Advertisement

Identification of TAAR5 Agonist Activity of Alpha-NETA and Its Effect on Mismatch Negativity Amplitude in Awake Rats

  • Aleksander A. Aleksandrov
  • Veronika M. Knyazeva
  • Anna B. Volnova
  • Elena S. Dmitrieva
  • Olga Korenkova
  • Stefano Espinoza
  • Andrey Gerasimov
  • Raul R. Gainetdinov
ORIGINAL ARTICLE

Abstract

Mismatch negativity (MMN) is a well-defined component of human event-related potentials that reflects the pre-attentive, stimulus-discrimination process and is associated with involuntary switching of attention. MMN-like responses detected in animal models provide an opportunity to investigate the neural mechanisms of this process that involves several neurotransmitter and neuromodulator systems. Trace amines are believed to play a significant role in neuromodulation of synaptic transmission. The present study aimed to determine the role of trace amine-associated receptor 5 (TAAR5) in the MMN-like response in rats. First, using a bioluminescence resonance energy transfer (BRET) cAMP biosensor, we performed unbiased screening of TAAR5 ligands from a commercially available compound library (661 compounds) and identified 2-(alpha-naphthoyl)ethyltrimethylammonium iodide (alpha-NETA) as a potent (EC50 150 nM) TAAR5 agonist. Then, we recorded auditory event-related potentials during an oddball paradigm in awake freely moving rats that were intraperitoneally injected with a vehicle or two doses of the putative TAAR5 agonist alpha-NETA. The MMN-like response was increased by alpha-NETA 3 mg/kg dose, but not by 1 mg/kg dose or 0.9% saline solution. These results suggest that the MMN-like response in rats may be modulated, at least in part, through TAAR5-dependent processes.

Keywords

Trace amine-associated receptors TAAR5 2-(Alpha-naphthoyl)ethyltrimethylammonium iodide (alpha-NETA) Mismatch negativity (MMN) Oddball paradigm Awake rats 

Notes

Funding Information

This study was supported by a grant from the Russian Foundation of Basic Research (Project № 17-04-00082 to AAA). BRET assay screening was supported by the Russian Science Foundation grant № 14-50-00069 to RRG and AG.

Compliance with Ethical Standards

All animal studies were carried out in strict accordance with the guidelines of the Ministry of Health of Russian Federation and the principles adopted by the FELASA and RusLASA organizations of laboratory animal use. All experiments were approved by the Saint Petersburg State University Ethical Committee for Animal Research (approval number 131-03-4). All surgical procedures were performed under anesthesia, and all efforts were made to minimize suffering.

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

12640_2018_9902_MOESM1_ESM.docx (56 kb)
ESM 1 (DOCX 56 kb)

