Anatomical and functional evidence for trace amines as unique modulators of locomotor function in the mammalian spinal cord

Frontiers in Neural Circuits

Volumn 8, Issue November, 2014, Pages

  Gozal, Elizabeth A ^a   O'Neill, Brannan E ^a   Sawchuk, Michael A ^a   Zhu, Hong ^a   Halder, Mallika ^a   Chou, Ching Chieh ^a   Hochman, Shawn ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Dopa decarboxylase; Locomotion; TAAR; Tryptamine; Tyramine; phenylethylamine

Indexed keywords

AMINE; CYCLOHEXIMIDE; N METHYL DEXTRO ASPARTIC ACID; RECEPTOR; SEROTONIN; TRACE AMINE ASSOCIATED RECEPTOR 1; TRACE AMINE ASSOCIATED RECEPTOR 4; TRYPTAMINE; TYRAMINE; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER; AROMATIC LEVO AMINO ACID DECARBOXYLASE; BIOGENIC AMINE; G PROTEIN COUPLED RECEPTOR; N METHYLASPARTIC ACID; PHENETHYLAMINE; PHENETHYLAMINE DERIVATIVE; TAAR4 PROTEIN, RAT; TRACE AMINE-ASSOCIATED RECEPTOR 1; TRYPTAMINE DERIVATIVE;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CENTRAL PATTERN GENERATOR; CONTROLLED STUDY; IN VITRO STUDY; INTRACELLULAR TRANSPORT; LOCOMOTION; MONOAMINE NERVE CELL; MOTONEURON; MOTOR ACTIVITY; NERVE PROJECTION; NEUROMODULATION; NEWBORN; NONHUMAN; RAT; SPINAL CORD; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; METABOLISM; NERVE CELL; PHYSIOLOGY; SPINAL ROOT; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; AROMATIC-L-AMINO-ACID DECARBOXYLASES; BIOGENIC MONOAMINES; CENTRAL PATTERN GENERATORS; LOCOMOTION; MOTOR ACTIVITY; N-METHYLASPARTATE; NEURONS; PHENETHYLAMINES; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; SEROTONIN; SPINAL CORD; SPINAL NERVE ROOTS; TRYPTAMINES; TYRAMINE;

EID: 84927544584     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2014.00134     Document Type: Article

References (122)

1. Abbas, A. K. (2013). Evidence for constitutive protein synthesis in hippocampal LTP stabilization. Neuroscience 246, 301-311. doi: 10.1016/j.neuroscience.2013.05.011.
2. Allen_Spinal_Cord_Atlas. (2009). Allen Institute for Brain Science [Online]. Seattle, WA. Available online at:http://mousespinal.brain-map.org.
3. Ambalavanar, R., and Morris, R. (1989). Fluoro-Gold injected either subcutaneously or intravascularly results in extensive retrograde labelling of CNS neurones having axons terminating outside the blood-brain barrier. Brain res. 505, 171-175. doi: 10.1016/0006-8993(89)90133-9.
4. Anwar, M. A., Ford, W. R., Broadley, K. J., and Herbert, A. A. (2012). Vasoconstrictor and vasodilator responses to tryptamine of rat-isolated perfused mesentery: comparison with tyramine and beta-phenylethylamine. Br. J. Pharmacol. 165, 2191-2202. doi: 10.1111/j.1476-5381.2011.01706.x.
5. Babu, E., Kanai, Y., Chairoungdua, A., Kim, D. K., Iribe, Y., Tangtrongsup, S., et al. (2003). Identification of a novel system L amino acid transporter structurally distinct from heterodimeric amino acid transporters. J. Biol. Chem. 278, 43838-43845. doi: 10.1074/jbc.M305221200.
6. Babusyte, A., Kotthoff, M., Fiedler, J., and Krautwurst, D. (2013). Biogenic amines activate blood leukocytes via trace amine-associated receptors TAAR1 and TAAR2. J. Leukoc. Biol. 93, 387-394. doi: 10.1189/jlb.0912433.
7. Barraud, Q., Obeid, I., Aubert, I., Barriere, G., Contamin, H., McGuire, S., et al. (2010). Neuroanatomical study of the A11 diencephalospinal pathway in the non-human primate. PLoS ONE 5:e13306. doi: 10.1371/journal.pone.0013306.
8. Barriere, G., Mellen, N., and Cazalets, J. R. (2004). Neuromodulation of the locomotor network by dopamine in the isolated spinal cord of newborn rat. Eur. J. Neurosci. 19, 1325-1335. doi: 10.1111/j.1460-9568.2004.03210.x.
