Real-time telemetry monitoring of oxygen in the central complex of freely-walking Gromphadorhina portentosa

English version

Autoři: Pier Andrea Serra ^aff001; Paola Arrigo ^aff001; Andrea Bacciu ^aff001; Daniele Zuncheddu ^aff001; Riccardo Deliperi ^aff001; Diego Antón Viana ^aff001; Patrizia Monti ^aff001; Maria Vittoria Varoni ^aff004; Maria Alessandra Sotgiu ^aff005; Pasquale Bandiera ^aff005; Gaia Rocchitta ^aff001
Působiště autorů: Department of Medical, Surgical and Experimental Medicine, Medical School, University of Sassari, Sassari, Italy ^aff001; Institute of Sciences of Food Production, Italian National Research Council, Sassari, Italy ^aff002; Mediterranean Center for Disease Control, University of Sassari, Sassari, Italy ^aff003; Department of Veterinary Medicine, Medical School, University of Sassari, Sassari, Italy ^aff004; Department of Biomedical Sciences, Medical School, University of Sassari, Sassari, Italy ^aff005
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224932

Souhrn

A new telemetric system for the electrochemical monitoring of dissolved oxygen is showed. The device, connected with two amperometric sensors, has been successfully applied to the wireless detection of the extracellular oxygen in the central complex of freely-walking Gromphadorhina portentosa. The unit was composed of a potentiostat, a two-channel sensor conditioning circuit, a microprocessor module, and a wireless serial transceiver. The amperometric signals were digitalized and sent to a notebook using a 2.4 GHz transceiver while a serial-to-USB converter was connected to a second transceiver for completing the communication bridge. The software, running on the laptop, allowed to save and graph the oxygen signals. The electronics showed excellent stability and the acquired data was linear in a range comprised between 0 and -165 nA, covering the entire range of oxygen concentrations. A series of experiments were performed to explore the dynamics of dissolved oxygen by exposing the animals to different gases (nitrogen, oxygen and carbon dioxide), to low temperature and anesthetic agents (chloroform and triethylamine). The resulting data are in agreement with previous O₂ changes recorded in the brain of awake rats and mice. The proposed system, based on simple and inexpensive components, can constitute a new experimental model for the exploration of central complex neurochemistry and it can also work with oxidizing sensors and amperometric biosensors.

Klíčová slova:

Insects – Glucose metabolism – Carbon dioxide – Oxygen – Anesthetics – Oxygen metabolism – Cockroaches – Chloroform

Zdroje

1. Castro MA, Angulo C, Brauchi S, Nualart F, Concha II. Ascorbic acid participates in a general mechanism for concerted glucose transport inhibition and lactate transport stimulation. Pflugers Arch Eur J Physiol. 2008; doi: 10.1007/s00424-008-0526-1 18506475

2. Castro MA, Beltrán FA, Brauchi S, Concha II. A metabolic switch in brain: glucose and lactate metabolism modulation by ascorbic acid. J Neurochem. 2009;110: 423–40. doi: 10.1111/j.1471-4159.2009.06151.x 19457103

3. Rangaraju V, Calloway N, Ryan TA. Activity-driven local ATP synthesis is required for synaptic function. Cell. 2014; doi: 10.1016/j.cell.2013.12.042 24529383

4. Bordone MP, Salman MM, Titus HE, Amini E, Andersen J V., Chakraborti B, et al. The energetic brain. A review from students to students. J Neurochem. 2019; doi: 10.1111/jnc.14829 31318452

5. Lowry JP, Boutelle MG, Fillenz M. Measurement of brain tissue oxygen at a carbon past electrode can serve as an index of increases in regional cerebral blood flow. J Neurosci Methods. 1997;71: 177–82. Available: http://www.ncbi.nlm.nih.gov/pubmed/9128153 doi: 10.1016/s0165-0270(96)00140-9 9128153

6. Fillenz M. The role of lactate in brain metabolism. Neurochem Int. 2005;47: 413–7. doi: 10.1016/j.neuint.2005.05.011 16039756