References

  1. Ahmed M, Mällo T, Leppänen PHT, Hämäläinen J, Äyräväinen L, Ruusuvirta T, Astikainen P (2011) Mismatch brain response to speech sound changes in rats. Front Psychol 2.  https://doi.org/10.3389/fpsyg.2011.00283
  2. Ahveninen J, Kähkönen S, Pennanen S, Liesivuori J, Ilmoniemi RJ, Jääskeläinen IP (2002) Tryptophan depletion effects on EEG and MEG responses suggest serotonergic modulation of auditory involuntary attention in humans. NeuroImage 16:1052–1061.  https://doi.org/10.1006/nimg.2002.1142 CrossRefPubMedGoogle Scholar
  3. Astikainen P, Stefanics G, Nokia M, Lipponen A, Cong F, Penttonen M, Ruusuvirta T (2011) Memory-based mismatch response to frequency changes in rats. PLoS One 6:e24208.  https://doi.org/10.1371/journal.pone.0024208 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baldeweg T, Wong D, Stephan KE (2006) Nicotinic modulation of human auditory sensory memory: evidence from mismatch negativity potentials. Int J Psychophysiol 59:49–58.  https://doi.org/10.1016/j.ijpsycho.2005.07.014 CrossRefPubMedGoogle Scholar
  5. Barak LS, Salahpour A, Zhang X, Masri B, Sotnikova TD, Ramsey AJ, Violin JD, Lefkowitz RJ, Caron MG, Gainetdinov RR (2008) Pharmacological characterization of membrane-expressed human trace amine-associated receptor 1 (TAAR1) by a bioluminescence resonance energy transfer cAMP biosensor. Mol Pharmacol 74:585–594.  https://doi.org/10.1124/mol.108.048884 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Berry MD (2004) Mammalian central nervous system trace amines. Pharmacologic amphetamines, physiologic neuromodulators. J Neurochem 90:257–271.  https://doi.org/10.1111/j.1471-4159.2004.02501.x CrossRefPubMedGoogle Scholar
  7. Boulton AA (1980) Trace amines and mental disorders. Can J Neurol Sci / J Can des Sci Neurol 7:261–263.  https://doi.org/10.1017/S0317167100023313 CrossRefGoogle Scholar
  8. Branchek TA, Blackburn TP (2003) Trace amine receptors as targets for novel therapeutics: legend, myth and fact. Curr Opin Pharmacol 3:90–97.  https://doi.org/10.1016/S1471-4892(02)00028-0 CrossRefPubMedGoogle Scholar
  9. Bröcher S, Artola A, Singer W (1992) Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res 573:27–36.  https://doi.org/10.1016/0006-8993(92)90110-U CrossRefPubMedGoogle Scholar
  10. Csépe V, Juckel G, Molnár M, Karmos G (1994) Stimulus-related oscillatory responses in the auditory cortex of cats. In: Pantev C., Elbert T., Lütkenhöner B. (eds) Oscillatory event-related brain dynamics. Springer, Boston, MA, pp. 383–388Google Scholar
  11. Csépe V, Karmos G, Molnár M (1989) Subcortical evoked potential correlates of early information processing: mismatch negativity in cats. In: Basar E, Bullock TH (eds) Brain dynamics. Springer-Verlag, Berlin Heidelberg, pp 279–289CrossRefGoogle Scholar
  12. Dinter J, Mühlhaus J, Wienchol CL, Yi CX, Nürnberg D, Morin S, Grüters A, Köhrle J, Schöneberg T, Tschöp M, Krude H, Kleinau G, Biebermann H (2015) Inverse agonistic action of 3-iodothyronamine at the human trace amine-associated receptor 5. PLoS One 10:e0117774.  https://doi.org/10.1371/journal.pone.0117774 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dulude L, Labelle A, Knott VJ (2010) Acute nicotine alteration of sensory memory impairment in smokers with schizophrenia. J Clin Psychopharmacol 30:541–548.  https://doi.org/10.1097/JCP.0b013e3181f0c9c6 CrossRefPubMedGoogle Scholar
  14. Dunbar G, Boeijinga PH, Demazieres A, Cisterni C, Kuchibhatla R, Wesnes K et al (2007) Effects of TC-1734 (AZD3480), a selective neuronal nicotinic receptor agonist, on cognitive performance and the EEG of young healthy male volunteers. Psychopharmacology 191:919–929.  https://doi.org/10.1007/s00213-006-0675-x CrossRefPubMedGoogle Scholar
  15. Engeland C, Mahoney C, Mohr E, Ilivitsky V, Knott VJ (2002) Acute nicotine effects on auditory sensory memory in tacrine-treated and nontreated patients with Alzheimer’s disease: an event-related potential study. Pharmacol Biochem Behav 72:457–464.  https://doi.org/10.1016/S0091-3057(02)00711-6 CrossRefPubMedGoogle Scholar
  16. Eriksson J, Villa AE (2005) Event-related potentials in an auditory oddball situation in the rat. Biosystems 79(12):207–212.  https://doi.org/10.1016/j.biosystems.2004.09.017 CrossRefPubMedGoogle Scholar
  17. Espinoza S, Lignani G, Caffino L, Maggi S, Sukhanov I, Leo D, Mus L, Emanuele M, Ronzitti G, Harmeier A, Medrihan L, Sotnikova TD, Chieregatti E, Hoener MC, Benfenati F, Tucci V, Fumagalli F, Gainetdinov RR (2015) TAAR1 modulates cortical glutamate NMDA receptor function. Neuropsychopharmacology 40:2217–2227.  https://doi.org/10.1038/npp.2015.65 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Evstigneeva MD, Alexandrov AA, Mathiassen SE, Lyskov E (2010) Muscle contraction force and fatigue: effects on mismatch negativity. Neuroreport 21:1152–1156.  https://doi.org/10.1097/WNR.0b013e328340cc66 CrossRefPubMedGoogle Scholar
  19. Featherstone RE, Shin R, Kogan JH, Liang Y, Matsumoto M, Siegel SJ (2015) Mice with subtle reduction of NMDA NR1 receptor subunit expression have a selective decrease in mismatch negativity: implications for schizophrenia prodromal population. Neurobiol Dis 73:289–295.  https://doi.org/10.1016/j.nbd.2014.10.010 CrossRefPubMedGoogle Scholar
  20. Fisher DJ, Grant B, Smith DM, Borracci G, Labelle A, Knott VJ (2012) Nicotine and the hallucinating brain: effects on mismatch negativity (MMN) in schizophrenia. Psychiatry Res 196:181–187.  https://doi.org/10.1016/j.psychres.2012.01.026 CrossRefPubMedGoogle Scholar
  21. Graham KL, Zhang JV, Lewén S, Burke TM, Dang T, Zoudilova M, Sobel RA, Butcher EC, Zabel BA (2014) A novel CMKLR1 small molecule antagonist suppresses CNS autoimmune inflammatory disease. PLoS One 9:e112925.  https://doi.org/10.1371/journal.pone.0112925 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815–835.  https://doi.org/10.1016/S0306-4522(02)00026-X CrossRefPubMedGoogle Scholar
  23. Harms L, Fulham WR, Todd J, Budd TW, Hunter M, Meehan C, Penttonen M, Schall U, Zavitsanou K, Hodgson DM, Michie PT (2014) Mismatch negativity (MMN) in freely-moving rats with several experimental controls. PLoS One 9:e110892.  https://doi.org/10.1371/journal.pone.0110892 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Harms L, Fulham WR, Todd J, Meehan C, Schall U, Hodgson DM, Michie PT (2017) Late deviance detection in rats is reduced, while early deviance detection is augmented by the NMDA receptor antagonist MK-801. Schizophr Res doi 191:43–50.  https://doi.org/10.1016/j.schres.2017.03.042 CrossRefGoogle Scholar
  25. Harms L, Michie PT, Näätänen R (2016) Criteria for determining whether mismatch responses exist in animal models: focus on rodents. Biol Psychol 116:28–35.  https://doi.org/10.1016/j.biopsycho.2015.07.006 CrossRefPubMedGoogle Scholar
  26. Howell TJ, Conduit R, Toukhsati S, Bennett P (2012) Auditory stimulus discrimination recorded in dogs, as indicated by mismatch negativity (MMN). Behav Process 89:8–13.  https://doi.org/10.1016/j.beproc.2011.09.009 CrossRefGoogle Scholar
