#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Methamphetamine regulation of activity and topology of ventral midbrain networks


Autoři: Douglas R. Miller aff001;  Joseph J. Lebowitz aff001;  Dylan T. Guenther aff001;  Alexander J. Refowich aff001;  Carissa Hansen aff001;  Andrew P. Maurer aff001;  Habibeh Khoshbouei aff001
Působiště autorů: Department of Neuroscience, University of Florida, Gainesville, FL, United States of America aff001;  McKnight Brain Institute, University of Florida, Gainesville, FL, United States of America aff002;  Department of Biomedical Engineering, University of Florida, Gainesville, FL, United States of America aff003;  Department of Civil and Coastal Engineering, University of Florida, Gainesville, FL, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222957

Souhrn

The ventral midbrain supports a variety of functions through the heterogeneity of neurons. Dopaminergic and GABA neurons within this region are particularly susceptible targets of amphetamine-class psychostimulants such as methamphetamine. While this has been evidenced through single-neuron methods, it remains unclear whether and to what extent the local neuronal network is affected and if so, by which mechanisms. Both GABAergic and dopaminergic neurons were heavily featured within the primary ventral midbrain network model system. Using spontaneous calcium activity, our data suggest methamphetamine decreased total network output via a D2 receptor-dependent manner. Over culture duration, functional connectivity between neurons decreased significantly but was unaffected by methamphetamine. However, across culture duration, exposure to methamphetamine significantly altered changes in network assortativity. Here we have established primary ventral midbrain networks culture as a viable model system that reveals specific changes in network activity, connectivity, and topology modulation by methamphetamine. This network culture system enables control over the type and number of neurons that comprise a network and facilitates detection of emergent properties that arise from the specific organization. Thus, the multidimensional properties of methamphetamine can be unraveled, leading to a better understanding of its impact on the local network structure and function.

Klíčová slova:

Biology and life sciences – Cell biology – Cellular types – Animal cells – Signal transduction – Cell signaling – Calcium signaling – Neuroscience – Cellular neuroscience – Neurons – Neural networks – Computational neuroscience – Single neuron function – Dopaminergics – Gamma-aminobutyric acid – Anatomy – Brain – Brainstem – Midbrain – Computational biology – Biochemistry – Neurochemistry – Neurochemicals – Neurotransmitters – Biogenic amines – Catecholamines – Dopamine – Hormones – Computer and information sciences – Medicine and health sciences – Physical sciences – Chemistry – Chemical compounds – Organic compounds – Amines – Organic chemistry


Zdroje

1. Di Chiara G, Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 1988;85:5274–8. doi: 10.1073/pnas.85.14.5274 2899326

2. Rice ME. Distinct regional differences in dopamine-mediated volume transmission. Prog. Brain Res., vol. 125, Elsevier; 2000, p. 277–90. doi: 10.1016/S0079-6123(00)25017-6 11098664

3. O’Neill B, Patel JC, Rice ME. Characterization of Optically and Electrically Evoked Dopamine Release in Striatal Slices from Digenic Knock-in Mice with DAT-Driven Expression of Channelrhodopsin. ACS Chem Neurosci 2017;8:310–9. doi: 10.1021/acschemneuro.6b00300 28177213

4. Beckstead MJ, Grandy DK, Wickman K, Williams JT. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 2004;42:939–46. doi: 10.1016/j.neuron.2004.05.019 15207238

5. Branch SY, Beckstead MJ. Methamphetamine produces bidirectional, concentration-dependent effects on dopamine neuron excitability and dopamine-mediated synaptic currents. J Neurophysiol 2012;108:802–9. doi: 10.1152/jn.00094.2012 22592307

6. Jiao D, Liu Y, Li X, Liu J, Zhao M. The role of the GABA system in amphetamine-type stimulant use disorders. Front Cell Neurosci 2015;9:162. doi: 10.3389/fncel.2015.00162 25999814

7. Morales M, Margolis EB. Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat Rev Neurosci 2017;18:73–85. doi: 10.1038/nrn.2016.165 28053327

8. Newman MEJ. The Structure and Function of Complex Networks. SIAM Rev 2003;45:167–256. Pii S0036144503424804\rDoi doi: 10.1137/S003614450342480

9. Rubinov M, Sporns O. Complex network measures of brain connectivity: Uses and interpretations. Neuroimage 2010;52:1059–69. doi: 10.1016/j.neuroimage.2009.10.003 19819337

10. Newman MEJ. Mixing patterns in networks. Phys Rev E 2003;67:026126. doi: 10.1103/PhysRevE.67.026126 12636767

11. Aertsen AMHJ, Gerstein GL, Habib MK, Palm G. Dynamics of Neuronal Firing Correlation: Modulation of "Effective Connectivity" vol. 61. 1989.

