Reward circuitry is perturbed in the absence of the serotonin transporter

NeuroImage

Volumn 46, Issue 4, 2009, Pages 1091-1104

  Bearer, Elaine L ^a,b   Zhang, Xiaowei ^a   Janvelyan, Davit ^a   Boulat, Benoit ^a   Jacobs, Russell E ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

DTI; Knock out; Manganese enhanced MRI; Morphometry; MRS; Serotonin transporter; Statistical parametric mapping; Synaptic transmission; Transport

Indexed keywords

MANGANESE; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; RAPHE NUCLEUS; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM; WILD TYPE;

ANIMALS; BRAIN MAPPING; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; MICE, KNOCKOUT; NEURAL PATHWAYS; PREFRONTAL CORTEX; REWARD; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 67349129763     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.03.026     Document Type: Article

References (129)

1. Adamec R., Holmes A., and Blundell J.T. Vulnerability to lasting anxiogenic effects of brief exposure to predator stimuli: sex, serotonin and other factors-relevance to PTSD. Neurosci. Biobehav. Rev. 32 (2008) 1287-1292
2. Alexander D.C., Pierpaoli C., Basser P.J., and Gee J.C. Spatial transformations of diffusion tensor magnetic resonance images. IEEE Trans. Med. Imaging 20 (2001) 1131-1139
3. Altamura C., Dell'Acqua M.L., Moessner R., Murphy D.L., Lesch K.P., and Persico A.M. Altered neocortical cell density and layer thickness in serotonin transporter knockout mice: a quantitation study. Cereb. Cortex 17 (2007) 1394-1401
4. Aoki I., Tanaka C., Takegami T., Ebisu T., Umeda M., Fukunaga M., Fukuda K., Silva A.C., Koretsky A.P., and Naruse S. Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI). Magn. Reson. Med. 48 (2002) 927-933
5. Basser P.J. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 8 (1995) 333-344
6. Bearer E.L., Falzone T.L., Zhang X., Biris O., Rasin A., and Jacobs R.E. Role of neuronal activity and kinesin on tract tracing by manganese-enhanced MRI (MEMRI). Neuroimage 37 (2007) S37-S46
7. Bearer E.L., Zhang X., and Jacobs R.E. Live imaging of neuronal connections by magnetic resonance: robust transport in the hippocampal-septal memory circuit in a mouse model of Down syndrome. Neuroimage 37 (2007) 230-242
8. Bengel D., Heils A., Petri S., Seemann M., Glatz K., Andrews A., Murphy D.L., and Lesch K.P. Gene structure and 5′-flanking regulatory region of the murine serotonin transporter. Molecular Brain Research 44 (1997) 286-292
9. Berton O., and Nestler E.J. New approaches to antidepressant drug discovery: beyond monoamines. Nat. Rev. Neurosci. 7 (2006) 137-151
10. Bottomley P.A. Spatial localization in NMR spectroscopy in vivo. Ann. N. Y. Acad. Sci. 508 (1987) 333-348
11. Brian Ross S.B. Magnetic resonance spectroscopy of the human brain. Anat. Rec. 265 (2001) 54-84
12. Canals S., Beyerlein M., Keller A.L., Murayama Y., and Logothetis N.K. Magnetic resonance imaging of cortical connectivity in vivo. Neuroimage 40 (2008) 458-472
13. Canli T., Zhao Z., Desmond J.E., Kang E.J., Gross J., and Gabrieli J.D.E. An fMRI study of personality influences on brain reactivity to emotional stimuli. Behav. Neurosci. 115 (2001) 33-42
14. Caron M.G. Genetic targeting of catecholamine transporters reveal essential roles in neuromodulation, maintenance of homeostasis and psychostimulant action. Biol. Psychiatry 45 (1999) 5S-6S
15. Carr D.B., and Sesack S.R. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 20 (2000) 3864-3873
16. Choi I.Y., Lee S.P., Guilfoyle D.N., and Helpern J.A. In vivo NMR studies of neurodegenerative diseases in transgenic and rodent models. Neurochem. Res. 28 (2003) 987-1001
17. Cross D.J., Minoshima S., Anzai Y., Flexman J.A., Keogh B.P., Kim Y., and Maravilla K.R. Statistical mapping of functional olfactory connections of the rat brain in vivo. Neuroimage 23 (2004) 1326-1335
18. Cudalbu C., Cavassila S., Rabeson H., van Ormondt D., and Graveron-Demilly D. Influence of measured and simulated basis sets on metabolite concentration estimates. NMR Biomed. 9999 (2007) n/a
19. Dedeoglu A., Choi J.-K., Cormier K., Kowall N.W., and Jenkins B.G. Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that express mutant human APP shows altered neurochemical profile. Brain Res. 1012 (2004) 60-65
20. Dong H.W. Allen Reference Atlas - a Digital Color Brain Atlas of the C57Black/6J Male Mouse (2008), John Wiley & Sons, Inc., Hoboken, NJ
21. Drapeau P., and Nachshen D.A. Manganese fluxes and manganese-dependent neurotransmitter release in presynaptic nerve-endings isolated from rat-brain. J. Physiol. (London) 348 (1984) 493-510
22. Drobyshevsky A., Song S.-K., Gamkrelidze G., Wyrwicz A.M., Derrick M., Meng F., Li L., Ji X., Trommer B., Beardsley D.J., Luo N.L., Back S.A., and Tan S. Developmental changes in diffusion anisotropy coincide with immature oligodendrocyte progression and maturation of compound action potential. J. Neurosci. 25 (2005) 5988-5997
23. Dykstra L.A., Bohn L.M., Rodriguiz R.M., Wetsel W.C., Gainetdinov R.R., and Caron M.G. Rewarding properties of cocaine in dopamine/norepinephrine transporter knockout mice. FASEB J. 17 (2003) A205
24. Everitt B.J., and Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8 (2005) 1481-1489
25. Fox M., Andrews A., Wendland J., Lesch K.-P., Holmes A., and Murphy D. A pharmacological analysis of mice with a targeted disruption of the serotonin transporter. Psychopharmacology 195 (2007) 147-166
26. Gabbott P.L.A., Warner T.A., Jays P.R.L., Salway P., and Busby S.J. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 492 (2005) 145-177
27. Gainetdinov R.R., and Caron M.G. Monoamine transporters: from genes to behavior. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 261-284
28. Gainetdinov R.R., Sotnikova T.D., and Caron M.G. Monoamine transporter pharmacology and mutant mice. Trends Pharmacol. Sci. 23 (2002) 367-373
29. Gerfen C.R. Basal ganglia. In: Paxinos G. (Ed). The Rat Nervous System (2004), Academic Press, Sydney 455-508
30. Gobbi G., Murphy D.L., Lesch K.-P., and Blier P. Modifications of the serotonergic system in mice lacking serotonin transporters: an in vivo electrophysiological study. J. Pharmacol. Exp. Ther. 296 (2001) 987-995
31. Govindaraju V., Young K., and Maudsley A.A. Proton NMR chemical shifts and coupling constants for brain metabolites. NMR Biomed. 13 (2000) 129-153
32. Graveron-Demilly D., Diop A., Briguet A., and Fenet B. Product operator algebra for strongly coupled spin system. J. Magn. Reson. A101 (1993) 233-239
33. Groenewegen H.J., and Uylings H.B.M. The prefrontal cortex and the integration of sensory, limbic and autonomic information. Cognition, Emotion and Autonomic Responses: the Integrative Role of the Prefrontal Cortex and Limbic Structures 126 (2000) 3-28
34. Groenewegen H.J., Wright C.I., and Uylings H.B.M. The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. J. Psychopharmacol. 11 (1997) 99-106
35. Gruetter R. Automatic, localized in vivo adjustment of all 1st-order and 2nd-order shim coils. Magn. Reson. Med. 29 (1993) 804-811
36. Hagen M.C., Zald D.H., Thornton T.A., and Pardo J.V. Somatosensory processing in the human inferior prefrontal cortex. J. Neurophysiol. 88 (2002) 1400-1406