9. Berry, M. D. (2004). Mammalian central nervous system trace amines. Pharmacologic amphetamines, physiologic neuromodulators. J. Neurochem. 90, 257-271. doi: 10.1111/j.1471-4159.2004.02501.x.
10. Berry, M. D. (2007). The potential of trace amines and their receptors for treating neurological and psychiatric diseases. Rev. Recent Clin. Trials 2, 3-19. doi: 10.2174/157488707779318107.
11. Berry, M. D., Shitut, M. R., Almousa, A., Alcorn, J., and Tomberli, B. (2013). Membrane permeability of trace amines: evidence for a regulated, activity-dependent, nonexocytotic, synaptic release. Synapse 67, 656-667. doi: 10.1002/syn.21670.
12. Beugnet, A., Tee, A. R., Taylor, P. M., and Proud, C. G. (2003). Regulation of targets of mTOR (mammalian target of rapamycin) signalling by intracellular amino acid availability. Biochem. J. 372, 555-566. doi: 10.1042/BJ20021266.
13. Boess, F. G., and Martin, I. L. (1994). Molecular biology of 5-HT receptors. Neuropharmacology 33, 275-317. doi: 10.1016/0028-3908(94)90059-0.
14. Borowsky, B., Adham, N., Jones, K. A., Raddatz, R., Artymyshyn, R., Ogozalek, K. L., et al. (2001). Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc. Natl. Acad. Sci. U.S.A. 98, 8966-8971. doi: 10.1073/pnas.151105198.
15. Boulton, A. A. (1976). Identification, distribution, metabolism, and function of meta and para tyramine, phenylethylamine and tryptamine in brain. Adv. Biochem. Psychopharmacol. 15, 57-67.
16. Boulton, A. A. (1978). The tyramines: functionally significant biogenic amines or metabolic accidents? Life Sci. 23, 659-671. doi: 10.1016/0024-3205(78)90064-4.
17. Boulton, A. A. (1991). Phenylethylaminergic modulation of catecholaminergic neurotransmission. Prog. Neuropsychopharmacol. Biol. Psychiatry 15, 139-156. doi: 10.1016/0278-5846(91)90076-D.
18. Boulton, A. A., Juorio, A. V., and Paterson, I. A. (1990). Phenylethylamine in the CNS: effects of monoamine oxidase inhibiting drugs, deuterium substitution and lesions and its role in the neuromodulation of catecholaminergic neurotransmission. J. Neural Transm. Suppl. 29, 119-129.
19. Boulton, A. A., Juorio, A. V., Philips, S. R., and Wu, P. H. (1977). The effects of reserpine and 6-hydroxydopamine on the concentrations of some arylakylamines in rat brain. Br. J. Pharmacol. 59, 209-214. doi: 10.1111/j.1476-5381.1977.tb06996.x.
20. Bowman, W. C., Callingham, B. A., and Osuide, G. (1964). EFFECTS OF TYRAMINE ON A SPINAL REFLEX IN THE ANAESTHETISED CHICK. J. Pharm. Pharmacol. 16, 505-515. doi: 10.1111/j.2042-7158.1964.tb07505.x.
21. Bradaia, A., Trube, G., Stalder, H., Norcross, R. D., Ozmen, L., Wettstein, J. G., et al. (2009). The selective antagonist EPPTB reveals TAAR1-mediated regulatory mechanisms in dopaminergic neurons of the mesolimbic system. Proc. Natl. Acad. Sci. U.S.A. 106, 20081-20086. doi: 10.1073/pnas.0906522106.
22. Branchek, T. A., and Blackburn, T. P. (2003). Trace amine receptors as targets for novel therapeutics: legend, myth and fact. Curr. Opin. Pharmacol. 3, 90-97. doi: 10.1016/S1471-4892(02)00028-0.
23. Broadley, K. J. (2010). The vascular effects of trace amines and amphetamines. Pharmacol. Ther. 125, 363-375. doi: 10.1016/j.pharmthera.2009.11.005.
24. Brocard, F., Shevtsova, N. A., Bouhadfane, M., Tazerart, S., Heinemann, U., Rybak, I. A., et al. (2013). Activity-dependent changes in extracellular Ca2+ and K+ reveal pacemakers in the spinal locomotor-related network. Neuron 77, 1047-1054. doi: 10.1016/j.neuron.2013.01.026.
25. Bunzow, J. R., Sonders, M. S., Arttamangkul, S., Harrison, L. M., Zhang, G., Quigley, D. I., et al. (2001). Amphetamine, 3,4-methylenedioxy methamphetamine, lysergic acid diethylamide, and metabolites of the catecholamine neurotransmitters are agonists of a rat trace amine receptor. Mol. Pharmacol. 60, 1181-1188. doi: 10.1124/mol.60.6.1181.
26. Burchett, S. A., and Hicks, T. P. (2006). The mysterious trace amines: protean neuromodulators of synaptic transmission in mammalian brain. Prog. Neurobiol. 79, 223-246. doi: 10.1016/j.pneurobio.2006.07.003.
27. Cazalets, J. R., Borde, M., and Clarac, F. (1995). Localization and organization of the central pattern generator for hindlimb locomotion in newborn rat. J. Neurosci. 15, 4943-4951.
28. Chiellini, G., Frascarelli, S., Ghelardoni, S., Carnicelli, V., Tobias, S. C., Debarber, A., et al. (2007). Cardiac effects of 3-iodothyronamine: a new aminergic system modulating cardiac function. FASEB J. 21, 1597-1608. doi: 10.1096/fj.06-7474com.
29. Clarac, F., Pearlstein, E., Pflieger, J. F., and Vinay, L. (2004). The in vitro neonatal rat spinal cord preparation: a new insight into mammalian locomotor mechanisms. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 190, 343-357. doi: 10.1007/s00359-004-0499-2.
30. Cowley, K. C., and Schmidt, B. J. (1994). Some limitations of ventral root recordings for monitoring locomotion in the in vitro neonatal rat spinal cord preparation. Neurosci. Lett. 171, 142-146. doi: 10.1016/0304-3940(94)90625-4.
31. Cowley, K. C., and Schmidt, B. J. (1997). Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J. Neurophysiol. 77, 247-259.
32. Cui, D., Dougherty, K. J., Machacek, D. W., Sawchuk, M., Hochman, S., and Baro, D. J. (2006). Divergence between motoneurons: gene expression profiling provides a molecular characterization of functionally discrete somatic and autonomic motoneurons. Physiol. Genomics 24, 276-289. doi: 10.1152/physiolgenomics.00109.2005.
33. De Bono, J. P., Adlam, D., Paterson, D. J., and Channon, K. M. (2006). Novel quantitative phenotypes of exercise training in mouse models. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R926-R934. doi: 10.1152/ajpregu.00694.2005.
34. Durden, D. A., Philips, S. R., and Boulton, A. A. (1973). Identification and distribution of beta-phenylethylamine in the rat. Can. J. Biochem. 51, 995-1002. doi: 10.1139/o73-129.
35. Eikelboom, R., and Mills, R. (1988). A microanalysis of wheel running in male and female rats. Physiol. Behav. 43, 625-630. doi: 10.1016/0031-9384(88)90217-X.
36. Engel, K., and Wang, J. (2005). Interaction of organic cations with a newly identified plasma membrane monoamine transporter. Mol. Pharmacol. 68, 1397-1407. doi: 10.1124/mol.105.016832.
37. Fischer, W., Neubert, R. H., and Brandsch, M. (2010). Transport of phenylethylamine at intestinal epithelial (Caco-2) cells: mechanism and substrate specificity. Eur. J. Pharm. Biopharm. 74, 281-289. doi: 10.1016/j.ejpb.2009.11.014.
38. Garcia-Ramirez, D. L., Calvo, J. R., Hochman, S., and Quevedo, J. N. (2014). Serotonin, dopamine and noradrenaline adjust actions of myelinated afferents via modulation of presynaptic inhibition in the mouse spinal cord. PLoS ONE 9:e89999. doi: 10.1371/journal.pone.0089999.
39. Gerin, C., Becquet, D., and Privat, A. (1995). Direct evidence for the link between monoaminergic descending pathways and motor activity. 1. A study with microdialysis probes implanted in the ventral funiculus of the spinal cord. Brain Res. 704, 191-201. doi: 10.1016/0006-8993(95)01111-0.
40. Gieseker, E., Williams, K., Sawchuk, M., and Hochman, S. (2004). The trace amine tyramine is found in spinal ventral horn neurons and induces locomotor-like activity in the isolated neonatal rat spinal cord. Soc. Neurosci. Abstr. 30.
