1007\/s00441-004-0956-9","article-title":"Stages in the development of Parkinson\u2019s disease-related pathology","volume":"318","author":"H. Braak","year":"2004","journal-title":"Cell and Tissue Res"},{"issue":"8","key":"pone.0265604.ref062","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1002\/mds.27741","article-title":"Changing views of the pathophysiology of Parkinsonism","volume":"34","author":"T. Wichmann","year":"2019","journal-title":"Movement Disorders"},{"issue":"1","key":"pone.0265604.ref063","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/j.expneurol.2010.06.017","article-title":"Elevated tauopathy and alpha-synuclein pathology in postmortem Parkinson\u2019s disease brains with and without dementia","volume":"225","author":"J. Wills","year":"2010","journal-title":"Exper Neurol"},{"issue":"6","key":"pone.0265604.ref064","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1007\/s00401-011-0815-1","article-title":"Changes in the solubility and phosphorylation of \u03b1-synuclein over the course of Parkinson\u2019s disease","volume":"121","author":"J. Zhou","year":"2011","journal-title":"Acta Neuropathologica"},{"key":"pone.0265604.ref065","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.nbd.2013.05.017","article-title":"Divergent \u03b1-synuclein solubility and aggregation properties in G2019S LRRK2 Parkinson\u2019s disease brains with Lewy Body pathology compared to idiopathic cases","volume":"58","author":"A. Mamais","year":"2013","journal-title":"Neurobiol Disease"},{"key":"pone.0265604.ref066","article-title":"Sequential extraction of soluble and insoluble alpha-synuclein from parkinsonian brains","volume":"107","author":"R. Bandopadhyay","year":"2016","journal-title":"JOVE"},{"issue":"1","key":"pone.0265604.ref067","doi-asserted-by":"crossref","first-page":"27","DOI":"10.3109\/02699206.2014.951901","article-title":"Speech-related fatigue and fatigability in Parkinson\u2019s disease","volume":"29","author":"M. J. Makashay","year":"2015","journal-title":"Clinical Linguistics and Phonetics"},{"issue":"3","key":"pone.0265604.ref068","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1159\/000479927","article-title":"Speech and communication changes reported by people with Parkinson\u2019s disease","volume":"69","author":"E. Schalling","year":"2017","journal-title":"Folia Phoniatrica et Logopaedica"},{"issue":"1\u20132","key":"pone.0265604.ref069","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/S0166-4328(01)00374-6","article-title":"Quantifying song bout production during zebra finch sensory-motor learning suggests a sensitive period for vocal practice","volume":"131","author":"F. Johnson","year":"2002","journal-title":"Behavioural brain research"},{"issue":"2","key":"pone.0265604.ref070","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1177\/0748730411435965","article-title":"Circadian regulation of bird song, call, and locomotor behavior by pineal melatonin in the zebra finch","volume":"27","author":"G. Wang","year":"2012","journal-title":"Journal of Biological Rhythms"},{"issue":"2","key":"pone.0265604.ref071","doi-asserted-by":"crossref","first-page":"a009399","DOI":"10.1101\/cshperspect.a009399","article-title":"\u03b1-Synuclein in Parkinson\u2019s disease","volume":"2","author":"L. Stefanis","year":"2012","journal-title":"Cold Spring Harbor Perspectives in Medicine"},{"issue":"2","key":"pone.0265604.ref072","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1038\/nrneurol.2013.275","article-title":"Extracellular \u03b1-synuclein is a novel and crucial factor in Lewy body diseases","volume":"10","author":"H. J. Lee","year":"2014","journal-title":"Nature Rev Neurol"},{"issue":"4","key":"pone.0265604.ref073","doi-asserted-by":"crossref","first-page":"699","DOI":"10.3233\/JPD-150642","article-title":"The synaptic function of \u03b1-synuclein","volume":"5","author":"J. Burr\u00e9","year":"2015","journal-title":"J Parkinson\u2019s Dis"},{"issue":"3","key":"pone.0265604.ref074","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1111\/jnc.13570","article-title":"The contribution of alpha synuclein to neuronal survival and function\u2013Implications for Parkinson\u2019s