12. Teller S, Granell C, De Domenico M, Soriano J, Gómez S, Arenas A. Emergence of Assortative Mixing between Clusters of Cultured Neurons. PLoS Comput Biol 2014;10:e1003796. doi: 10.1371/journal.pcbi.1003796 25188377

13. Bettencourt LMA, Stephens GJ, Ham MI, Gross GW. Functional structure of cortical neuronal networks grown in vitro. Phys Rev E—Stat Nonlinear, Soft Matter Phys 2007;75. doi: 10.1103/PhysRevE.75.021915 17358375

14. Schroeter MS, Charlesworth P, Kitzbichler MG, Paulsen O, Bullmore ET. Emergence of Rich-Club Topology and Coordinated Dynamics in Development of Hippocampal Functional Networks In Vitro. J Neurosci 2015;35:5459–70. doi: 10.1523/JNEUROSCI.4259-14.2015 25855164

15. Bonifazi P, Goldin M, Picardo MA, Jorquera I, Cattani A, Bianconi G, et al. GABAergic hub neurons orchestrate synchrony in developing hippocampal networks. Science 2009;326:1419–24. doi: 10.1126/science.1175509 19965761

16. Margolis EB, Toy B, Himmels P, Morales M, Fields HL. Identification of Rat Ventral Tegmental Area GABAergic Neurons. PLoS One 2012;7:e42365. doi: 10.1371/journal.pone.0042365 22860119

17. Heysieattalab S, Naghdi N, Hosseinmardi N, Zarrindast MR, Haghparast A, Khoshbouei H. Methamphetamine-induced enhancement of hippocampal long-term potentiation is modulated by NMDA and GABA receptors in the shell–accumbens. Synapse 2016;70:325–35. doi: 10.1002/syn.21905 27029021

18. Padgett CL, Lalive AL, Tan KR, Terunuma M, Munoz MB, Pangalos MN, et al. Methamphetamine-evoked depression of GABA(B) receptor signaling in GABA neurons of the VTA. Neuron 2012;73:978–89. doi: 10.1016/j.neuron.2011.12.031 22405207

19. Runfeldt MJ, Sadovsky AJ, MacLean JN. Acetylcholine functionally reorganizes neocortical microcircuits. J Neurophysiol 2014;112:1205–16. doi: 10.1152/jn.00071.2014 24872527

20. Hiolski EM, Ito S, Beggs JM, Lefebvre KA, Litke AM, Smith DR. Domoic acid disrupts the activity and connectivity of neuronal networks in organotypic brain slice cultures. Neurotoxicology 2016;56:215–24. doi: 10.1016/j.neuro.2016.08.004 27506300

21. Pologruto TA, Yasuda R, Svoboda K. Monitoring neural activity and [Ca2+] with genetically encoded Ca2+ indicators. J Neurosci 2004;24:9572–9. doi: 10.1523/JNEUROSCI.2854-04.2004 15509744

22. Sambo D, Lin M, Richardson B, Jagnarine D, Madhurt S, Owens A, et al. The sigma-1 receptor modulates methamphetamine-dysregulated dopamine neurotransmission. FASEB J 2017;31:911–86. doi: 10.1038/s41467-017-02087-x

23. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009;10:186–98. doi: 10.1038/nrn2575 19190637

24. Dechery JB, MacLean JN. Functional triplet motifs underlie accurate predictions of single-trial responses in populations of tuned and untuned V1 neurons. PLoS Comput Biol 2018;14:e1006153. doi: 10.1371/journal.pcbi.1006153 29727448

25. Chambers B, MacLean JN. Higher-Order Synaptic Interactions Coordinate Dynamics in Recurrent Networks. PLoS Comput Biol 2016;12:e1005078. doi: 10.1371/journal.pcbi.1005078 27542093