7. Aubert A, Costalat R, Magistretti PJ, Pellerin L. Brain lactate kinetics: Modeling evidence for neuronal lactate uptake upon activation. Proc Natl Acad Sci U S A. 2005;102: 16448–53. doi: 10.1073/pnas.0505427102 16260743

8. Rittschof CC, Schirmeier S. Insect models of central nervous system energy metabolism and its links to behavior. GLIA. 2018. doi: 10.1002/glia.23235 28960551

9. Bazzu G, Puggioni GM, Dedola S, Calia G, Rocchitta G, Migheli R, et al. Real-time monitoring of brain tissue oxygen using a miniaturized biotelemetric device implanted in freely moving rats. Anal Chem. 2009;81: 2235–2241. doi: 10.1021/ac802390f 19222224

10. Calia G, Rocchitta G, Migheli R, Puggioni G, Spissu Y, Bazzu G, et al. Biotelemetric monitoring of brain neurochemistry in conscious rats using microsensors and biosensors. Sensors (Switzerland). 2009;9. doi: 10.3390/s90402511 22574029

11. Bolger F, Lowry J. Brain Tissue Oxygen: In Vivo Monitoring with Carbon Paste Electrodes. Sensors. 2005;5: 473–487. doi: 10.3390/s5110473

12. Pletcher D, Greff R, Peat R, Peter LM, Robinson J. Southampton Electrochemistry Group. Instrumental Methods in Electrochemistry. Woodhead Publishing; 2001. doi: 10.1533/9781782420545

13. Rocchitta G, Migheli R, Dedola S, Calia G, Desole MS, Miele E, et al. Development of a distributed, fully automated, bidirectional telemetry system for amperometric microsensor and biosensor applications. Sensors Actuators, B Chem. 2007;126. doi: 10.1016/j.snb.2007.04.019

14. Serra PA, Rocchitta G, Bazzu G, Manca A, Puggioni GM, Lowry JP, et al. Design and construction of a low cost single-supply embedded telemetry system for amperometric biosensor applications. Sensors Actuators, B Chem. 2007;122. doi: 10.1016/j.snb.2006.05.013

15. Heinze S, Pfeiffer K. Editorial: The Insect Central Complex—From Sensory Coding to Directing Movement. Frontiers in Behavioral Neuroscience. 2018. doi: 10.3389/fnbeh.2018.00156 30104965

16. Andersen ML, Winter LMF. Animal models in biological and biomedical research–experimental and ethical concerns. An Acad Bras Cienc. 2019; doi: 10.1590/0001-3765201720170238 28876358

17. Sherwin CM. Can Invertebrates Suffer? Or, How Robust is Argument-by-Analogy? Animal Welfare. 2001;10(1);103–118.

18. Elwood RW, Appel M. Pain experience in hermit crabs? Anim Behav. 2009;77;1243–1246. doi: 10.1016/j.anbehav.2009.01.028

19. Bovenkerk B, Kaldewaij F. The use of animal models in behavioural neuroscience research. Curr Top Behav Neurosci. 2015;19:17–46. doi: 10.1007/7854_2014_329 25031123

20. Carrel JE, Tanner EM. Sex-specific food preferences in the Madagascar hissing cockroach Gromphadorhina portentosa (Dictyoptera: Blaberidae). J Insect Behav. 2002;15: 707–714. doi: 10.1023/A:1020704108399

21. Wipfler B, Weissing K, Klass KD, Weihmann T. The cephalic morphology of the American cockroach Periplaneta americana (Blattodea). Arthropod Syst Phylogeny. 2016;74: 267–297.

22. Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, et al. A systematic nomenclature for the insect brain. Neuron. 2014;81: 755–765. doi: 10.1016/j.neuron.2013.12.017 24559671

23. Rocchitta G, Secchi O, Alvau MD, Farina D, Bazzu G, Calia G, et al. Simultaneous telemetric monitoring of brain glucose and lactate and motion in freely moving rats. Anal Chem. 2013; 85(21):10282–8. doi: 10.1021/ac402071w 24102201

24. Dittmar A, Mangin S, Ruban C, Newman WH, Bowman HF, Dupuis V, et al. In vivo and in vitro evaluation of specially designed gold and carbon fiber oxygen microelectrodes for living tissues. Sensors Actuators, B Chem. 1997;44: 316–320. doi: 10.1016/S0925-4005(97)00224-4

25. Bazzu G, Serra PA, Hamelink R, Feenstra MGP, Willuhn I, Denys D. Monitoring deep brain stimulation by measuring regional brain oxygen responses in freely moving mice. J Neurosci Methods. 2019;317. doi: 10.1016/j.jneumeth.2019.01.012 30716350

26. McMahon CP, Rocchitta G, Kirwan SM, Killoran SJ, Serra PA, Lowry JP, et al. Oxygen tolerance of an implantable polymer/enzyme composite glutamate biosensor displaying polycation-enhanced substrate sensitivity. Biosens Bioelectron. 2007;22. doi: 10.1016/j.bios.2006.06.027 16887344

27. O’Neill RD, Rocchitta G, McMahon CP, Serra PA, Lowry JP. Designing sensitive and selective polymer/enzyme composite biosensors for brain monitoring in vivo. TrAC—Trends Anal Chem. 2008;27. doi: 10.1016/j.trac.2007.11.008

28. Rocchitta G, Secchi O, Alvau MD, Migheli R, Calia G, Bazzu G, et al. Development and characterization of an implantable biosensor for telemetric monitoring of ethanol in the brain of freely moving rats. Anal Chem. 2012;84. doi: 10.1021/ac301253h 22823474

29. Secchi O, Zinellu M, Spissu Y, Pirisinu M, Bazzu G, Migheli R, et al. Further in-vitro characterization of an implantable biosensor for ethanol monitoring in the brain. Sensors (Switzerland). 2013;13. doi: 10.3390/s130709522 23881145

30. Rocchitta G, Peana AT, Bazzu G, Cossu A, Carta S, Arrigo P, et al. Simultaneous wireless and high-resolution detection of nucleus accumbens shell ethanol concentrations and free motion of rats upon voluntary ethanol intake. Alcohol. 2019;78. doi: 10.1016/j.alcohol.2019.04.002 31029631

31. Quinlan MC, Gibbs AG. Discontinuous gas exchange in insects. Respir Physiol Neurobiol. 2006;154: 18–29. doi: 10.1016/j.resp.2006.04.004 16870512

32. Schimpf NG, Matthews PGD, Wilson RS, White CR. Cockroaches breathe discontinuously to reduce respiratory water loss. J Exp Biol. 2009;212: 2773–2780. doi: 10.1242/jeb.031310 19684210

33. Contreras HL, Bradley TJ. Transitions in insect respiratory patterns are controlled by changes in metabolic rate. J Insect Physiol. 2010;56: 522–528. doi: 10.1016/j.jinsphys.2009.05.018 19523955

34. Boardman L, Terblanche JS, Hetz SK, Marais E, Chown SL. Reactive oxygen species production and discontinuous gas exchange in insects. Proc R Soc B Biol Sci. 2012;279: 893–901. doi: 10.1098/rspb.2011.1243 21865257

35. Berman TS, Ayali A, Gefen E. Neural Control of Gas Exchange Patterns in Insects: Locust Density-Dependent Phases as a Test Case. PLoS One. 2013;8. doi: 10.1371/journal.pone.0059967 23555850

36. Groenewald B, Chown SL, Terblanche JS. A hierarchy of factors influence discontinuous gas exchange in the grasshopper Paracinema tricolor (Orthoptera: Acrididae). J Exp Biol. 2014;217: 3407–3415. doi: 10.1242/jeb.102814 25063854

37. Slama K, Santiago-Blay JA. Terrestrial Insects with Tracheae Breath by Actively Regulating Ventilatory Movements: Physiological Similarities to Humans. Life Excit Biol. 2017;5: 4–70. doi: 10.9784/leb5(1)slama.01

38. Seiger MB, Kink JF. The effect of anesthesia on the photoresponses of four sympatric species of Drosophila. Behav Genet. 1993;23: 99–104. doi: 10.1007/bf01067559 8476397

