Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Review

Free Access

Invertebrate Models in Addiction Research

Søvik E. · Barron A.B.

Author affiliations

Department of Biological Sciences, Macquarie University, Sydney, N.S.W., Australia

Corresponding Author

Eirik Søvik

Department of Biological Sciences, Macquarie University

209 Culloden Road

Marsfield, NSW 2122 (Australia)

E-Mail eirik.sovik@mq.edu.au

Related Articles for ""

Brain Behav Evol 2013;82:153-165

Do you have an account?

Login Information





Contact Information










I have read the Karger Terms and Conditions and agree.



Abstract

While drug addiction is a uniquely human problem, most research examining the biological mechanisms of the transition from substance use to addiction is conducted with vertebrate animal models. Many other fields of neuroscience have greatly benefitted from contributions from simple and manipulable invertebrate model systems. However, the potential of invertebrate research has yet to be fully capitalised on in the field of addiction neuroscience. This may be because of the complexity of addiction and the clinical imperative of addiction research. We argue that the homocentric diagnostic criteria of addiction are no more a hindrance to the use of invertebrate models than they are to vertebrate models. We highlight the strengths of the diversity of different invertebrate model systems in terms of neuroanatomy and molecular machinery, and stress that working with a range of different models will aid in understanding addiction and not be a disadvantage. Finally, we discuss the specific advantages of utilising invertebrate animals for addiction research and highlight key areas in which invertebrates are suited for making unique and meaningful contributions to this field.