26. Adhikari S, Curtis PD, Adrian AB, Corchado JC, Comeron JM, Adu-Gyamfi R, et al. Epigenetic regulation in Parkinson’s disease. Sci Rep 2016;7:1–8. doi: 10.1016/j.bios.2016.07.082

27. Goodwin JS, Larson GA, Swant J, Sen N, Javitch JA, Zahniser NR, et al. Amphetamine and methamphetamine differentially affect dopamine transporters in vitro and in vivo. J Biol Chem 2009;284:2978–89. doi: 10.1074/jbc.M805298200 19047053

28. Saha K, Sambo D, Richardson BD, Lin LM, Butler B, Villarroel L, et al. Intracellular methamphetamine prevents the dopamine-induced enhancement of neuronal firing. J Biol Chem 2014;289:22246–57. doi: 10.1074/jbc.M114.563056 24962577

29. Lin M, Sambo D, Khoshbouei H. Methamphetamine Regulation of Firing Activity of Dopamine Neurons. J Neurosci 2016;36:10376–91. doi: 10.1523/JNEUROSCI.1392-16.2016 27707972

30. Sambo DO, Lin M, Owens A, Lebowitz J, Richardson B, Jagnarine D, et al. The sigma-1 receptor modulates methamphetamine dysregulation of dopamine neurotransmission. Nat Commun 2017.

31. Surmeier DJ, Obeso JA, Halliday GM. Selective neuronal vulnerability in Parkinson disease. Nat Rev Neurosci 2017;18:101–13. doi: 10.1038/nrn.2016.178 28104909

32. Chen T-W, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013;499:295–300. doi: 10.1038/nature12354 23868258

33. Mukamel EA, Nimmerjahn A, Schnitzer MJ. Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data. Neuron 2009;63:747–60. doi: 10.1016/j.neuron.2009.08.009 19778505

34. Reznichenko L, Cheng Q, Nizar K, Gratiy SL, Saisan PA, Rockenstein EM, et al. In vivo alterations in calcium buffering capacity in transgenic mouse model of synucleinopathy. J Neurosci 2012;32:9992–8. doi: 10.1523/JNEUROSCI.1270-12.2012 22815513

35. Balkenius A, Johansson AJ, Balkenius C. Comparing Analysis Methods in Functional Calcium Imaging of the Insect Brain. PLoS One 2015;10:e0129614. doi: 10.1371/journal.pone.0129614 26046538

36. Saha K, Sambo D, Richardson BD, Lin LM, Butler B, Villarroel L, et al. Intracellular methamphetamine prevents the dopamine-induced enhancement of neuronal firing. J Biol Chem 2014;289:22246–57. doi: 10.1074/jbc.M114.563056 24962577

37. Vallar L, Meldolesi J. Mechanisms of signal transduction at the dopamine D2 receptor. Trends Pharmacol Sci 1989;10:74–7. doi: 10.1016/0165-6147(89)90082-5 2655242

38. Kravitz A V., Freeze BS, Parker PRL, Kay K, Thwin MT, Deisseroth K, et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010;466:622–6. doi: 10.1038/nature09159 20613723

39. Kravitz A V, Tye LD, Kreitzer AC. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci 2012;15:816–8. doi: 10.1038/nn.3100 22544310

40. Krasnova IN, Justinova Z, Ladenheim B, Jayanthi S, McCoy MT, Barnes C, et al. Methamphetamine self-administration is associated with persistent biochemical alterations in striatal and cortical dopaminergic terminals in the rat. PLoS One 2010;5:e8790. doi: 10.1371/journal.pone.0008790 20098750

41. Moszczynska A, Callan SP. Molecular, Behavioral and Physiological Consequences Methamphetamine Neurotoxicity: Implications for Treatment. J Pharmacol Exp Ther 2017;362:jpet.116.238501. doi: 10.1124/jpet.116.238501 28630283

42. Orsini CA, Colon-Perez LM, Heshmati SC, Setlow B, Febo M. Functional Connectivity of Chronic Cocaine Use Reveals Progressive Neuroadaptations in Neocortical, Striatal and Limbic Networks. Eneuro 2018;5:ENEURO.0081-18.2018. doi: 10.1523/ENEURO.0081-18.2018 30073194

43. Colon-Perez LM, Pino JA, Saha K, Pompilus M, Kaplitz S, Choudhury N, et al. Functional connectivity, behavioral and dopaminergic alterations 24 hours following acute exposure to synthetic bath salt drug methylenedioxypyrovalerone. Neuropharmacology 2018;137:178–93. doi: 10.1016/j.neuropharm.2018.04.031 29729891

44. Nephew BC, Febo M, Huang W, Colon-Perez LM, Payne L, Poirier GL, et al. Early life social stress and resting state functional connectivity in postpartum rat anterior cingulate circuits. J Affect Disord 2018;229:213–23. doi: 10.1016/j.jad.2017.12.089 29324369

45. Huang Y, Tsai SJ, Su TW, Sim CB. Effects of Repeated High-Dose Methamphetamine on Local Cerebral Glucose Utilization in Rats. Neuropsychopharmacology 1999;21:427–34. doi: 10.1016/S0893-133X(99)00029-9 10457540

46. Xi Z-X, Kleitz HK, Deng X, Ladenheim B, Peng X-Q, Li X, et al. A single high dose of methamphetamine increases cocaine self-administration by depletion of striatal dopamine in rats. Neuroscience 2009;161:392–402. doi: 10.1016/j.neuroscience.2009.03.060 19336247

47. Krasnova IN, Ladenheim B, Hodges AB, Volkow ND, Cadet JL. Chronic methamphetamine administration causes differential regulation of transcription factors in the rat midbrain. PLoS One 2011;6:e19179. doi: 10.1371/journal.pone.0019179 21547080

48. Gutierrez A, Williams MT, Vorhees C V. A Single High Dose of Methamphetamine Reduces Monoamines and Impairs Egocentric and Allocentric Learning and Memory in Adult Male Rats. Neurotox Res 2018;33:671–80. doi: 10.1007/s12640-018-9871-9 29427284

49. Woodman MM, Jirsa VK. Emergent Dynamics from Spiking Neuron Networks through Symmetry Breaking of Connectivity. PLoS One 2013;8:e64339. doi: 10.1371/journal.pone.0064339 23691200

50. Nowotny T, Rabinovich MI. Dynamical Origin of Independent Spiking and Bursting Activity in Neural Microcircuits 2007. doi: 10.1103/PhysRevLett.98.128106 17501162

51. Lautenschläger J, Mosharov E V., Kanter E, Sulzer D, Kaminski Schierle GS. An Easy-to-Implement Protocol for Preparing Postnatal Ventral Mesencephalic Cultures. Front Cell Neurosci 2018;12:44. doi: 10.3389/fncel.2018.00044 29556177

52. Liang X, He Y, Salmeron BJ, Gu H, Stein EA, Yang Y. Interactions between the Salience and Default-Mode Networks Are Disrupted in Cocaine Addiction. J Neurosci 2015;35:8081–90. doi: 10.1523/JNEUROSCI.3188-14.2015 26019326

53. Luo Q, Poelzing S, Tech V, Shaoqun Zeng U, Dubbs alex A, Yuste R, et al. moco: Fast Motion Correction for Calcium Imaging. Front Neuroinformatics | www.Frontiersin.Org 2016;10. doi: 10.3389/fninf.2016.00006 26909035

54. Lim S, Radicchi F, van den Heuvel MP, Sporns O. Discordant attributes of structural and functional brain connectivity in a two-layer multiplex network. Sci Rep 2019;9:2885. doi: 10.1038/s41598-019-39243-w 30814615

55. Newman MEJ. Assortative Mixing in Networks. Phys Rev Lett 2002;89:208701. doi: 10.1103/PhysRevLett.89.208701 12443515

56. Onnela J-P, Saramäki J, Kertész J, Kaski K. Intensity and coherence of motifs in weighted complex networks. Phys Rev E 2005;71:065103. doi: 10.1103/PhysRevE.71.065103 16089800


Článek vyšel v časopise

PLOS One


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 3/2024 (znalostní test z časopisu)
nový kurz

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Aktuální možnosti diagnostiky a léčby litiáz
Autoři: MUDr. Tomáš Ürge, PhD.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#