39. MacMillan HA, NØrgård M, MacLean HJ, Overgaard J, Williams CJA. A critical test of Drosophila anaesthetics: Isoflurane and sevoflurane are benign alternatives to cold and CO2. J Insect Physiol. 2017;101: 97–106. doi: 10.1016/j.jinsphys.2017.07.005 28733237

40. Kohler I, Meier R, Busato A, Neiger-Aeschbacher G, Schatzmann U. Is carbon dioxide (CO2) a useful short acting anaesthetic for small laboratory animals? Lab Anim. 1999;33: 155–161. doi: 10.1258/002367799780578390 10780819

41. Colinet H, Renault D. Metabolic effects of CO2 anaesthesia in Drosophila melanogaster. Biol Lett. 2012;8: 1050–1054. doi: 10.1098/rsbl.2012.0601 22915627

42. Matthews PGD, White CR. Regulation of gas exchange and haemolymph pH in the cockroach Nauphoeta cinerea. J Exp Biol. 2011;214: 3062–3073. doi: 10.1242/jeb.053991 21865519

43. Streicher JW, Cox CL, Birchard GF. Non-linear scaling of oxygen consumption and heart rate in a very large cockroach species (Gromphadorhina portentosa): correlated changes with body size and temperature. J Exp Biol. 2012;215: 1137–1143. doi: 10.1242/jeb.061143 22399658

44. Matthews PGD, White CR. Reversible brain inactivation induces discontinuous gas exchange in cockroaches. J Exp Biol. 2013;216: 2012–2016. doi: 10.1242/jeb.077479 23430991

45. Gamo S, Ogaki M, Nakashima-Tanaka E. Strain differences in minimum anesthetic concentrations in Drosophila melanogaster. Anesthesiology. 1981;54: 289–93. doi: 10.1097/00000542-198104000-00006 6782911

46. Chen W, Hillyer JF. FlyNap (Triethylamine) Increases the Heart Rate of Mosquitoes and Eliminates the Cardioacceleratory Effect of the Neuropeptide CCAP. PLoS One. 2013;8: 1–12. doi: 10.1371/journal.pone.0070414 23875027

47. Ueda I. Molecular mechanisms of anesthesia. Keio J Med. 2000;50: 20–25.

48. Tasbihgou SR, Netkova M, Kalmar AF, Doorduin J, Struys MMRF, Schoemaker RG, et al. Brain changes due to hypoxia during light anaesthesia can be prevented by deepening anaesthesia; a study in rats. PLoS One. 2018;13: 1–19. doi: 10.1371/journal.pone.0193062 29451906

49. Hosie AM, Aronstein K, Sattelle DB, Ffrench-Constant RH. Molecular biology of insect neuronal GABA receptors. Trends Neurosci. 1997;20: 578–583. doi: 10.1016/s0166-2236(97)01127-2 9416671

50. Homberg U, Humberg TH, Seyfarth J, Bode K, Pérez MQ. GABA immunostaining in the central complex of dicondylian insects. J Comp Neurol. 2018;526: 2301–2318. doi: 10.1002/cne.24497 30004590

51. Strausfeld NJ, Hirth F. Deep Homology of Arthropod Central Complex and Vertebrate Basal Ganglia. Science. 2013; 340: 157–161. doi: 10.1126/science.1231828 23580521

52. Li G, Zhang D. Brain-Computer Interface Controlled Cyborg: Establishing a Functional Information Transfer Pathway from Human Brain to Cockroach Brain. PLoS One. 2016;11: e0150667. doi: 10.1371/journal.pone.0150667 26982717

53. Joshua Martin AP, Guo P, Mu L, Harley CM, Martin JP, Ritzmann RE. Central-Complex Control of Movement in the Freely Walking Cockroach. Curr Biol. 2015;25: 2795–2803. doi: 10.1016/j.cub.2015.09.044 26592340

Real-time telemetry monitoring of oxygen in the central complex of freely-walking Gromphadorhina portentosa

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz