Evolutionarily conserved organization of the dopaminergic system in lamprey: SNc/VTA afferent and efferent connectivity and D2 receptor expression

Journal of Comparative Neurology

Volumn 522, Issue 17, 2014, Pages 3775-3794

  Pérez Fernández, Juan ^a   Stephenson Jones, Marcus ^a   Suryanarayana, Shreyas M ^a   Robertson, Brita ^a   Grillner, Sten ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Basal ganglia; Posterior tuberculum; RRID:AB_2201528; RRID:AB_514497; Substantia nigra pars compacta; Ventral tegmental area

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; TRACER; TYROSINE 3 MONOOXYGENASE; DOPAMINE;

ADULT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN STEM; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; EFFERENT NERVE; FEMALE; GENETIC CONSERVATION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LAMPREY; LOCOMOTION; MALE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS OF THE TUBERCULUM POSTERIOR; OLFACTORY BULB; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REWARD; SENSORY NERVE; SENSORY STIMULATION; SIGNAL PROCESSING; SUBSTANTIA NIGRA PARS COMPACTA; SUPERIOR COLLICULUS; TECTUM; VENTRAL TEGMENTUM; ANATOMY AND HISTOLOGY; ANIMAL; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL NETWORK; NERVE TRACT; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SPINAL CORD; SUBSTANTIA NIGRA;

ANIMALS; CONSERVED SEQUENCE; DOPAMINE; FEMALE; LAMPREYS; MALE; NERVE NET; NEURAL PATHWAYS; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; SPINAL CORD; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA;

EID: 84908476903     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23639     Document Type: Article

References (88)

1. Abalo XM, Villar-Cheda B, Anadón R, Rodicio MC. 2005. Development of the dopamine-immunoreactive system in the central nervous system of the sea lamprey. Brain Res Bull 66:560-564.
2. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
3. Anzalone A, Lizardi-Ortiz JE, Ramos M, De Mei C, Hopf FW, Iaccarino C, Halbout B, Jacobsen J, Kinoshita C, Welter M, Caron MG, Bonci A, Sulzer D, Borrelli E. 2012. Dual control of dopamine synthesis and release by presynaptic and postsynaptic dopamine D2 receptors. J Neurosci 32:9023-9034.
4. Barreiro-Iglesias A, Villar-Cerviño V, Anadón R, Rodicio MC. 2009. Dopamine and gamma-aminobutyric acid are colocalized in restricted groups of neurons in the sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215:601-610.
5. Baumgarten HG. 1972. Biogenic monoamines in the cyclostome and lower vertebrate brain. Prog. Histochem. Cytochem 4:1-90.
6. Bertram C, Dahan L, Boorman LW, Harris S, Vautrelle N, Leriche M, Redgrave P, Overton PG. 2013. Cortical regulation of dopaminergic neurons: role of the midbrain superior colliculus. J Neurophysiol Nov 13 Epub ahead of print.
7. Bevan MD, Hallworth NE, Baufreton J. 2007. GABAergic control of the subthalamic nucleus. Prog Brain Res 160:173-188.
8. Bodznick D, Northcutt RG. 1981. Electroreception in lampreys: Evidence that the earliest vertebrates were electroreceptive. Science 212:465-467.
9. Bromberg-Martin ES, Matsumoto M, Hikosaka O. 2010. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834.
10. Callier S, Snapyan M, Le Crom S, Prou D, Vincent JD, Vernier P. 2003. Evolution and cell biology of dopamine receptors in vertebrates. Biol Cell 95:489-502.
11. Campbell KJ, Takada M. 1989. Bilateral tectal projection of single nigrostriatal dopamine cells in the rat. Neuroscience 33:311-321.
12. Campbell KJ, Takada M, Hattori T. 1991. Co-localization of tyrosine hydroxylase and glutamate decarboxylase in a subpopulation of single nigrotectal projection neurons. Brain Res 558:239-244.
13. Carrera I, Sueiro C, Molist P, Ferreiro S, Adrio F, Rodríguez MA, Anadón R, Rodríguez-Moldes I. 2005. Temporal and spatial organization of tyrosine hydroxylase-immunoreactive cell groups in the embryonic brain of an elasmobranch, the lesser-spotted dogfish Scyliorhinus canicula. Brain Res Bull 66:541-545.
14. Comoli E, Coizet V, Boyes J, Bolam JP, Canteras NS, Quirk RH, Overton PG, Redgrave P. 2003. A direct projection from superior colliculus to substantia nigra for detecting salient visual events. Nat Neurosci 6:974-980.
15. Derjean D, Moussaddy A, Atallah E, St-Pierre M, Auclair F, Chang S, Ren X, Zielinski B, Dubuc R. 2010. A novel neural substrate for the transformation of olfactory inputs into motor output. PLoS Biol 8:e1000567.
16. Dolen G, Darvishzadeh A, Huang KW, Malenka RC. 2013. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501:179-184.
17. Dommett E, Coizet V, Blaha CD, Martindale J, Lefebvre V, Walton N, Mayhew JE, Overton PG, Redgrave P. 2005. How visual stimuli activate dopaminergic neurons at short latency. Science 307:1476-1479.
18. Dubuc R, Bongianni F, Ohta Y, Grillner S. 1993. Anatomical and physiological study of brainstem nuclei relaying dorsal column inputs in lampreys. J Comp Neurol 327:260-270.
19. El Manira A, Pombal MA, Grillner S. 1997. Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis. J Comp Neurol 389:603-616.
20. Ericsson J, Silberberg G, Robertson B, Wikstrom MA, Grillner S. 2011. Striatal cellular properties conserved from lampreys to mammals. J Physiol 589:2979-2992.
21. Ericsson J, Stephenson-Jones M, Pérez-Fernández J, Robertson B, Silberberg G, Grillner S. 2013. Dopamine differentially modulates the excitability of striatal neurons of the direct and indirect pathways in lamprey. J Neurosci 33:8045-8054.
22. Filippi A, Mueller T, Driever W. 2014. vglut2 and gad expression reveal distinct patterns of dual GABAergic versus glutamatergic cotransmitter phenotypes of dopaminergic and noradrenergic neurons in the zebrafish brain. J Comp Neurol 522:2019-2037.