  27. Inami R, Kirino E, Inoue R, Arai H (2005) Transdermal nicotine administration enhances automatic auditory processing reflected by mismatch negativity. Pharmacol Biochem Behav 80:453–461.  https://doi.org/10.1016/j.pbb.2005.01.001 CrossRefPubMedGoogle Scholar
  28. Javit DC, Steinschneider M, Schroeder CE, Vaughan HG, Arezzo JC (1994) Detection of stimulus deviance within primate primary auditory cortex: intracortical mechanisms of mismatch negativity (MMN) generation. Brain Res 667:192–200.  https://doi.org/10.1016/0006-8993(94)91496-6 CrossRefGoogle Scholar
  29. Javitt DC, Doneshka P, Zylberman I, Ritter W, Vaughan HG (1993) Impairment of early cortical processing in schizophrenia: an event-related potential confirmation study. Biol Psychiatry 33:513–519.  https://doi.org/10.1016/0006-3223(93)90005-X CrossRefPubMedGoogle Scholar
  30. Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci U S A 93:11962–11967.  https://doi.org/10.1073/pnas.93.21.11962 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Jung F, Stephan KE, Backes H, Moran R, Gramer M, Kumagai T, Graf R, Endepols H, Tittgemeyer M (2013) Mismatch responses in the awake rat: evidence from epidural recordings of auditory cortical fields. PLoS One 8:e63203.  https://doi.org/10.1371/journal.pone.0063203 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kähkönen S, Ahveninen J, Jääskeläinen IP, Kaakkola S, Näätänen R, Huttunen J, Pekkonen E (2001) Effects of haloperidol on selective attention: a combined whole-head MEG and high-resolution EEG study. Neuropsychopharmacology 25:498–504.  https://doi.org/10.1016/S0893-133X(01)00255-X CrossRefPubMedGoogle Scholar
  33. Kähkönen S, Mäkinen V, Jääskeläinen IP, Pennanen S, Liesivuori J, Ahveninen J (2005) Serotonergic modulation of mismatch negativity. Psychiatry Res - Neuroimaging 138:61–74.  https://doi.org/10.1016/j.pscychresns.2004.09.006 CrossRefGoogle Scholar
  34. Karl A, Malta LS, Maercker A (2006) Meta-analytic review of event-related potential studies in post-traumatic stress disorder. Biol Psychol 71:123–147.  https://doi.org/10.1016/j.biopsycho.2005.03.004 CrossRefPubMedGoogle Scholar
  35. Khan MZ, Nawaz W (2016) The emerging roles of human trace amines and human trace amine-associated receptors (hTAARs) in central nervous system. Biomed Pharmacother 83:439–449.  https://doi.org/10.1016/j.biopha.2016.07.002 CrossRefPubMedGoogle Scholar
  36. Kohlhaas KL, Robb HM, Roderwald VA, Rueter LE (2015) Nicotinic modulation of auditory evoked potential electroencephalography in a rodent neurodevelopmental model of schizophrenia. Biochem Pharmacol 97:482–487.  https://doi.org/10.1016/j.bcp.2015.05.011 CrossRefPubMedGoogle Scholar
  37. Kraus N, McGee T, Littman T, Nicol T, King C (1994) Nonprimary auditory thalamic representation of acoustic change. J Neurophysiol 72:1270–1277.  https://doi.org/10.1152/jn.1994.72.3.1270 CrossRefPubMedGoogle Scholar
  38. Kreitschmann-Andermahr I, Rosburg T, Demme U, Gaser E, Nowak H, Sauer H (2001) Effect of ketamine on the neuromagnetic mismatch field in healthy humans. Cogn Brain Res 12:109–116.  https://doi.org/10.1016/S0926-6410(01)00043-X CrossRefGoogle Scholar
  39. Kumar R, Långström B, Darreh-Shori T (2016) Novel ligands of choline acetyltransferase designed by in silico molecular docking, hologram QSAR and lead optimization. Sci Rep 6.  https://doi.org/10.1038/srep31247
  40. Liberles SD (2009) Trace amine-associated receptors are olfactory receptors in vertebrates. Ann N Y Acad Sci 1170:168–172.  https://doi.org/10.1111/j.1749-6632.2009.04014.x CrossRefPubMedGoogle Scholar