41. Gozal, E. A., Sawchuk, M. A., and Hochman, S. (2007). Trace amine immunolabeling and motor patterning in the neonatal rat spinal cord. Soc. Neurosci. Abstr. 33.
42. Gozal, E. A., Williams, K., Sawchuk, M. A., and Hochman, S. (2006). Trace amines recruit motor activity in the isolated neonatal rat spinal cord. Soc. Neurosci. Abstr. 32.
43. Hanagasioglu, M., and Borbely, A. A. (1982). Effect of voluntary locomotor activity on sleep in the rat. Behav. Brain Res. 4, 359-368. doi: 10.1016/0166-4328(82)90060-2.
44. Hardebo, J. E., Falck, B., Owman, C., and Rosengren, E. (1979). Studies on the enzymatic blood-brain barrier: quantitative measurements of DOPA decarboxylase in the wall of microvessels as related to the parenchyma in various CNS regions. Acta Physiol. Scand. 105, 453-460. doi: 10.1111/j.1748-1716.1979.tb00110.x.
45. Hayes, H. B., Chang, Y. H., and Hochman, S. (2009). An in vitro spinal cord-hindlimb preparation for studying behaviorally relevant rat locomotor function. J. Neurophysiol. 101, 1114-1122. doi: 10.1152/jn.90523.2008.
46. Ho, H. T., Pan, Y., Cui, Z., Duan, H., Swaan, P. W., and Wang, J. (2011). Molecular analysis and structure-activity relationship modeling of the substrate/inhibitor interaction site of plasma membrane monoamine transporter. J. Pharmacol. Exp. Ther. 339, 376-385. doi: 10.1124/jpet.111.184036.
47. Hochman, S., Garraway, S. M., Machacek, D. W., and Shay, B. L. (2001). "5-HT receptors and the neuromodulatory control of spinal cord function," in Motor Neurobiology of the Spinal Cord, ed T. C. Cope (Boca Raton: CRC Press), 47-87.
48. Hochman, S., Gozal, E. A., Hayes, H. B., Anderson, J. T., Deweerth, S. P., and Chang, Y. H. (2012). Enabling techniques for in vitro studies on mammalian spinal locomotor mechanisms. Front. Biosci. 17, 2158-2180. doi: 10.2741/4043.
49. Hochman, S., Jordan, L. M., and Macdonald, J. F. (1994). N-methyl-D-aspartate receptor-mediated voltage oscillations in neurons surrounding the central canal in slices of rat spinal cord. J. Neurophysiol. 72, 565-577.
50. Jacobs, B. L., and Fornal, C. A. (1993). 5-HT and motor control: a hypothesis. Trends Neurosci. 16, 346-352. doi: 10.1016/0166-2236(93)90090-9.
51. Jaeger, C. B., Ruggiero, D. A., Albert, V. R., Joh, T. H., and Reis, D. J. (1984). "Immunocytochemical localization of aromatic-L-amino acid decarboxylase," in Handbook of Chemical Neuroanatomy, Vol. 2, Classical Transmitters in the CNS, Part 1, eds A. Bjorkland and T. Hokfelt (Amsterdam: Elsevier), 387-408.
52. Jaeger, C. B., Teitelman, G., Joh, T. H., Albert, V. R., Park, D. H., and Reis, D. J. (1983). Some neurons of the rat central nervous system contain aromatic-L-amino-acid decarboxylase but not monoamines. Science 219, 1233-1235. doi: 10.1126/science.6131537.
53. Jonker, J. W., and Schinkel, A. H. (2004). Pharmacological and physiological functions of the polyspecific organic cation transporters: OCT1, 2, and 3 (SLC22A1-3). J. Pharmacol. Exp. Ther. 308, 2-9. doi: 10.1124/jpet.103.053298.
54. Jung, N., Lehmann, C., Rubbert, A., Knispel, M., Hartmann, P., Van Lunzen, J., et al. (2008). Relevance of the organic cation transporters 1 and 2 for antiretroviral drug therapy in human immunodeficiency virus infection. Drug Metab. Dispos. 36, 1616-1623. doi: 10.1124/dmd.108.020826.
55. Juorio, A. V. (1979). Drug-induced changes in the formation, storage and metabolism of tyramine in the mouse. Br. J. Pharmacol. 66, 377-384. doi: 10.1111/j.1476-5381.1979.tb10841.x.
56. Juorio, A. V. (1980). Effects of molindone and fluphenazine on the brain concentration of some phenolic and catecholic amines in the mouse and the rat. Br. J. Pharmacol. 70, 475-480. doi: 10.1111/j.1476-5381.1980.tb08726.x.