37. Hall F.S., Sora I., Drgonova J., Li X.F., Goeb M., and Uhl G.R. Molecular mechanisms underlying the rewarding effects of cocaine. Current Status of Drug Dependence/Abuse Studies: Cellular and Molecular Mechanisms of Drugs of Abuse and Neurotoxicity (2004) 47-56
38. Hammers A., Allom R., Koepp M.J., Free S.L., Myers R., Lemieux L., Mitchell T.N., Brooks D.J., and Duncan J.S. Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Hum. Brain Mapp. 19 (2003) 224-247
39. Hariri A.R., and Holmes A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn. Sci. 10 (2006) 182-191
40. Hasan K.M., Basser P.J., Parker D.L., and Alexander A.L. Analytical computation of the eigenvalues and eigenvectors in DT-MRI. J. Magn. Reson. 152 (2001) 41-47
41. Hennig J., Nauerth A., and Friedburg H. Rare imaging - a fast imaging method for clinical MR. Magn. Reson. Med. 3 (1986) 823-833
42. Hetherington H.P., Pan J.W., Chu W.J., Mason G.F., and Newcomer B.R. Biological and clinical MRS at ultra-high field. NMR Biomed. 10 (1997) 360-371
43. Hof P.R., Bloom F.E., Belichenko P.V., and Celio M.R. Comparative Cytoarchitectonic Atlas of the C57bl/6 and 129/SV Mouse Brains (2000), Elsevier, New York
44. Holmes A., Li Q., Murphy D.L., Gold E., and Crawley J.N. Abnormal anxiety-related behavior in serotonin transporter null mutant mice: the influence of genetic background. Genes, Brain Behav. 2 (2003) 365-380
45. Homberg J.R., Olivier J.D.A., Smits B.M.G., Mul J.D., Mudde J., Verheul M., Nieuwenhuizen O.F.M., Schoffelmeere A.N.M., Ellenbroeik B.A., and Clippen E. Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 146 (2007) 1662-1676
46. Jansen J.F.A., Backes W.H., Nicolay K., and Kooi M.E. 1H MR spectroscopy of the brain: absolute quantification of metabolites. Radiology 240 (2006) 318-332
47. Kassubek J., Juengling F.D., Kioschies T., Henkel K., Karitzky J., Kramer B., Ecker D., Andrich J., Saft C., Kraus P., Aschoff A.J., Ludolph A.C., and Landwehrmeyer G.B. Topography of cerebral atrophy in early Huntington's disease: a voxel based morphometric MRI study. J. Neurol. Neurosurg. Psychiatry 75 (2004) 213-220
48. Kim D.-K., Tolliver T.J., Huang S.-J., Martin B.J., Andrews A.M., Wichems C., Holmes A., Lesch K.-P., and Murphy D.L. Altered serotonin synthesis, turnover and dynamic regulation in multiple brain regions of mice lacking the serotonin transporter. Neuropharmacology 49 (2005) 798-810
49. Kita T., Wagner G.C., and Nakashima T. Current research on methamphetamine-induced neurotoxicity: animal models of monoamine disruption. J. Pharmacol. Sci. 92 (2003) 178-195
50. Kochunov P., Lancaster J.L., Thompson P., Woods R., Mazziotta J., Hardies J., and Fox P. Regional spatial normalization: toward an optimal target. J. Comput. Assist. Tomogr. 25 (2001) 805-816
51. Kovacevic N., Henderson J.T., Chan E., Lifshitz N., Bishop J., Evans A.C., Henkelman R.M., and Chen X.J. A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb. Cortex 15 (2005) 639-645
52. LeBihan D. Molecular diffusion, tissue microdynamics and microstructure. NMR Biomed. 8 (1995) 375-386
53. Lee E.-F., Jacobs R.E., Dinov I., Loew A., and Toga A.W. Standard atlas space for C57BL/6J neonatal mouse brain. Anat. Embryol. 210 (2005) 245-263
54. Lepore N., Brun C., Yi-Yu C., Ming-Chang C., Dutton R.A., Hayashi K.M., Luders E., Lopez O.L., Aizenstein H.J., Toga A.W., Becker J.T., and Thompson P.M. Generalized tensor-based morphometry of HIV/AIDS using multivariate statistics on deformation tensors. Medical Imaging, IEEE Transactions on 27 (2008) 129-141
55. Li Q. Cellular and molecular alterations in mice with deficient and reduced serotonin transporters. Mol. Neurobiol. 34 (2006) 51-65
56. Li Q., Wichems C.H., Ma L., Van de Kar L.D., Garcia F., and Murphy D.L. Brain region-specific alterations of 5-HT2A and 5-HT2C receptors in serotonin transporter knockout mice. J. Neurochem. 84 (2003) 1256-1265
57. Lira A., Zhou M.M., Castanon N., Ansorge M.S., Gordon J.A., Francis J.H., Bradley-Moore M., Lira J., Underwood M.D., Arango V., Kung H.F., Hofer M.A., Hen R., and Gingrich J.A. Altered depression-related behaviors and functional changes in the dorsal raphe nucleus of serotonin transporter-deficient mice. Biol. Psychiatry 54 (2003) 960-971
58. Lyoo I.K., and Renshaw P.F. Magnetic resonance spectroscopy: current and future applications in psychiatric research. Biol. Psychiatry 51 (2002) 195-207
59. Ma Y., Hof P.R., Grant S.C., Blackband S.J., Bennett R., Slatest L., McGuigan M.D., and Benveniste H. A three-dimensional digital atlas database of the adult C57BL/6J mouse brain by magnetic resonance microscopy. Neuroscience 135 (2005) 1203-1215
60. Marjanska M., Curran G.L., Wengenack T.M., Henry P.-G., Bliss R.L., Poduslo J.F., Jack Jr. C.R., Ugurbil K., and Garwood M. Monitoring disease progression in transgenic mouse models of Alzheimer's disease with proton magnetic resonance spectroscopy. Proc. Natl. Acad. Sci. 102 (2005) 11906-11910
61. Mathews T.A., Fedele D.E., Coppelli F.M., Avila A.M., Murphy D.L., and Andrews A.M. Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression. J. Neurosci. Methods 140 (2004) 169-181
62. Mattiello J., Basser P.J., and LeBihan D. The b matrix in diffusion tensor echo-planar imaging. Magn. Reson. Med. 37 (1997) 292-300
63. Maudsley A.A. Magnetic resonance spectroscopic imaging. In: Toga A.W., and Mazziotta J. (Eds). Brain Mapping: the Methods (2002), Academic Press, San Diego 351-378
64. May A., and Gaser C. Magnetic resonance-based morphometry: a window into structural plasticity of the brain. Curr. Opin. Neurol. 19 (2006) 407-411
65. Mechelli A., Friston K.J., Frackowiak R.S., and Price C.J. Structural covariance in the human cortex. J. Neurosci. 25 (2005) 8303-8310
66. Montanez S., Owens W.A., Gould G.G., Murphy D.L., and Daws L.C. Exaggerated effect of fluvoxamine in heterozygote serotonin transporter knockout mice. J. Neurochem. 86 (2003) 210-219
67. Mori S., Itoh R., Zhang J.Y., Kaufmann W.E., van Zijl P.C.M., Solaiyappan M., and Yarowsky P. Diffusion tensor imaging of the developing mouse brain. Magn. Reson. Med. 46 (2001) 18-23
68. Morris P.G. Magnetic resonance imaging and magnetic resonance spectroscopy assessment of brain function in experimental animals and man. J. Psychopharmacol. 13 (1999) 330-336
69. Murayama Y., Weber B., Saleem K.S., Augath M., and Logothetis N.K. Tracing neural circuits in vivo with Mn-enhanced MRI. Magn. Reson. Imaging 24 (2006) 349-358
70. Murphy D.L., Lerner A., Rudnick G., and Lesch K.P. Serotonin transporter: gene, genetic disorders, and pharmacogenetics. Mol. Interv. 4 (2004) 109-123
71. Murphy D.L., and Lesch K.-P. Targeting the murine serotonin transporter: insights into human neurobiology. Nat. Rev. Neurosci. 9 (2008) 85-96
72. Murphy D.L., Li Q., Engel S., Wichems C., Andrews A., Lesch K.-P., and Uhl G. Genetic perspectives on the serotonin transporter. Brain Res. Bull. 56 (2001) 487-494
73. Murphy D.L., Uhl G.R., Holmes A., Ren-Patterson R., Hall F.S., Sora I., Detera-Wadleigh S., and Lesch K.P. Experimental gene interaction studies with SERT mutant mice as models for human polygenic and epistatic traits and disorders. Genes Brain Behav. 2 (2003) 350-364
74. Naressi A., Couturier C., Devos J., Janssen M., Mangeat C., de Beer R., and Graveron-Demilly D. Java-based graphical user interface for the MRUI quantitation package. Magma 12 (2001) 141-152
75. Narita K., Kawasaki F., and Kita H. Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res. 510 (1990) 289-295
76. Nelson R.J., and Trainor B.C. Neural mechanisms of aggression. Nat. Rev. Neurosci. 8 (2007) 536-546
77. Numachi Y., Ohara A., Yamashita M., Fukushima S., Kobayashi H., Hata H., Watanabe H., Hall F.S., Lesch K.P., Murphy D.L., Uhl G.R., and Sora L. Methamphetamine-induced hyperthermia and lethal toxicity: role of the dopamine and serotonin transporters. Eur. J. Pharmacol. 572 (2007) 120-128
78. Papadakis N., Xing D., Houston G., Smith J., Smith M., James M., Parsons A., Huang C., Hall L., and Carpenter T. A study of rotationally invariant and symmetric indices of diffusion anisotropy. Magn. Reson. Imaging 17 (1999) 881-892
79. Pautler R.G., Mongeau R., and Jacobs R.E. In vivo trans-synaptic tract tracing from the murine striatum and amygdala utilizing manganese enhanced MRI (MEMRI). Magn. Reson. Med. 50 (2003) 33-39
80. Paxinos G. The Rat Nervous System. 3rd ed. (2004), Academic Press, Sydney
81. Paxinos G., and Franklin K. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. (2001), Academic Press, San Diego
82. Perani D., Brambati S., Borroni B., Agosti C., Broli M., Alberici A., Mattioli F., Garibotto V., Cotelli M., Gasparotti R., Scifo P., Alonso R., Binetti G., Cappa S., and Padovani A. Voxel based morphometry and diffusion tensor imaging in corticobasal degeneration and the relationship with neurological features. Neurology 64 (2005) A99
83. Persico A.M. Serotonin and neurodevelopment: the rodent somatosensory system paradigm. Eur. Neuropsychopharmacol. 14 (2004) S169-S170
84. Persico A.M., Altamura C., Calia E., Puglisi-Allegra S., Ventura R., Lucchese F., and Keller F. Serotonin depletion and barrel cortex development: impact of growth impairment vs. serotonin effects on thalamocortical endings. Cereb. Cortex 10 (2000) 181-191
85. Persico A.M., Baldi A., Dell'Acqua M.L., Moessner R., Murphy D.L., Lesch K.P., and Keller F. Reduced programmed cell death in brains of serotonin transporter knockout mice. Neuroreport 14 (2003) 341-344
86. Persico A.M., Mengual E., Moessner R., Hall S.F., Revay R.S., Sora I., Arellano J., DeFelipe J., Gimenez-Amaya J.M., Conciatori M., Marino R., Baldi A., Cabib S., Pascucci T., Uhl G.R., Murphy D.L., Lesch K.P., and Keller F. Barrel pattern formation requires serotonin uptake by thalamocortical afferents, and not vesicular monoamine release. J. Neurosci. 21 (2001) 6862-6873
87. Persico A.M., Mengual E., Moessner R., Revay R.S., Sora I., Arellano J., DeFelipe J., Gimenez-Amaya J.M., Conciatori M., Marino R., Baldi A., Cabib S., Pascucci T., Uhl G.R., Murphy D.L., Lesch K.P., and Keller F. Barrel pattern formation requires serotonin uptake by thalamocortical afferents, while vesicular monoamine release is necessary for development of supragranular layers. Pflugers Archiv-European J. Physiol. 440 (2000) R34
88. Pfefferbaum A., Sullivan E., Hedehus M., Adalsteinsson E., Lim K., and Moseley M. In vivo detection and functional correlates of white matter microstructural disruption in chronic alcoholism. Alcohol., Clin. Exp. Res. 24 (2000) 1214-1221
89. Puig M.V., Celada P., and Artigas F. Serotonergic control of prefrontal cortex. Revista De Neurologia 39 (2004) 539-547
90. Ratiney H., Sdika M., Coenradie Y., Cavassila S., van Ormondt D., and Graveron-Demilly D. Time-domain semi-parametric estimation based on a metabolite basis set. NMR Biomed. 18 (2005) 1-13
91. Reading S.A.J., Yassa M.A., Bakker A., Dziorny A.C., Gourley L.M., Yallapragada V., Rosenblatt A., Margolis R.L., Aylward E.H., Brandt J., Mori S., van Zijl P., Bassett S.S., and Ross C.A. Regional white matter change in pre-symptomatic Huntington's disease: a diffusion tensor imaging study. Psychiatry Research Neuroimaging 140 (2005) 55-62
92. Reith M.E.A. Studying monoamine transporters: beyond hypermonoaminaemia. J. Neurosci. Methods 143 (2005) 1-2
93. Rex D.E., Ma J.Q., and Toga A.W. The LONI pipeline processing environment. Neuroimage 19 (2003) 1033-1048
94. Robbins T.W., and Everitt B.J. Limbic-striatal memory systems and drug addiction. Neurobiol. Learn. Mem. 78 (2002) 625-636
95. Rocha B.A. Stimulant and reinforcing effects of cocaine in monoamine transporter knockout mice. Eur. J. Pharmacol. 479 (2003) 107-115
96. Rorden C., and Brett M. Stereotaxic display of brain lesions. Behav. Neurol. 12 (2000) 191-200
97. Rothman D.L., Behar K.L., Hyder F., and Shulman R.G. In vivo NMR studies of the glutamate neurotransmitter flux and neuroenergetics: implications for brain function. Annu. Rev. Physiol. 65 (2003) 401-427
98. Rudin M., Beckmann N., Mir A., and Sauter A. In-vivo magnetic-resonance-imaging and spectroscopy in pharmacological research - assessment of morphological, physiological and metabolic effects of drugs. Eur. J. Pharm. Sci. 3 (1995) 255-264
99. Saleem K.S., Pauls J.M., Augath M., Trinath T., Prause B.A., Hashikawa T., and Logothetis N.K. Magnetic resonance imaging of neuronal connections in the macaque monkey. Neuron 34 (2002) 685-700
100. Sesack S.R., and Pickel V.M. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus-accumbens-septi and on dopamine neurons in the ventral tegmental area. J. Comp. Neurol. 320 (1992) 145-160
101. Shattuck D.W., and Leahy R.M. Automated graph-based analysis and correction of cortical volume topology. IEEE Trans. Med. Imaging 20 (2001) 1167-1177
102. Shen H.W., Hagino Y., Kobayashi H., Shinohara-Tanaka K., Ikeda K., Yamamoto H., Yamamoto T., Lesch K.P., Murphy D.L., Hall F.S., Uhl G.R., and Sora I. Regional differences in extracellular dopamine and serotonin assessed by in vivo microdialysis in mice lacking dopamine and/or serotonin transporters. Neuropsychopharmacology 29 (2004) 1790-1799
103. Silva A.C., Lee J.H., Aoki I., and Koretsky A.P. Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed. 17 (2004) 532-543
104. Simmons J.M., Saad Z.S., Lizak M.J., Ortiz M., Koretsky A.P., and Richmond B.J. Mapping prefrontal circuits in vivo with manganese-enhanced magnetic resonance imaging in monkeys. J. Neurosci. 28 (2008) 7637-7647
105. Sled J.G., Zijdenbos A.P., and Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 17 (1998) 87-97
106. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., and Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17 (2002) 1429-1436
107. Sora I., Hall F.S., Andrews A.M., Itokawa M., Li X.F., Wei H.B., Wichems C., Lesch K.P., Murphy D.L., and Uhl G.R. Molecular mechanisms of cocaine reward: combined dopamine and serotonin transporter knockouts eliminate cocaine place preference. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 5300-5305
108. Soria G., Wiedermann D., Justicia C., Ramos-Cabrer P., and Hoehn M. Reproducible imaging of rat corticothalamic pathway by longitudinal manganese-enhanced MRI (L-MEMRI). Neuroimage 41 (2008) 668-674
109. Spring S., Lerch J.P., and Henkelman R.M. Sexual dimorphism revealed in the structure of the mouse brain using three-dimensional magnetic resonance imaging. Neuroimage 35 (2007) 1424-1433
110. Thomsen M., Hall F.S., Uhl G.R., and Caine S.B. Dramatically decreased cocaine self-administration in dopamine but not serotonin transporter knock-out mice. J. Neurosci. 29 (2009) 1087-1092
111. Tkac I., Henry P.-G., Andersen P., Keene C.D., Low W.C., and Gruetter R. Highly resolved in vivo 1H NMR spectroscopy of the mouse brain at 9.4 T. Magn. Reson. Med. 52 (2004) 478-484
112. Tkáč I., Staručk Z., Choi I.-Y., and Gruetter R. In Vivo 1H NMR Spectroscopy of Rat Brain at 1 ms Echo Time. Magn. Reson. Med. 41 (1999) 649-656
113. In: Toga A.W., and Mazziotta J.C. (Eds). Brain Mapping: the Methods. 2nd Ed. (2002), Academic Press, San Diego
114. Torres G.E., and Caron M.G. Approaches to identify monoamine transporter interacting proteins. J. Neurosci. Methods 143 (2005) 63-68
115. Tyszka J.M., Readhead C., Bearer E., Pautler R., and Jacobs R.E. Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage 2006 (2006) 1058-1065
116. Uhl G.R. Dopamine transporter: basic science and human variation of a key molecule for dopaminergic function, locomotion, and parkinsonism. Mov. Disord. 18 (2003) S71-S80
117. Uhl G.R. Molecular genetics of addiction vulnerability. NeuroRX 3 (2006) 295-301
118. Uhl G.R., Hall F.S., and Sora I. Cocaine, reward, movement and monoamine transporters. Mol. Psychiatry 7 (2002) 21-26
119. Uhl G.R., and Lin Z.C. The top 20 dopamine transporter mutants: structure-function relationships and cocaine actions. Eur. J. Pharmacol. 479 (2003) 71-82
120. Van der Linden A., Van Camp N., Ramos-Cabrer P., and Hoeh M. Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition. NMR Biomed. 20 (2007) 522-545
121. van Doorn A., Bovendeerd P.H., Nicolay K., Drost M.R., and Janssen J.D. Determination of muscle fibre orientation using diffusion-weighted MRI [published erratum appears in Eur J Morphol 1996 Nov;34(4):325]. Eur. J. Morphol. 34 (1996) 5-10
122. Verma R., Mori S., Shen D.G., Yarowsky P., Zhang J.Y., and Davatzikos C. Spatiotemporal maturation patterns of murine brain quantified by diffusion tensor MRI and deformation-based morphometry. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 6978-6983
123. Wellman C.L., Izquierdo A., Garrett J.E., Martin K.P., Carroll J., Millstein R., Lesch K.P., Murphy D.L., and Holmes A. Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J. Neurosci. 27 (2007) 684-691
124. Wieshmann U., Clark C., Symms M., Franconi F., Barker G., and Shorvon S. Reduced anisotropy of water diffusion in structural cerebral abnormalities demonstrated with diffusion tensor imaging. Magn. Reson. Imaging 17 (1999) 1269-1274
125. Woods R.P., Grafton S.T., Holmes C.J., Cherry S.R., and Mazziotta J.C. Automated image registration: I. General methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. 22 (1998) 139-152
126. Woods R.P., Grafton S.T., Watson J.D., Sicotte N.L., and Mazziotta J.C. Automated image registration: II. Intersubject validation of linear and nonlinear models. J. Comput. Assist. Tomogr. 22 (1998) 153-165
127. Xu F., Gainetdinov R.R., Wetsel W.C., Jones S.R., Bohn L.M., Miller G.W., Wang Y.-M., and Caron M.G. Mice lacking the norepinephrine transporter are supersensitive to psychostimulants. Nat. Neurosci. 3 (2000) 465-471
128. Yamashita M., Fukushima S., Shen H.W., Hall F.S., Uhl G.R., Numachi Y., Kobayashi H., and Sora I. Norepinephrine transporter blockade can normalize the prepulse inhibition deficits found in dopamine transporter knockout mice. Neuropsychopharmacology 31 (2006) 2132-2139
129. Zald D.H., Mattson D.L., and Pardo J.V. Brain activity in ventromedial prefrontal cortex correlates with individual differences in negative affect. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 2450-2454