  41. Light GA, Braff DL (2005) Mismatch negativity deficits are associated with poor functioning in schizophrenia patients. Arch Gen Psychiatry 62:127–136.  https://doi.org/10.1001/archpsyc.62.2.127 CrossRefPubMedGoogle Scholar
  42. Light GA, Swerdlow NR (2015) Future clinical uses of neurophysiological biomarkers to predict and monitor treatment response for schizophrenia. Ann N Y Acad Sci 1344:105–119.  https://doi.org/10.1111/nyas.12730 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Lindemann L, Meyer CA, Jeanneau K, Bradaia A, Ozmen L, Bluethmann H, Bettler B, Wettstein JG, Borroni E, Moreau JL, Hoener MC (2008) Trace amine-associated receptor 1 modulates dopaminergic activity. J Pharmacol Exp Ther 324:948–956.  https://doi.org/10.1124/jpet.107.132647 CrossRefPubMedGoogle Scholar
  44. Mahmoudzadeh M, Dehaene-Lambertz G, Wallois F (2017) Electrophysiological and hemodynamic mismatch responses in rats listening to human speech syllables. PLoS One 12:e0173801.  https://doi.org/10.1371/journal.pone.0173801 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Martin LF, Davalos DB, Kisley MA (2009) Nicotine enhances automatic temporal processing as measured by the mismatch negativity waveform. Nicotine Tob Res 11:698–706.  https://doi.org/10.1093/ntr/ntp052 CrossRefPubMedGoogle Scholar
  46. Michie PT (2001) What has MMN revealed about the auditory system in schizophrenia? Int J Psychophysiol 42:177–194.  https://doi.org/10.1016/S0167-8760(01)00166-0 CrossRefPubMedGoogle Scholar
  47. Miller GM (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.  https://doi.org/10.1111/j.1471-4159.2010.07109.x CrossRefPubMedPubMedCentralGoogle Scholar
  48. Näätänen R (1990) The role of attention in auditory information processing as revealed by event-related potentials and other brain measures of cognitive function. Behav Brain Sci 13:201–233.  https://doi.org/10.1017/S0140525X00078407 CrossRefGoogle Scholar
  49. Näätänen R, Gaillard AWK, Mäntysalo S (1978) Early selective-attention effect on evoked potential reinterpreted. Acta Psychol 42:313–329.  https://doi.org/10.1016/0001-6918(78)90006-9 CrossRefGoogle Scholar
  50. Näätänen R, Jacobsen T, Winkler I (2005) Memory-based or afferent processes in mismatch negativity (MMN): a review of the evidence. Psychophysiology 42:25–32.  https://doi.org/10.1111/j.1469-8986.2005.00256.x CrossRefPubMedGoogle Scholar
  51. Näätänen R, Kähkönen S (2009) Central auditory dysfunction in schizophrenia as revealed by the mismatch negativity (MMN) and its magnetic equivalent MMNm: a review. Int J Neuropsychopharmacol 12:125–135CrossRefPubMedGoogle Scholar
  52. Näätänen R, Kujala T, Winkler I (2011) Auditory processing that leads to conscious perception: a unique window to central auditory processing opened by the mismatch negativity and related responses. Psychophysiology 48:4–22.  https://doi.org/10.1111/j.1469-8986.2010.01114.x CrossRefPubMedGoogle Scholar
  53. Nakamura T, Michie PT, Fulham WR, Todd J, Budd TW, Schall U, Hunter M, Hodgson DM (2011) Epidural auditory event-related potentials in the rat to frequency and duration deviants: evidence of mismatch negativity? Front Psychol 2.  https://doi.org/10.3389/fpsyg.2011.00367