23. Gerfen CR, Surmeier DJ. 2011. Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34:441-466.
24. González A, Marín O, Tuinhof R, Smeets WJ. 1994. Ontogeny of catecholamine systems in the central nervous system of anuran amphibians: an immunohistochemical study with antibodies against tyrosine hydroxylase and dopamine. J Comp Neurol 346:63-79.
25. González MJ, Yáñez J, Anadón R. 1999. Afferent and efferent connections of the torus semicircularis in the sea lamprey: an experimental study. Brain Res 826:83-94.
26. Graybiel AM. 2008. Habits, rituals, and the evaluative brain. Annu Rev Neurosci. 31:359-387.
27. Green WW, Basilious A, Dubuc R, Zielinski BS. 2013. The neuroanatomical organization of projection neurons associated with different olfactory bulb pathways in the sea lamprey, Petromyzon marinus. PLoS One 8:e69525.
28. Grillner S, Robertson B, Stephenson-Jones M. 2013. The evolutionary origin of the vertebrate basal ganglia and its role in action-selection. J Physiol 591:5425-5431.
29. Gurevich EV, Joyce JN. 1999. Distribution of dopamine D3 receptor expressing neurons in the human forebrain: comparison with D2 receptor expressing neurons. Neuropsychopharmacol 20:60-80.
30. Haber SN. 2003. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat 26:317-330.
31. Hikosaka O. 2007. Basal ganglia mechanisms of reward-oriented eye movement. Ann N Y Acad Sci 1104:229-249.
32. Hu Z, Cooper M, Crockett DP, Zhou R. 2004. Differentiation of the midbrain dopaminergic pathways during mouse development. J Comp Neurol 476:301-311.
33. Hurd YL, Suzuki M, Sedvall GC. 2001. D1 and D2 dopamine receptor mRNA expression in whole hemisphere sections of the human brain. J Chem Neuroanat 22:127-137.
34. Ibáñez-Sandoval O, Hernández A, Florán B, Galarraga E, Tapia D, Valdiosera R, Erlij D, Aceves J, Bargas J. 2006. Control of the subthalamic innervation of substantia nigra pars reticulata by D1 and D2 dopamine receptors. J Neurophysiol 95:1800-1811.
35. Jones MR, Grillner S, Robertson B. 2009. Selective projection patterns from subtypes of retinal ganglion cells to tectum and pretectum: distribution and relation to behavior. J Comp Neurol 517:257-275.
36. Kincheski GC, Mota-Ortiz SR, Pavesi E, Canteras NS, Carobrez AP. 2012. The dorsolateral periaqueductal gray and its role in mediating fear learning to life threatening events. PLoS One 7:e50361.
37. Kubikova L, Wada K, Jarvis ED. 2010. Dopamine receptors in a songbird brain. J Comp Neurol 518:741-769.
38. Kumar S, Hedges SB. 1998. A molecular timescale for vertebrate evolution. Nature 392:917-920.
39. Lammel S, Lim BJ, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC. 2012. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491:212-217.
40. Maltais S, Côté S, Drolet G, Falardeau P. 2000. Cellular colocalization of dopamine D1 mRNA and D2 receptor in rat brain using a D2 dopamine receptor specific polyclonal antibody. Prog Neuropsychopharmacol Biol Psych 24:1127-1149.
41. Mansour A, Meador-Woodruff JH, Bunzow JR, Civelli O, Akil H, Watson SJ. 1990. Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization-receptor autoradiographic analysis. J Neurosci 10:2587-2600.
42. Marín O, González A, Smeets WJ. 1995. Evidence for a mesolimbic pathway in anuran amphibians: a combined tract-tracing/immunohistochemical study. Neurosci Lett 190:183-186.
43. McHaffie JG, Jiang H, May PJ, Coizet V, Overton PG, Stein BE, Redgrave P. 2006. A direct projection from superior colliculus to substantia nigra pars compacta in the cat. Neuroscience 138:221-234.
44. Meador-Woodruff JH, Mansour A, Healy DJ, Kuehn R, Zhou QY, Bunzow JR, Akil H, Civelli O, Watson SJ Jr. 1991. Comparison of the distributions of D1 and D2 dopamine receptor mRNAs in rat brain. Neuropsychopharmacol 5:231-242.
45. Medina L, Puelles L, Smeets WJ. 1994. Development of catecholamine systems in the brain of the lizard Gallotia galloti. J Comp Neurol 350:41-62.
46. Ménard A, Auclair F, Bourcier-Lucas C, Grillner S, Dubuc R. 2007. Descending GABAergic projections to the mesencephalic locomotor region in the lamprey Petromyzon marinus. J Comp Neurol 501:260-273.
47. Naito A, Kita H. 1994. The Cotico-nigral projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res 637:317-322.
48. O'Connell LA, Fontenot MR, Hofmann HA. 2011. Characterization of the dopaminergic system in the brain of an African cichlid fish, Astatotilapia burtoni. J Comp Neurol 519:75-92.
49. Pasqualini C, Weltzien FA, Vidal B, Baloche S, Rouget C, Gilles N, Servent D, Vernier P, Dufour S. 2009. Two distinct dopamine D2 receptor genes in the European eel: molecular characterization, tissue-specific transcription, and regulation by sex steroids. Endocrinology 150:1377-1392.
50. Pérez-Fernández J. 2013. Characterization of Y and dopamine receptors in lampreys by using in situ hybridization: an evolutionary approach. PhD Thesis, Neurolam Group, Dept of Functional Biology and Health Sciences, University of Vigo, Spain.
51. Pierre J, Mahouche M, Suderevskaya EI, Repérant J, Ward R. 1997. Immunocytochemical localization of dopamine and its synthetic enzymes in the central nervous system of the lamprey Lampetra fluviatilis. J Comp Neurol 380:119-135.
52. Pombal MA, Puelles L. 1999. Prosomeric map of the lamprey forebrain based on calretinin immunocytochemistry, Nissl stain, and ancillary markers. J Comp Neurol 414:391-422.
53. Pombal MA, El Manira A, Grillner S. 1997. Afferents of the lamprey striatum with special reference to the dopaminergic system: a combined tracing and immunohistochemical study. J Comp Neurol 386:71-91.
54. Pombal MA, Rodríguez-Alonso M, Megías M, Moussa CE, Sidhu A, Vernier P. 2007. Distribution of the dopamine D1 receptor in the lamprey brain: evolutionary implications. SfN abstract 351.29.
55. Pombal MA, Megías M, Bardet SM, Puelles L. 2009. New and old thoughts on the segmental organization of the forebrain in lampreys. Brain Behav Evol 74:7-19.
56. Quintana-Urzainqui I, Sueiro C, Carrera I, Ferreiro-Galve S, Santos-Durán G, Pose-Méndez S, Mazan S, Candal E, Rodríguez-Moldes I. 2012. Contributions of developmental studies in the dogfish Scyliorhinus canicula to the brain anatomy of elasmobranchs: insights on the basal ganglia. Brain Behav Evol 80:127-141.
57. Quintana-Urzainqui I, Candal E, Rodríguez-Moldes I. 2013. Basal ganglia organization in elasmobranchs: catecholaminergic cells of the posterior tubercle, ventral tegmental area and substantia nigra project to subpallium. Abstract 7th European Conference of Comparative Neurobiologists, Budapest, Hungary.
58. Redgrave P, Gurney K. 2006. The short-latency dopamine signal: a role in discovering novel actions? Nat Rev Neurosci 7:967-975.
59. Redgrave P, Coizet V, Comoli E, McHaffie JG, Leriche M, Vautrelle N, Hayes LM, Overton P. 2010. Interactions between the midbrain superior colliculus and the basal ganglia. Front Neuroanat 4: 10.3389/fnana.2010.00132.
60. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Gunturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED, Avian Brain Nomenclature Forum. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
61. Rink E, Wullimann MF. 2001. The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889:316-330.
62. Robertson B, Huerta-Ocampo I, Ericsson J, Stephenson-Jones M, Pérez-Fernández J, Bolam JP, Diaz-Heijtz R, Grillner S. 2012. The dopamine D2 receptor gene in lamprey, its expression in the striatum and cellular effects of D2 receptor activation. PLoS One 7:e35642.
63. Ronan M. 1988. Anatomical and physiological evidence for electroreception in larval lampreys. Brain Res 448:173-177.
64. Ryczko D, Gratsch S, Auclair F, Dube C, Bergeron S, Alpert MH, Cone JJ, Roitman MF, Alford S, Dubuc R. 2013. Forebrain dopamine neurons project down to a brainstem region controlling locomotion. Proc Natl Acad Sci U S A 110:E3235-3242.
65. Saitoh K, Ménard A, Grillner S. 2007. Tectal control of locomotion, steering, and eye movements in lamprey. J Neurophysiol 97:3093-3108.
66. Schotland J, Shupliakov O, Wikstrom M, Brodin L, Srinivasan M, You ZB, Herrera-Marschitz M, Zhang W, Hokfelt T, Grillner S. 1995. Control of lamprey locomotor neurons by colocalized monoamine transmitters. Nature 374:266-268.
67. Shelton L, Becerra L, Borsook D. 2012. Unmasking the mysteries of the habenula in pain and analgesia. Prog Neurobiol 96:208-219.
68. Schultz W. 2013. Updating dopamine reward signals. Curr Opin Neurobiol 23:229-238.
69. Schultz W., Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593-1599.
70. Smeets WJ, Marín O, González A. 2000. Evolution of the basal ganglia: new perspectives through a comparative approach. J Anat 196 (Pt 4):501-517.
71. Smits SM, Burbach JP, Smidt MP. 2006. Developmental origin and fate of meso-diencephalic dopamine neurons. Prog Neurobiol 78:1-16.
72. Stephenson-Jones M, Samuelsson E, Ericsson J, Robertson B, Grillner S. 2011. Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr Biol 21:1081-1091.
73. Stephenson-Jones M, Ericsson J, Robertson B, Grillner S. 2012a. Evolution of the basal ganglia: dual-output pathways conserved throughout vertebrate phylogeny. J Comp Neurol 520:2957-2973.
74. Stephenson-Jones M, Floros O, Robertson B, Grillner S. 2012b. Evolutionary conservation of the habenular nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems. Proc Natl Acad Sci U S A. 109:E164-173.
75. Stephenson-Jones M, Kardamakis AA, Robertson B, Grillner S. 2013. Independent circuits in the basal ganglia for the evaluation and selection of actions. Proc Natl Acad Sci U S A. 110:E3670-3679.
76. Takada M, Li ZK, Hattori T. 1988a. Collateral projection from the substantia nigra to the striatum and superior colliculus in the rat. Neuroscience 25:563-568.
77. Takada M, Li ZK, Hattori T. 1988b. Dopaminergic nigrotectal projection in the rat. Brain Res 457:165-168.
78. Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W. 2011. Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. Nat Commun 2:171.
79. Thompson RH, Menard A, Pombal M, Grillner S. 2008. Forebrain dopamine depletion impairs motor behavior in lamprey. Eur J Neurosci 27:1452-1460.
80. Vacher C, Pellegrini E, Anglade I, Ferriere F, Saligaut C, Kah O. 2003. Distribution of dopamine D2 receptor mRNAs in the brain and the pituitary of female rainbow trout: an in situ hybridization study. J Comp Neurol 458:32-45.
81. Verney C, Zecevic N, Puelles L. 2001. Structure of longitudinal brain zones that provide the origin for the substantia nigra and ventral tegmental area in human embryos, as revealed by cytoarchitecture and tyrosine hydroxylase, calretinin, calbindin, and GABA immunoreactions. J Comp Neurol. 429:22-44.
82. Vernier P, Wullimann MF. 2009. Evolution of the posterior tuberculum and preglomerular nuclear complex. In: Binder MD, Hirokawa N, Windhorst U, editors. Encyclopedia of Neurosciences, Part 5. Berlin: Springer. P1404-1413.
83. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N. 2012. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858-873.
84. Weiner DM, Levey AI, Sunahara RK, Niznik HB, O'Dowd BF, Seeman P, Brann MR. 1991. D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci U S A 88:1859-1863.
85. Wullimann MF. 2014. Ancestry of basal ganglia circuits: New evidence in teleosts. J Comp Neurol 522:2013-2018.
86. Yamamoto K, Vernier P. 2011. The evolution of dopamine systems in chordates. Front Neuroanat 5:21.
87. Yamamoto K, Ruuskanen JO, Wullimann MF, Vernier P. 2011. Differential expression of dopaminergic cell markers in the adult zebrafish forebrain. J Comp Neurol 519:576-598.
88. Zahm DS, Cheng AY, Lee TJ, Ghobadi CW, Schwartz ZM, Geisler S, Parsely KP, Gruber C, Veh RW. 2011. Inputs to the midbrain dopaminergic complex in the rat, with emphasis on extended amygdala-recipient sectors. J Comp Neurol 519:3159-3188.