57. Juorio, A. V. (1988). "Brain beta-phenylethylamine: localization, pathways, and interrelation with catecholamines," in Progress in Catecholamine Research, eds A. Dahlstrom, M. Sandler, and R. Belmarker (New York, NY: Alan R. Liss), 433-437.
58. Karoum, F., Nasrallah, H., Potkin, S., Chuang, L., Moyer-Schwing, J., Phillips, I., et al. (1979). Mass fragmentography of phenylethylamine, m-and p-tyramine and related amines in plasma, cerebrospinal fluid, urine, and brain. J. Neurochem. 33, 201-212. doi: 10.1111/j.1471-4159.1979.tb11722.x.
59. Katz, P. S., and Clemens, S. (2001). Biochemical networks in nervous systems: expanding neuronal information capacity beyond voltage signals. Trends Neurosci. 24, 18-25. doi: 10.1016/S0166-2236(00)01686-6.
60. Kiehn, O. (2006). Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29, 279-306. doi: 10.1146/annurev.neuro.29.051605.112910.
61. Kiehn, O., and Kjaerulff, O. (1996). Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J. Neurophysiol. 75, 1472-1482.
62. Kiehn, O., and Kjaerulff, O. (1998). Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann. N.Y. Acad. Sci. 860, 110-129. doi: 10.1111/j.1749-6632.1998.tb09043.x.
63. Kiehn, O., Sillar, K. T., Kjaerulff, O., and McDearmid, J. R. (1999). Effects of noradrenaline on locomotor rhythm-generating networks in the isolated neonatal rat spinal cord. J. Neurophysiol. 82, 741-746.
64. Kitazawa, T., Saito, K., and Ohga, A. (1985). Effects of catecholamines on spinal motoneurones and spinal reflex discharges in the isolated spinal cord of the newborn rat. Brain Res. 351, 31-36. doi: 10.1016/0165-3806(85)90228-7.
65. Kjaerulff, O., Barajon, I., and Kiehn, O. (1994). Sulphorhodamine-labelled cells in the neonatal rat spinal cord following chemically induced locomotor activity in vitro. J. Physiol. 478(Pt 2), 265-273.
66. Kjaerulff, O., and Kiehn, O. (1996). Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord in vitro: a lesion study. J. Neurosci. 16, 5777-5794.
67. Kremer, E., and Lev, T. A. (1997). Localization of the spinal network associated with generation of hindlimb locomotion in the neonatal rat and organization of its transverse coupling system. J. Neurophysiol. 77, 1155-1170.
68. Leo, D., Mus, L., Espinoza, S., Hoener, M. C., Sotnikova, T. D., and Gainetdinov, R. R. (2014). Taar1-mediated modulation of presynaptic dopaminergic neurotransmission: role of D2 dopamine autoreceptors. Neuropharmacology 81, 283-291. doi: 10.1016/j.neuropharm.2014.02.007.
69. Li, Y., Li, L., Stephens, M. J., Zenner, D., Murray, K. C., Winship, I. R., et al. (2014). Synthesis, transport, and metabolism of serotonin formed from exogenously applied 5-HTP after spinal cord injury in rats. J. Neurophysiol. 111, 145-163. doi: 10.1152/jn.00508.2013.
70. Lindemann, L., Meyer, C. A., Jeanneau, K., Bradaia, A., Ozmen, L., Bluethmann, H., et al. (2008). Trace amine-associated receptor 1 modulates dopaminergic activity. J. Pharmacol. Exp. Ther. 324, 948-956. doi: 10.1124/jpet.107.132647.
71. Liu, J., Akay, T., Hedlund, P. B., Pearson, K. G., and Jordan, L. M. (2009). Spinal 5-HT7 receptors are critical for alternating activity during locomotion: in vitro neonatal and in vivo adult studies using 5-HT7 receptor knockout mice. J. Neurophysiol. 102, 337-348. doi: 10.1152/jn.91239.2008.
72. Liu, J., and Jordan, L. M. (2005). Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. J. Neurophysiol. 94, 1392-1404. doi: 10.1152/jn.00136.2005.
73. Madriaga, M. A., McPhee, L. C., Chersa, T., Christie, K. J., and Whelan, P. J. (2004). Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J. Neurophysiol. 92, 1566-1576. doi: 10.1152/jn.01181.2003.
74. Mandela, P., Chandley, M., Xu, Y. Y., Zhu, M. Y., and Ordway, G. A. (2010). Reserpine-induced reduction in norepinephrine transporter function requires catecholamine storage vesicles. Neurochem. Int. 56, 760-767. doi: 10.1016/j.neuint.2010.02.011.
75. Mann, R., and Bell, C. (1991). Neuronal metabolism and DOPA decarboxylase immunoreactivity in terminal noradrenergic sympathetic axons of rat. J. Histochem. Cytochem. 39, 663-668. doi: 10.1177/39.5.1673138.
76. Martin, L. L., Baker, G. B., and Wood, P. L. (1988). "Tryptamine turnover: effects of drugs," in Trace Amines: Comparative and Clinical Neurobiology, eds A. A. Boulton, A. V. Juorio, and R. G. H. Downer (New Jersey, NJ: Humana Press), 95-104, 57-174.
77. Matsushima, T., and Grillner, S. (1992). Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. J. Neurophysiol. 67, 373-388.
78. Merchenthaler, I. (1991). Neurons with access to the general circulation in the central nervous system of the rat: a retrograde tracing study with fluoro-gold. Neuroscience 44, 655-662. doi: 10.1016/0306-4522(91)90085-3.
79. Millan, M. J. (2002). Descending control of pain. Prog. Neurobiol. 66, 355-474. doi: 10.1016/S0301-0082(02)00009-6.
80. Miller, G. M. (2011). The emerging role of trace amine-associated receptor 1 in the functional regulation of monoamine transporters and dopaminergic activity. J. Neurochem. 116, 164-176. doi: 10.1111/j.1471-4159.2010.07109.x.
81. Murray, K. C., Stephens, M. J., Ballou, E. W., Heckman, C. J., and Bennett, D. J. (2011). Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J. Neurophysiol. 105, 731-748. doi: 10.1152/jn.00774.2010.
82. Nagatsu, I., Sakai, M., Yoshida, M., and Nagatsu, T. (1988). Aromatic L-amino acid decarboxylase-immunoreactive neurons in and around the cerebrospinal fluid-contacting neurons of the central canal do not contain dopamine or serotonin in the mouse and rat spinal cord. Brain Res. 475, 91-102. doi: 10.1016/0006-8993(88)90202-8.
83. Nguyen, T. V., and Juorio, A. V. (1989). Binding sites for brain trace amines. Cell. Mol. Neurobiol. 9, 297-311. doi: 10.1007/BF00711411.
84. Ono, H., Ito, H., and Fukuda, H. (1991). 2-phenylethylamine and methamphetamine enhance the spinal monosynaptic reflex by releasing noradrenaline from the terminals of descending fibers. Jpn. J. Pharmacol. 55, 359-366. doi: 10.1254/jjp.55.359.
85. Pacifico, R., Dewan, A., Cawley, D., Guo, C., and Bozza, T. (2012). An olfactory subsystem that mediates high-sensitivity detection of volatile amines. Cell Rep. 2, 76-88. doi: 10.1016/j.celrep.2012.06.006.
86. Panas, M. W., Xie, Z., Panas, H. N., Hoener, M. C., Vallender, E. J., and Miller, G. M. (2012). Trace amine associated receptor 1 signaling in activated lymphocytes. J. Neuroimmune Pharmacol. 7, 866-876. doi: 10.1007/s11481-011-9321-4.
87. Paulos, M. A., and Tessel, R. E. (1982). Excretion of beta-phenethylamine is elevated in humans after profound stress. Science 215, 1127-1129. doi: 10.1126/science.7063846.
88. Peddi, S., Roth, B. L., Glennon, R. A., and Westkaemper, R. B. (2003). Spiro[9,10-dihydroanthracene]-9,3′-pyrrolidine-a structurally unique tetracyclic 5-HT2A receptor antagonist. Eur. J. Pharmacol. 482, 335-337. doi: 10.1016/j.ejphar.2003.09.059.
89. Pfeil, U., Kuncova, J., Bruggmann, D., Paddenberg, R., Rafiq, A., Henrich, M., et al. (2014). Intrinsic vascular dopamine-a key modulator of hypoxia-induced vasodilation in splanchnic vessels. J. Physiol. 592(Pt 8), 1745-1756. doi: 10.1113/jphysiol.2013.262626.
90. Philips, S. R., Davis, B. A., Durden, D. A., and Boulton, A. A. (1975). Identification and distribution of m-tyramine in the rat. Can. J. Biochem. 53, 65-69. doi: 10.1139/o75-010.
91. Philips, S. R., Durden, D. A., and Boulton, A. A. (1974a). Identification and distribution of p-tyramine in the rat. Can. J. Biochem. 52, 366-373. doi: 10.1139/o74-055.
92. Philips, S. R., Durden, D. A., and Boulton, A. A. (1974b). Identification and distribution of tryptamine in the rat. Can. J. Biochem. 52, 447-451. doi: 10.1139/o74-068.
93. Premont, R. T., Gainetdinov, R. R., and Caron, M. G. (2001). Following the trace of elusive amines. Proc. Natl. Acad. Sci. U.S.A. 98, 9474-9475. doi: 10.1073/pnas.181356198.
94. Reddy, S. V., Maderdrut, J. L., and Yaksh, T. L. (1980). Spinal cord pharmacology of adrenergic agonist-mediated antinociception. J. Pharmacol. Exp. Ther. 213, 525-533.
95. Rekling, J. C., Funk, G. D., Bayliss, D. A., Dong, X. W., and Feldman, J. L. (2000). Synaptic control of motoneuronal excitability. Physiol. Rev. 80, 767-852.
96. Revel, F. G., Moreau, J. L., Gainetdinov, R. R., Bradaia, A., Sotnikova, T. D., Mory, R., et al. (2011). TAAR1 activation modulates monoaminergic neurotransmission, preventing hyperdopaminergic and hypoglutamatergic activity. Proc. Natl. Acad. Sci. U.S.A. 108, 8485-8490. doi: 10.1073/pnas.1103029108.
97. Reynolds, I. J., and Aizenman, E. (1992). Pentamidine is an N-methyl-D-aspartate receptor antagonist and is neuroprotective in vitro. J. Neurosci. 12, 970-975.
98. Reynolds, I. J., Zeleski, D. M., Rothermund, K. D., Hartnett, K. A., Tidwell, R., and Aizenman, E. (1993). Studies on the effects of several pentamidine analogues on the NMDA receptor. Eur. J. Pharmacol. Mol. Pharmacol. 244, 175-179. doi: 10.1016/0922-4106(93)90023-3.
99. Saavedra, J. M. (1989). "á-phenylethylamine, phenylethanoamine, tyramine and octopamine," in Catecholamines II, eds U. Trendelenburg and N. Weiner (Berlin: Springer-Verlag), 181-210.
100. Schmidt, B. J., Hochman, S., and Maclean, J. N. (1998). NMDA receptor-mediated oscillatory properties: potential role in rhythm generation in the mammalian spinal cord. Ann. N.Y. Acad. Sci. 860, 189-202. doi: 10.1111/j.1749-6632.1998.tb09049.x.
101. Schmidt, B. J., and Jordan, L. M. (2000). The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull. 53, 689-710. doi: 10.1016/S0361-9230(00)00402-0.
102. Schomig, E., Lazar, A., and Grundemann, D. (2006). Extraneuronal monoamine transporter and organic cation transporters 1 and 2: a review of transport efficiency. Handb. Exp. Pharmacol. 151-180. doi: 10.1007/3-540-29784-7_8.
103. Shen, Y., Monsma, F. J. Jr., Metcalf, M. A., Jose, P. A., Hamblin, M. W., and Sibley, D. R. (1993). Molecular cloning and expression of a 5-hydroxytryptamine7 serotonin receptor subtype. J. Biol. Chem. 268, 18200-18204.
104. Shreckengost, J., Calvo, J., Quevedo, J., and Hochman, S. (2010). Bicuculline-sensitive primary afferent depolarization remains after greatly restricting synaptic transmission in the mammalian spinal cord. J. Neurosci. 30, 5283-5288. doi: 10.1523/JNEUROSCI.3873-09.2010.
105. Spector, S., Melmon, K., Lovenberg, W., and Sjoerdsma, A. (1963). The presence and distribution of tyramine in mammalian tissues. J. Pharmacol. Exp. Ther. 140, 229-235.
106. Sqalli-Houssaini, Y., and Cazalets, J. R. (2000). Noradrenergic control of locomotor networks in the in vitro spinal cord of the neonatal rat. Brain Res. 852, 100-109. doi: 10.1016/S0006-8993(99)02219-2.
107. Sqalli-Houssaini, Y., Cazalets, J. R., and Clarac, F. (1993). Oscillatory properties of the central pattern generator for locomotion in neonatal rats. J. Neurophysiol. 70, 803-813.