  54. Nelson DA, Tolbert MD, Singh SJ, Bost KL (2007) Expression of neuronal trace amine-associated receptor (Taar) mRNAs in leukocytes. J Neuroimmunol 192:21–30.  https://doi.org/10.1016/j.jneuroim.2007.08.006 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Pei Y, Asif-Malik A, Canales JJ (2016) Trace amines and the trace amine-associated receptor 1: pharmacology, neurochemistry, and clinical implications. Front Neurosci 10:148.  https://doi.org/10.3389/fnins.2016.00148 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Pekkonen E, Jousmäki V, Reinikainen K, Partanen J (1995) Automatic auditory discrimination is impaired in Parkinson’s disease. Electroencephalogr Clin Neurophysiol 95:47–52.  https://doi.org/10.1016/0013-4694(94)00304-4 CrossRefPubMedGoogle Scholar
  57. Revel FG, Moreau JL, Gainetdinov RR, Bradaia A, Sotnikova TD, Mory R, Durkin S, Zbinden KG, Norcross R, Meyer CA, Metzler V, Chaboz S, Ozmen L, Trube G, Pouzet B, Bettler B, Caron MG, Wettstein JG, Hoener MC (2011) TAAR1 activation modulates monoaminergic neurotransmission, preventing hyperdopaminergic and hypoglutamatergic activity. Proc Natl Acad Sci 108:8485–8490.  https://doi.org/10.1073/pnas.1103029108 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Roger C, Hasbroucq T, Rabat A, Vidal F, Burle B (2009) Neurophysics of temporal discrimination in the rat: a mismatch negativity study. Psychophysiology 46:1028–1032.  https://doi.org/10.1111/j.1469-8986.2009.00840.x CrossRefPubMedGoogle Scholar
  59. Rosburg T, Kreitschmann-Andermahr I (2016) The effects of ketamine on the mismatch negativity (MMN) in humans—a meta-analysis. Clin Neurophysiol 127:1387–1394.  https://doi.org/10.1016/j.clinph.2015.10.062 CrossRefPubMedGoogle Scholar
  60. Ruusuvirta T, Korhonen T, Arikoski J, Kivirikko K (1996) Multiple-unit responses to pitch changes in rabbits. Neuroreport 7:1266–1268.  https://doi.org/10.1097/00001756-199605170-00009 CrossRefPubMedGoogle Scholar
  61. Ruusuvirta T, Lipponen A, Pellinen E, Penttonen M, Astikainen P (2013) Auditory cortical and hippocampal-system mismatch responses to duration deviants in urethane-anesthetized rats. PLoS One 8:e54624.  https://doi.org/10.1371/journal.pone.0054624 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ruusuvirta T, Lipponen A, Pellinen EK, Penttonen M, Astikainen P (2015) Auditory cortical and hippocampal local-field potentials to frequency deviant tones in urethane-anesthetized rats: an unexpected role of the sound frequencies themselves. Int J Psychophysiol 96:134–140.  https://doi.org/10.1016/j.ijpsycho.2015.04.007 CrossRefPubMedGoogle Scholar
  63. Ruusuvirta T, Penttonen M, Korhonen T (1998) Auditory cortical event-related potentials to pitch deviances in rats. Neurosci Lett 248:45–48.  https://doi.org/10.1016/S0304-3940(98)00330-9 CrossRefPubMedGoogle Scholar
  64. Sastry BV, Jaiswal N, Owens LK, Janson VE, Moore RD (1988) 2-(alpha-Naphthoyl) ethyltrimethylammonium iodide and its beta-isomer: new selective, stable and fluorescent inhibitors of choline acetyltransferase. J Pharmacol Exp Ther 245:72–80PubMedGoogle Scholar
  65. Sherwani SI, Khan HA (2017) Trace amines in neuropsychiatric disorders. In: Farooqui T, Farooqui AA (ed) Trace amines and neurological disorders. Academic Press, San Diego, pp 269–284Google Scholar
  66. Shiramatsu TI, Kanzaki R, Takahashi H (2013) Cortical mapping of mismatch negativity with deviance detection property in rat. PLoS One 8:e82663.  https://doi.org/10.1371/journal.pone.0082663 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Siegel SJ, Talpos JC, Geyer MA (2013) Animal models and measures of perceptual processing in schizophrenia. Neurosci Biobehav Rev 37:2092–2098.  https://doi.org/10.1016/j.neubiorev.2013.06.016 CrossRefPubMedGoogle Scholar
  68. Sivarao DV, Chen P, Yang Y, Li YW, Pieschl R, Ahlijanian MK (2014) NR2B antagonist CP-101,606 abolishes pitch-mediated deviance detection in awake rats. Front Psychiatry 5.  https://doi.org/10.3389/fpsyt.2014.00096
  69. Stephan KE, Baldeweg T, Friston KJ (2006) Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry 59:929–939.  https://doi.org/10.1016/j.biopsych.2005.10.005 CrossRefPubMedGoogle Scholar
  70. Tikhonravov D, Neuvonen T, Pertovaara A, Savioja K, Ruusuvirta T, Näätänen R, Carlson S (2008) Effects of an NMDA-receptor antagonist MK-801 on an MMN-like response recorded in anesthetized rats. Brain Res 1203:97–102.  https://doi.org/10.1016/j.brainres.2008.02.006 CrossRefPubMedGoogle Scholar
  71. Tikhonravov D, Neuvonen T, Pertovaara A, Savioja K, Ruusuvirta T, Näätänen R, Carlson S (2010) Dose-related effects of memantine on a mismatch negativity-like response in anesthetized rats. Neuroscience 167:1175–1182.  https://doi.org/10.1016/j.neuroscience.2010.03.014 CrossRefPubMedGoogle Scholar
  72. Umbricht D, Koller R, Vollenweider FX, Schmid L (2002) Mismatch negativity predicts psychotic experiences induced by NMDA receptor antagonist in healthy volunteers. Biol Psychiatry 51:400–406.  https://doi.org/10.1016/S0006-3223(01)01242-2 CrossRefPubMedGoogle Scholar
  73. Umbricht D, Schmid L, Koller R, Vollenweider FX, Hell D, Javitt DC (2000) Ketamine-induced deficits in auditory and visual context-dependent processing in healthy volunteers. Arch Gen Psychiatry 57:1139–1147.  https://doi.org/10.1001/archpsyc.57.12.1139 CrossRefPubMedGoogle Scholar
  74. Umbricht D, Vollenweider FX, Schmid L, Grübel C, Skrabo A, Huber T, Koller R (2003) Effects of the 5-HT2Aagonist psilocybin on mismatch negativity generation and AX-continuous performance task: implications for the neuropharmacology of cognitive deficitsin schizophrenia. Neuropsychopharmacology 28:170–181.  https://doi.org/10.1038/sj.npp.1300005 CrossRefPubMedGoogle Scholar
  75. Umbricht D, Vyssotki D, Latanov A, Nitsch R, Lipp HP (2005) Deviance-related electrophysiological activity in mice: is there mismatch negativity in mice? Clin Neurophysiol 116:353–363.  https://doi.org/10.1016/j.clinph.2004.08.015 CrossRefPubMedGoogle Scholar
  76. Wallrabenstein I, Kuklan J, Weber L, Zborala S, Werner M, Altmüller J, Becker C, Schmidt A, Hatt H, Hummel T, Gisselmann G (2013) Human trace amine-associated receptor TAAR5 can be activated by trimethylamine. PLoS One 8:e54950.  https://doi.org/10.1371/journal.pone.0054950 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Zucchi R, Chiellini G, Scanlan TS, Grandy DK (2006) Trace amine-associated receptors and their ligands. Br J Pharmacol 149:967–978Google Scholar
  78. Zucchi R, Accorroni A, Chiellini G (2014) Update on 3-iodothyronamine and its neurological and metabolic actions. Front Physiol 5:402.  https://doi.org/10.3389/fphys.2014.00402 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Aleksander A. Aleksandrov
    • 1
  • Veronika M. Knyazeva
    • 1
  • Anna B. Volnova
    • 2
  • Elena S. Dmitrieva
    • 1
  • Olga Korenkova
    • 3
  • Stefano Espinoza
    • 4
  • Andrey Gerasimov
    • 3
  • Raul R. Gainetdinov
    • 3
    • 5
  1. 1.Department of Higher Nervous Activity and PsychophysiologySaint Petersburg State UniversitySaint PetersburgRussia
  2. 2.Department of General PhysiologySaint Petersburg State UniversitySaint PetersburgRussia
  3. 3.Institute of Translational BiomedicineSaint Petersburg State UniversitySaint PetersburgRussia
  4. 4.Neuroscience and Brain TechnologiesIstituto Italiano di TecnologiaGenoaItaly
  5. 5.Skolkovo Institute of Science and Technology, SkoltechMoscowRussia

Personalised recommendations