Speech-induced striatal dopamine release is left lateralized and coupled to functional striatal circuits in healthy humans: A combined PET, fMRI and DTI study

NeuroImage

Volumn 70, Issue , 2013, Pages 21-32

  Simonyan, Kristina ^a,b   Herscovitch, Peter ^b   Horwitz, Barry ^c  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

Dopamine; Speech functional networks; Striatum; Structural networks

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; RACLOPRIDE C 11;

ADULT; ARTICLE; ASSOCIATION CORTEX; BRAIN FUNCTION; CONTROLLED STUDY; CORPUS STRIATUM; DIFFUSION TENSOR IMAGING; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; IMAGE PROCESSING; LEFT HEMISPHERE; MALE; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SPEECH ARTICULATION;

CORPUS STRIATUM; DIFFUSION TENSOR IMAGING; DOPAMINE; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; POSITRON-EMISSION TOMOGRAPHY; SPEECH;

EID: 84872292474     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.12.042     Document Type: Article

References (107)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Alexander G.E., Crutcher M.D., DeLong M.R. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog. Brain Res. 1990, 85:119-146.
3. Aronson A.E. Clinical Voice Disorders. An Interdisciplinary Approach 1980, Thieme, Stuttgart.
4. Ballion B., Mallet N., Bezard E., Lanciego J.L., Gonon F. Intratelencephalic corticostriatal neurons equally excite striatonigral and striatopallidal neurons and their discharge activity is selectively reduced in experimental parkinsonism. Eur. J. Neurosci. 2008, 27:2313-2321.
5. Bamford N.S., Zhang H., Schmitz Y., Wu N.P., Cepeda C., Levine M.S., Schmauss C., Zakharenko S.S., Zablow L., Sulzer D. Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 2004, 42:653-663.
6. Bandettini P.A. What's new in neuroimaging methods?. Ann. N. Y. Acad. Sci. 2009, 1156:260-293.
7. Behrens T.E., Berg H.J., Jbabdi S., Rushworth M.F., Woolrich M.W. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. Neuroimage 2007, 34:144-155.
8. Bonvin C., Horvath J., Christe B., Landis T., Burkhard P.R. Compulsive singing: another aspect of punding in Parkinson's disease. Ann. Neurol. 2007, 62:525-528.
9. Carlsson A. The occurrence, distribution and physiological role of catecholamines in the nervous system. Pharmacol. Rev. 1959, 11:490-493.
10. Carson R.E. PET physiological measurements using constant infusion. Nucl. Med. Biol. 2000, 27:657-660.
11. Carson R.E., Channing M.A., Blasberg R.G., Dunn B.B., Cohen R.M., Rice K.C., Herscovitch P. Comparison of bolus and infusion methods for receptor quantitation: application to [18F]cyclofoxy and positron emission tomography. J. Cereb. Blood Flow Metab. 1993, 13:24-42.
12. Carson R.E., Breier A., de Bartolomeis A., Saunders R.C., Su T.P., Schmall B., Der M.G., Pickar D., Eckelman W.C. Quantification of amphetamine-induced changes in [11C]raclopride binding with continuous infusion. J. Cereb. Blood Flow Metab. 1997, 17:437-447.
13. Cervenka S., Backman L., Cselenyi Z., Halldin C., Farde L. Associations between dopamine D2-receptor binding and cognitive performance indicate functional compartmentalization of the human striatum. Neuroimage 2008, 40:1287-1295.
14. Ciabarra A.M., Elkind M.S., Roberts J.K., Marshall R.S. Subcortical infarction resulting in acquired stuttering. J. Neurol. Neurosurg. Psychiatry 2000, 69:546-549.
15. Ciucci M.R., Vinney L., Wahoske E.J., Connor N.P. A translational approach to vocalization deficits and neural recovery after behavioral treatment in Parkinson disease. J. Commun. Disord. 2010, 43:319-326.
16. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
17. David O., Maess B., Eckstein K., Friederici A.D. Dynamic causal modeling of subcortical connectivity of language. J. Neurosci. 2011, 31:2712-2717.
18. Davis M.H., Gaskell M.G. A complementary systems account of word learning: neural and behavioural evidence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364:3773-3800.
19. de la Fuente-Fernandez R., Kishore A., Calne D.B., Ruth T.J., Stoessl A.J. Nigrostriatal dopamine system and motor lateralization. Behav. Brain Res. 2000, 112:63-68.
20. Del Campo N., Tait R.J., Acosta-Cabronero J., Hong Y.T., Izquierdo-Garcia D., Smith R., Aigbirhio F.I., Sahakian B.J., Muller U., Robbins T.W., Fryer T.D. Quantification of receptor-ligand binding potential in sub-striatal domains using probabilistic and template regions of interest. Neuroimage 2011, 55(1):101-112.
21. D'Esposito M., Alexander M.P. Subcortical aphasia: distinct profiles following left putaminal hemorrhage. Neurology 1995, 45:38-41.
22. Draganski B., Kherif F., Kloppel S., Cook P.A., Alexander D.C., Parker G.J., Deichmann R., Ashburner J., Frackowiak R.S. Evidence for segregated and integrative connectivity patterns in the human Basal Ganglia. J. Neurosci. 2008, 28:7143-7152.
23. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25:1325-1335.
24. Endres C.J., Carson R.E. Assessment of dynamic neurotransmitter changes with bolus or infusion delivery of neuroreceptor ligands. J. Cereb. Blood Flow Metab. 1998, 18:1196-1210.
25. Endres C.J., Kolachana B.S., Saunders R.C., Su T., Weinberger D., Breier A., Eckelman W.C., Carson R.E. Kinetic modeling of [11C]raclopride: combined PET-microdialysis studies. J. Cereb. Blood Flow Metab. 1997, 17:932-942.
26. Fasano A., Daniele A., Albanese A. Treatment of motor and non-motor features of Parkinson's disease with deep brain stimulation. Lancet Neurol. 2012, 11:429-442.
27. Fino E., Glowinski J., Venance L. Bidirectional activity-dependent plasticity at corticostriatal synapses. J. Neurosci. 2005, 25:11279-11287.
28. Fisher R.S., Levine M.S., Sibley D.R., Ariano M.A. D2 dopamine receptor protein location: golgi impregnation-gold toned and ultrastructural analysis of the rat neostriatum. J. Neurosci. Res. 1994, 38:551-564.
29. Friedman J.H. Involuntary humming in autopsy-proven Parkinson's disease. Mov. Disord. 1993, 8:401.
30. Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997, 6:218-229.
31. Garraux G., Peigneux P., Carson R.E., Hallett M. Task-related interaction between basal ganglia and cortical dopamine release. J. Neurosci. 2007, 27:14434-14441.
32. Garris P.A., Ciolkowski E.L., Pastore P., Wightman R.M. Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J. Neurosci. 1994, 14:6084-6093.
33. Gertler T.S., Chan C.S., Surmeier D.J. Dichotomous anatomical properties of adult striatal medium spiny neurons. J. Neurosci. 2008, 28:10814-10824.
34. Glick S.D., Weaver L.M., Meibach R.C. Amphetamine enhancement of reward asymmetry. Psychopharmacology (Berl) 1981, 73:323-327.
35. Golfinopoulos E., Tourville J.A., Guenther F.H. The integration of large-scale neural network modeling and functional brain imaging in speech motor control. Neuroimage 2010, 52:862-874.
36. Gonon F. Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J. Neurosci. 1997, 17:5972-5978.
37. Guenther F.H., Ghosh S.S., Tourville J.A. Neural modeling and imaging of the cortical interactions underlying syllable production. Brain Lang. 2006, 96:280-301.
38. Hall H., Farde L., Halldin C., Hurd Y.L., Pauli S., Sedvall G. Autoradiographic localization of extrastriatal D2-dopamine receptors in the human brain using [125I]epidepride. Synapse 1996, 23:115-123.
39. Hara E., Kubikova L., Hessler N.A., Jarvis E.D. Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur. J. Neurosci. 2007, 25:3406-3416.
40. Heinz A., Knable M.B., Wolf S.S., Jones D.W., Gorey J.G., Hyde T.M., Weinberger D.R. Tourette's syndrome: [I-123]beta-CIT SPECT correlates of vocal tic severity. Neurology 1998, 51:1069-1074.