108. Tazerart, S., Vinay, L., and Brocard, F. (2008). The persistent sodium current generates pacemaker activities in the central pattern generator for locomotion and regulates the locomotor rhythm. J. Neurosci. 28, 8577-8589. doi: 10.1523/JNEUROSCI.1437-08.2008.
109. Toll, L., Berzetei-Gurske, I. P., Polgar, W. E., Brandt, S. R., Adapa, I. D., Rodriguez, L., et al. (1998). Standard binding and functional assays related to medications development division testing for potential cocaine and opiate narcotic treatment medications. NIDA Res. Monogr. 178, 440-466.
110. Torres, G. E., Gainetdinov, R. R., and Caron, M. G. (2003). Plasma membrane monoamine transporters: structure, regulation and function. Nat. Rev. Neurosci. 4, 13-25. doi: 10.1038/nrn1008.
111. U'Prichard, D. C., Greenberg, D. A., and Snyder, S. H. (1977). Binding characteristics of a radiolabeled agonist and antagonist at central nervous system alpha noradrenergic receptors. Mol. Pharmacol. 13, 454-473.
112. Whelan, P., Bonnot, A., and O'Donovan, M. J. (2000). Properties of rhythmic activity generated by the isolated spinal cord of the neonatal mouse. J. Neurophysiol. 84, 2821-2833.
113. Wienecke, J., Ren, L. Q., Hultborn, H., Chen, M., Moller, M., Zhang, Y., et al. (2014). Spinal cord injury enables aromatic l-amino acid decarboxylase cells to synthesize monoamines. J. Neurosci. 34, 11984-12000. doi: 10.1523/JNEUROSCI.3838-13.2014.
114. Wolinsky, T. D., Swanson, C. J., Smith, K. E., Zhong, H., Borowsky, B., Seeman, P., et al. (2007). The Trace Amine 1 receptor knockout mouse: an animal model with relevance to schizophrenia. Genes Brain Behav. 6, 628-639. doi: 10.1111/j.1601-183X.2006.00292.x.
115. Wyart, C., Del Bene, F., Warp, E., Scott, E. K., Trauner, D., Baier, H., et al. (2009). Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 461, 407-410. doi: 10.1038/nature08323.
116. Xie, Z., and Miller, G. M. (2008). Beta-phenylethylamine alters monoamine transporter function via trace amine-associated receptor 1: implication for modulatory roles of trace amines in brain. J. Pharmacol. Exp. Ther. 325, 617-628. doi: 10.1124/jpet.107.134247.
117. Xie, Z., Vallender, E. J., Yu, N., Kirstein, S. L., Yang, H., Bahn, M. E., et al. (2008). Cloning, expression, and functional analysis of rhesus monkey trace amine-associated receptor 6: evidence for lack of monoaminergic association. J. Neurosci. Res. 86, 3435-3446. doi: 10.1002/jnr.21783.
118. Xie, Z., Westmoreland, S. V., Bahn, M. E., Chen, G. L., Yang, H., Vallender, E. J., et al. (2007). Rhesus monkey trace amine-associated receptor 1 signaling: enhancement by monoamine transporters and attenuation by the D2 autoreceptor in vitro. J. Pharmacol. Exp. Ther. 321, 116-127. doi: 10.1124/jpet.106.116863.
119. Yamamoto, H., Kamegaya, E., Hagino, Y., Imai, K., Fujikawa, A., Tamura, K., et al. (2007). Genetic deletion of vesicular monoamine transporter-2 (VMAT2) reduces dopamine transporter activity in mesencephalic neurons in primary culture. Neurochem. Int. 51, 237-244. doi: 10.1016/j.neuint.2007.06.022.
120. Zar, J. H. (1999). Biostatistical Analysis: Upper Saddle River. New Jersey, NJ: Prentice Hall.
121. Zhu, H., Clemens, S., Sawchuk, M., and Hochman, S. (2007). Expression and distribution of all dopamine receptor subtypes (D(1)-D(5)) in the mouse lumbar spinal cord: a real-time polymerase chain reaction and non-autoradiographic in situ hybridization study. Neuroscience 149, 885-897. doi: 10.1016/j.neuroscience.2007.07.052.
122. Zimmerman, A. L., Sawchuk, M., and Hochman, S. (2012). Monoaminergic modulation of spinal viscero-sympathetic function in the neonatal mouse thoracic spinal cord. PLoS ONE 7:e47213. doi: 10.1371/journal.pone.0047213.