disease","volume":"137","author":"M. J. Benskey","year":"2016","journal-title":"J Neurochem"},{"key":"pone.0265604.ref075","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.neuroscience.2014.10.010","article-title":"Variability in action: Contributions of a songbird cortical-basal ganglia circuit to vocal motor learning and control","volume":"296","author":"S. C. Woolley","year":"2015","journal-title":"Neuroscience"},{"issue":"9","key":"pone.0265604.ref076","doi-asserted-by":"crossref","first-page":"e76310","DOI":"10.1371\/journal.pone.0076310","article-title":"Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain","volume":"8","author":"D. F. Aschauer","year":"2013","journal-title":"PloS one"},{"issue":"1","key":"pone.0265604.ref077","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/nrdp.2017.13","article-title":"Parkinson disease","volume":"3","author":"W. Poewe","year":"2017","journal-title":"Nature Rev Disease Primers"},{"issue":"43","key":"pone.0265604.ref078","doi-asserted-by":"crossref","first-page":"15227","DOI":"10.1523\/JNEUROSCI.3545-12.2012","article-title":"Systematic mutagenesis of \u03b1-synuclein reveals distinct sequence requirements for physiological and pathological activities","volume":"32","author":"J. Burr\u00e9","year":"2012","journal-title":"Journal of Neuroscience"},{"issue":"8","key":"pone.0265604.ref079","doi-asserted-by":"crossref","first-page":"1764","DOI":"10.1002\/jnr.22327","article-title":"Alpha-synuclein overexpression in mice alters synaptic communication in the corticostriatal pathway","volume":"88","author":"N. Wu","year":"2010","journal-title":"J Neuroscience Res"},{"issue":"5","key":"pone.0265604.ref080","doi-asserted-by":"crossref","first-page":"1365","DOI":"10.1093\/brain\/awz065","article-title":"Alpha-synuclein targets GluN2A NMDA receptor subunit causing striatal synaptic dysfunction and visuospatial memory alteration","volume":"142","author":"V. Durante","year":"2019","journal-title":"Brain"},{"issue":"2","key":"pone.0265604.ref081","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1002\/cne.11012","article-title":"An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch","volume":"469","author":"A. Reiner","year":"2004","journal-title":"J Comp Neurology"},{"issue":"3","key":"pone.0265604.ref082","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1152\/jn.01138.2005","article-title":"Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability","volume":"96","author":"M. H. Kao","year":"2006","journal-title":"J Neurophysiol"},{"issue":"1","key":"pone.0265604.ref083","doi-asserted-by":"crossref","first-page":"e54","DOI":"10.1371\/journal.pone.0000054","article-title":"The dark side of EGFP: defective polyubiquitination","volume":"1","author":"M. Baens","year":"2006","journal-title":"PloS one"},{"issue":"2","key":"pone.0265604.ref084","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1038\/mt.2013.266","article-title":"AAV9-mediated expression of a non-self protein in nonhuman primate central nervous system triggers widespread neuroinflammation driven by antigen-presenting cell transduction","volume":"22","author":"L. Samaranch","year":"2014","journal-title":"Molecular Therapy"},{"issue":"5","key":"pone.0265604.ref085","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s12015-016-9670-8","article-title":"Cellular GFP toxicity and immunogenicity: potential confounders in in vivo cell tracking experiments","volume":"12","author":"A. M. Ansari","year":"2016","journal-title":"Stem cell reviews and reports"},{"issue":"3","key":"pone.0265604.ref086","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1002\/jnr.24363","article-title":"Downregulation of tyrosine hydroxylase phenotype after AAV injection above substantia nigra: caution in experimental models of Parkinson\u2019s disease","volume":"97","author":"K. Albert","year":"2019","journal-title":"Journal of neuroscience research"},{"issue":"7362","key":"pone.0265604.ref087","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1038\/nature10324","article-title":"\u03b1-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation","volume":"477","author":"T. Bartels","year":"2011","journal-title":"Nature"},{"issue":"43","key":"pone.0265604.ref088","doi-asserted-by":"crossref","first-page":"17797","DOI":"10.1073\/pnas.1113260108","article-title":"A soluble \u03b1-synuclein construct forms a dynamic tetramer","volume":"108","author":"W. Wang","year":"2011","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"40","key":"pone.0265604.ref089","doi-asserted-by":"crossref","first-page":"E4274","DOI":"10.1073\/pnas.1416598111","article-title":"\u03b1-Synuclein assembles into higher-order multimers upon membrane binding to promote SNARE complex formation","volume":"111","author":"J. Burr\u00e9","year":"2014","journal-title":"Proceedings of the National Academy of Sciences"},{"issue":"19","key":"pone.0265604.ref090","doi-asserted-by":"crossref","first-page":"2319","DOI":"10.1016\/j.cub.2014.08.027","article-title":"\u03b1-synuclein multimers cluster synaptic vesicles and attenuate recycling","volume":"24","author":"L. Wang","year":"2014","journal-title":"Current Biology"},{"issue":"3","key":"pone.0265604.ref091","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1038\/mp.2013.3","article-title":"Loss of dopaminergic nigrostriatal neurons accounts for the motivational and affective deficits in Parkinson\u2019s disease","volume":"19","author":"G. Drui","year":"2014","journal-title":"Molecular psychiatry"},{"key":"pone.0265604.ref092","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bandl.2016.11.005","article-title":"Distinct patterns of imprecise consonant articulation among Parkinson\u2019s disease, progressive supranuclear palsy and multiple system atrophy","volume":"165","author":"T. Tykalova","year":"2017","journal-title":"Brain and Lang"},{"issue":"4","key":"pone.0265604.ref093","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1007\/s00415-015-7671-1","article-title":"Speech disorders reflect differing pathophysiology in Parkinson\u2019s disease, progressive supranuclear palsy and multiple system atrophy","volume":"262","author":"J. Rusz","year":"2015","journal-title":"J Neurol"},{"issue":"2S","key":"pone.0265604.ref094","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1044\/2017_AJSLP-16-0090","article-title":"Consonant acoustics in Parkinson\u2019s disease and multiple sclerosis: Comparison of clear and loud speaking conditions","volume":"26","author":"K. Tjaden","year":"2017","journal-title":"American Journal of Speech-Language Pathology"},{"issue":"1","key":"pone.0265604.ref095","first-page":"1","article-title":"Phonetic relevance and phonemic grouping of speech in the automatic detection of Parkinson\u2019s Disease","volume":"9","author":"L. Moro-Velazquez","year":"2019","journal-title":"Scientific Rep"},{"issue":"3","key":"pone.0265604.ref096","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1080\/136828200410654","article-title":"Voice characteristics in the progression of Parkinson\u2019s disease","volume":"35","author":"R. J. Holmes","year":"2000","journal-title":"International Journal of Language & Communication Disorders"},{"issue":"1","key":"pone.0265604.ref097","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1159\/000081959","article-title":"Task-based profile of vocal intensity decline in Parkinson\u2019s disease","volume":"57","author":"K. M. Rosen","year":"2005","journal-title":"Folia Phoniatrica et Logopaedica"},{"issue":"7","key":"pone.0265604.ref098","first-page":"2084","article-title":"Detection of articulatory deficits in Parkinson\u2019s Disease: can systematic manipulations of phonetic complexity help?","volume":"63","author":"M. Kuruvilla-Dugdale","year":"2020","journal-title":"JSLHR"},{"issue":"12","key":"pone.0265604.ref099","doi-asserted-by":"crossref","first-page":"3179","DOI":"10.1093\/brain\/awx263","article-title":"The direct basal ganglia pathway is hyperfunctional in focal dystonia","volume":"140","author":"K. Simonyan","year":"2017","journal-title":"Brain"},{"key":"pone.0265604.ref100","doi-asserted-by":"crossref","first-page":"e32167","DOI":"10.7554\/eLife.32167","article-title":"A subcortical circuit linking the cerebellum to the basal ganglia engaged in vocal learning","volume":"7","author":"L. 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