41. Hersch S.M., Ciliax B.J., Gutekunst C.A., Rees H.D., Heilman C.J., Yung K.K., Bolam J.P., Ince E., Yi H., Levey A.I. Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J. Neurosci. 1995, 15:5222-5237.
42. Heuer R.J., Sataloff R.T., Mandel S., Travers N. Neurogenic stuttering: further corroboration of site of lesion. Ear Nose Throat J. 1996, 75:161-168.
43. Hickok G., Poeppel D. The cortical organization of speech processing. Nat. Rev. Neurosci. 2007, 8:393-402.
44. Horwitz B., Duara R., Rapoport S.I. Age differences in intercorrelations between regional cerebral metabolic rates for glucose. Ann. Neurol. 1986, 19:60-67.
45. Horwitz B., Swedo S.E., Grady C.L., Pietrini P., Schapiro M.B., Rapoport J.L., Rapoport S.I. Cerebral metabolic pattern in obsessive-compulsive disorder: altered intercorrelations between regional rates of glucose utilization. Psychiatry Res. 1991, 40:221-237.
46. Huang Y.C., Hessler N.A. Social modulation during songbird courtship potentiates midbrain dopaminergic neurons. PLoS One 2008, 3:e3281.
47. Innis R.B., Cunningham V.J., Delforge J., Fujita M., Gjedde A., Gunn R.N., Holden J., Houle S., Huang S.C., Ichise M., Iida H., Ito H., Kimura Y., Koeppe R.A., Knudsen G.M., Knuuti J., Lammertsma A.A., Laruelle M., Logan J., Maguire R.P., Mintun M.A., Morris E.D., Parsey R., Price J.C., Slifstein M., Sossi V., Suhara T., Votaw J.R., Wong D.F., Carson R.E. Consensus nomenclature for in vivo imaging of reversibly binding radioligands. J. Cereb. Blood Flow Metab. 2007, 27:1533-1539.
48. Jarvis E.D., Nottebohm F. Motor-driven gene expression. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:4097-4102.
49. Jurgens U. Projections from the cortical larynx area in the squirrel monkey. Exp. Brain Res. 1976, 25:401-411.
50. Jurgens U. Neural pathways underlying vocal control. Neurosci. Biobehav. Rev. 2002, 26:235-258.
51. Karlsson F., Blomstedt P., Olofsson K., Linder J., Nordh E., van Doorn J. Control of phonatory onset and offset in Parkinson patients following deep brain stimulation of the subthalamic nucleus and caudal zona incerta. Parkinsonism Relat. Disord. 2012, 18:824-827.
52. Kataoka H., Ueno S. Compulsive singing associated with a dopamine agonist in Parkinson disease. Cogn. Behav. Neurol. 2010, 23:140-141.
53. Kelly R.M., Strick P.L. Macro-architecture of basal ganglia loops with the cerebral cortex: use of rabies virus to reveal multisynaptic circuits. Prog. Brain Res. 2004, 143:449-459.
54. Koylu B., Trinka E., Ischebeck A., Visani P., Trieb T., Kremser C., Bartha L., Schocke M., Benke T. Neural correlates of verbal semantic memory in patients with temporal lobe epilepsy. Epilepsy Res. 2006, 72:178-191.
55. Kreitzer A.C., Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 2007, 445:643-647.
56. Kreitzer A.C., Malenka R.C. Striatal plasticity and basal ganglia circuit function. Neuron 2008, 60:543-554.
57. Kunzle H. Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 1975, 88:195-209.
58. Laruelle M. Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. J. Cereb. Blood Flow Metab. 2000, 20:423-451.
59. Lee M.S., Lee S.B., Kim W.C. Spasmodic dysphonia associated with a left ventrolateral putaminal lesion. Neurology 1996, 47:827-828.
60. Lei W., Jiao Y., Del Mar N., Reiner A. Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J. Neurosci. 2004, 24:8289-8299.
61. Ludlow C.L., Adler C.H., Berke G.S., Bielamowicz S.A., Blitzer A., Bressman S.B., Hallett M., Jinnah H.A., Juergens U., Martin S.B., Perlmutter J.S., Sapienza C., Singleton A., Tanner C.M., Woodson G.E. Research priorities in spasmodic dysphonia. Otolaryngol. Head Neck Surg. 2008, 139:495-505.
62. Mahon S., Deniau J.M., Charpier S. Corticostriatal plasticity: life after the depression. Trends Neurosci. 2004, 27:460-467.
63. Mallet N., Ballion B., Le Moine C., Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 2006, 26:3875-3884.
64. Martin-Soelch C., Szczepanik J., Nugent A., Barhaghi K., Rallis D., Herscovitch P., Carson R.E., Drevets W.C. Lateralization and gender differences in the dopaminergic response to unpredictable reward in the human ventral striatum. Eur. J. Neurosci. 2011, 33:1706-1715.
65. Mawlawi O., Martinez D., Slifstein M., Broft A., Chatterjee R., Hwang D.R., Huang Y., Simpson N., Ngo K., Van Heertum R., Laruelle M. Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D(2) receptor parameter measurements in ventral striatum. J. Cereb. Blood Flow Metab. 2001, 21:1034-1057.
66. Metter E.J., Jackson C., Kempler D., Riege W.H., Hanson W.R., Mazziotta J.C., Phelps M.E. Left hemisphere intracerebral hemorrhages studied by (F-18)-fluorodeoxyglucose PET. Neurology 1986, 36:1155-1162.
67. Montague P.R., Hyman S.E., Cohen J.D. Computational roles for dopamine in behavioural control. Nature 2004, 431:760-767.
68. Morice E., Denis C., Macario A., Giros B., Nosten-Bertrand M. Constitutive hyperdopaminergia is functionally associated with reduced behavioral lateralization. Neuropsychopharmacology 2005, 30:575-581.
69. Newton-John H. Acute upper airway obstruction due to supraglottic dystonia induced by a neuroleptic. BMJ 1988, 297:964-965.
70. Nicola S.M., Malenka R.C. Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J. Neurophysiol. 1998, 79:1768-1776.
71. Nottebohm F., Stokes T.M., Leonard C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 1976, 165:457-486.
72. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
73. Price C.J. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann. N. Y. Acad. Sci. 2010, 1191:62-88.
74. Price C.J. A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 2012, 62:816-847.
75. Ramig L.O., Sapir S., Fox C., Countryman S. Changes in vocal loudness following intensive voice treatment (LSVT (R)) in individuals with Parkinson's disease: a comparison with untreated patients and normal age-matched controls. Mov. Disord. 2001, 16:79-83.
76. Redgrave P., Rodriguez M., Smith Y., Rodriguez-Oroz M.C., Lehericy S., Bergman H., Agid Y., DeLong M.R., Obeso J.A. Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat. Rev. Neurosci. 2010, 11:760-772.
77. Riecker A., Mathiak K., Wildgruber D., Erb M., Hertrich I., Grodd W., Ackermann H. fMRI reveals two distinct cerebral networks subserving speech motor control. Neurology 2005, 64:700-706.
78. Rossor M., Garrett N., Iversen L. No evidence for lateral asymmetry of neurotransmitters in post-mortem human brain. J. Neurochem. 1980, 35:743-745.
79. Salimpoor V.N., Benovoy M., Larcher K., Dagher A., Zatorre R.J. Anatomically distinct dopamine release during anticipation and experience of peak emotion to music. Nat. Neurosci. 2011, 14(2):257-262.
80. Sasaki A., Sotnikova T.D., Gainetdinov R.R., Jarvis E.D. Social context-dependent singing-regulated dopamine. J. Neurosci. 2006, 26:9010-9014.
81. Schultz W. Behavioral theories and the neurophysiology of reward. Annu. Rev. Psychol. 2006, 57:87-115.
82. Seghier M.L. Laterality index in functional MRI: methodological issues. Magn. Reson. Imaging 2008, 26:594-601.
83. Sesack S.R., Aoki C., Pickel V.M. Ultrastructural localization of D2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets. J. Neurosci. 1994, 14:88-106.
84. Shen W., Flajolet M., Greengard P., Surmeier D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 2008, 321:848-851.
85. Simonyan K., Jurgens U. Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey. Brain Res. 2003, 974:43-59.
86. Simonyan K., Horwitz B., Jarvis E.D. Dopaminergic regulation of human speech and bird song: a criticial review. Brain Lang. 2012, 122(3):142-150.
87. Slifstein M., Laruelle M. Models and methods for derivation of in vivo neuroreceptor parameters with PET and SPECT reversible radiotracers. Nucl. Med. Biol. 2001, 28:595-608.
88. Szostak C., Jakubovic A., Phillips A.G., Fibiger H.C. Bilateral augmentation of dopaminergic and serotonergic activity in the striatum and nucleus accumbens induced by conditioned circling. J. Neurosci. 1986, 6:2037-2044.
89. Taniwaki T., Tagawa K., Sato F., Iino K. Auditory agnosia restricted to environmental sounds following cortical deafness and generalized auditory agnosia. Clin. Neurol. Neurosurg. 2000, 102:156-162.
90. Tettamanti M., Moro A., Messa C., Moresco R.M., Rizzo G., Carpinelli A., Matarrese M., Fazio F., Perani D. Basal ganglia and language: phonology modulates dopaminergic release. Neuroreport 2005, 16:397-401.
91. Thompson J.L., Urban N., Abi-Dargham A. How have developments in molecular imaging techniques furthered schizophrenia research?. Imaging Med. 2009, 1:135-153.
92. Tripoliti E., Zrinzo L., Martinez-Torres I., Frost E., Pinto S., Foltynie T., Holl E., Petersen E., Roughton M., Hariz M.I., Limousin P. Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease. Neurology 2011, 76:80-86.
93. Van Lancker Sidtis D., Rogers T., Godier V., Tagliati M., Sidtis J.J. Voice and fluency changes as a function of speech task and deep brain stimulation. J. Speech Lang. Hear. Res. 2010, 53:1167-1177.
94. van Schouwenburg M., Aarts E., Cools R. Dopaminergic modulation of cognitive control: distinct roles for the prefrontal cortex and the basal ganglia. Curr. Pharm. Des. 2010, 16:2026-2032.
95. Walsh J.P. Depression of excitatory synaptic input in rat striatal neurons. Brain Res. 1993, 608:123-128.
96. Walsh B., Smith A. Linguistic complexity, speech production, and comprehension in Parkinson's disease: behavioral and physiological indices. J. Speech Lang. Hear. Res. 2011, 54:787-802.
97. Wang H., Pickel V.M. Dopamine D2 receptors are present in prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus. J. Comp. Neurol. 2002, 442:392-404.
98. Warren J., Thompson P. Drug-induced supraglottic dystonia and spasmodic dysphonia. Mov. Disord. 1998, 13:978-979.
99. Watabe H., Endres C.J., Breier A., Schmall B., Eckelman W.C., Carson R.E. Measurement of dopamine release with continuous infusion of [11C]raclopride: optimization and signal-to-noise considerations. J. Nucl. Med. 2000, 41:522-530.
100. Wickens J.R., Reynolds J.N., Hyland B.I. Neural mechanisms of reward-related motor learning. Curr. Opin. Neurobiol. 2003, 13:685-690.
101. Williams H., Crane L.A., Hale T.K., Esposito M.A., Nottebohm F. Right-side dominance for song control in the zebra finch. J. Neurobiol. 1992, 23:1006-1020.
102. Woods R.P., Mazziotta J.C., Cherry S.R. MRI-PET registration with automated algorithm. J. Comput. Assist. Tomogr. 1993, 17:536-546.
103. Wu J.C., Maguire G., Riley G., Lee A., Keator D., Tang C., Fallon J., Najafi A. Increased dopamine activity associated with stuttering. Neuroreport 1997, 8:767-770.
104. Xie Y., Zhang Y., Zheng Z., Liu A., Wang X., Zhuang P., Li Y. Changes in speech characters of patients with Parkinson's disease after bilateral subthalamic nucleus stimulation. J. Voice 2011, 25:751-758.
105. Yanagihara S., Hessler N.A. Modulation of singing-related activity in the songbird ventral tegmental area by social context. Eur. J. Neurosci. 2006, 24:3619-3627.
106. Ystad M., Eichele T., Lundervold A.J., Lundervold A. Subcortical functional connectivity and verbal episodic memory in healthy elderly - a resting state fMRI study. Neuroimage 2010, 52:379-388.
107. Zimmerberg B., Glick S.D., Jerussi T.P. Neurochemical correlate of a spatial preference in rats. Science 1974, 185:623-625.