© 2013 S. Karger AG, Basel


References

  1. Abarca C, Albrecht U, Spanagel R (2002): Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc Natl Acad Sci USA 99:9026-9030.
  2. Abramson CI, Kandolf A, Sheridan A, Donohue D, Bozic J, Meyers JE, et al (2004): Development of an ethanol model using social insects. III. Preferences for ethanol solutions. Psychol Rep 94:227-239.
  3. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, et al (2000): The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
    External Resources
  4. American Psychiatric Association (1994): Diagnostic and statistical manual of mental disorders: DSM-IV-TR. Washington.
  5. Andretic R, Chaney S, Hirsh J (1999): Requirement of circadian genes for cocaine sensitization in Drosophila. Science 285:1066-1068.
  6. Anier K, Malinovskaja K, Aonurm-Helm A, Zharkovsky A, Kalda A (2010): DNA methylation regulates cocaine-induced behavioral sensitization in mice. Neuropsychopharmacol 35:2450-2461.
  7. Arendt D, Nübler-Jung K (1994): Inversion of dorsoventral axis? Nature 371:26.
  8. Badshah H, Khan AS, Farid A, Zeb A (2004): Toxic effects of palpoluck Polygonum hydropepper L. and Bhang Cannabis sativa L. plants extracts against termites Heterotermes indicola (Wasmann) and Coptotermes heimi (Wasmann) (Isoptera: Rhinotermitidae). Songklanakarin J Sci Technol 27:705-710.
  9. Bainton RJ, Tsai LT, Singh CM, Moore MS, Neckameyer WS, Heberlein U (2000): Dopamine modulates acute responses to cocaine, nicotine and ethanol in Drosophila. Curr Biol 10:187-194.
  10. Barron AB, Maleszka R, Helliwell PG, Robinson GE (2009): Effects of cocaine on honey bee dance behaviour. J Exp Biol 212:163-168.
  11. Barron AB, Søvik E, Cornish JL (2010): The roles of dopamine and related compounds in reward-seeking behavior across animal phyla. Front Behav Neurosci 4:1-9.
  12. Blenau W, Baumann MH (2001): Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13-38.
  13. Blum M, Rivier L, Plowman T (1981): Fate of cocaine in the lymantriid Eloria noyesi, a predator of Erythroxylum coca. Phytochemistry 20:2499-2500.
    External Resources
  14. Borue X, Condron B, Venton BJ (2010): Both synthesis and reuptake are critical for replenishing the releasable serotonin pool in Drosophila. J Neurochem 113:188-199.
  15. Bozic J, Abramson CI, Bedencic M (2006): Reduced ability of ethanol drinkers for social communication in honeybees (Apis mellifera carnica Poll.). Alcohol 38:179-183.
  16. Brembs B (2003): Operant conditioning in invertebrates. Curr Opin Neurobiol 13:710-717.
  17. Burchett SA, Hicks TP (2006): The mysterious trace amines: protean neuromodulators of synaptic transmission in mammalian brain. Prog Neurobiol 79:223-246.
  18. Burne T, Scott E, van Swinderen B, Hilliard M, Reinhard J, Claudianos C, et al (2011): Big ideas for small brains: what can psychiatry learn from worms, flies, bees and fish? Mol Psychiatry 16:7-16.
  19. Butler AB, Hodos W (2005): Comparative Vertebrate Neuroanatomy: Evolution and Adaptation. Hoboken, John Wiley & Sons, Inc.
  20. Buttarelli FR, Pontieri FE, Margotta V, Palladini G (2002): Cannabinoid-induced stimulation of motor activity in Planaria through an opioid receptor-mediated mechanism. Prog Neuropsychopharmacol Biol Psychiatry 26:65-68.
  21. Caveney S, Cladman W, Verellen L, Donly C (2006): Ancestry of neuronal monoamine transporters in the Metazoa. J Exp Biol 209:4858-4868.
  22. Chao J, Nestler EJ (2004): Molecular neurobiology of drug addiction. Annu Rev Med 55:113-132.
  23. Chen R, Tilley M, Wei H (2006a): Abolished cocaine reward in mice with a cocaine-insensitive dopamine transporter. Proc Natl Acad Sci USA 103:9333-9338.
  24. Chen R, Wu X, Wei H, Han DD, Gu HH (2006b): Molecular cloning and functional characterization of the dopamine transporter from Eloria noyesi, a caterpillar pest of cocaine-rich coca plants. Gene 366:152-160.
  25. Chiang A-S, Lin C-Y, Chuang C-C, Chang H-M, Hsieh C-H, Yeh C-W, et al (2011): Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21:1-11.
  26. Chronis N (2010): Worm chips: microtools for C. elegans biology. Lab Chip 10:432-437.
  27. Crabbe J (2002): Genetic contributions to addiction. Annu Rev Psychol 53:435-462.
  28. Denes AS, Jékely G, Steinmetz PRH, Raible F, Snyman H, Prud'homme B, et al (2007): Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129:277-288.
  29. Deroche-Gamonet V, Belin D, Piazza PV (2004): Evidence for addiction-like behavior in the rat. Science 305:1014-1017.
  30. Devineni A V, Heberlein U (2009): Preferential ethanol consumption in Drosophila models features of addiction. Curr Biol 19:2126-2132.
  31. Elphick MR, Egertová M (2001): The neurobiology and evolution of cannabinoid signalling. Philos Trans R Soc Lond B Biol Sci 356:381-408.
  32. Everitt BJ, Robbins TW (2005): Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481-1489.
  33. Farris SM (2008a): Evolutionary convergence of higher brain centers spanning the protostome-deuterostome boundary. Brain Behav Evol 72:106-122.
  34. Farris SM (2008b): Structural, functional and developmental convergence of the insect mushroom bodies with higher brain centers of vertebrates. Brain Behav Evol 72:1-15.
  35. Fernando ABP, Robbins TW (2011): Animal models of neuropsychiatric disorders. Annu Rev Clin Psychol 7:39-61.
  36. Flores KB, Wolschin F, Allen AN, Corneveaux JJ, Huentelman M, Amdam GV (2012): Genome-wide association between DNA methylation and alternative splicing in an invertebrate. BMC Genomics 13:480.
  37. Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, et al (2012): DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc Natl Acad Sci USA 109:4968-4973.
  38. Giurfa M (2003): Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726-735.
  39. Han DD, Gu HH (2006): Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol 6:6.
  40. Harrison LM, Kastin AJ, Weber JT, Banks WA, Hurley DL, Zadina JE (1994): The opiate system in invertebrates. Peptides 15:1309-1329.
  41. Hasin D, Hatzenbuehler ML, Keyes K, Ogburn E (2006): Substance use disorders: Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV) and International Classification of Diseases, tenth edition (ICD-10). Addiction 101(suppl 1):59-75.
  42. Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B, Irizarry R, et al (2012): Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat Neurosci 15:1371-1373.
  43. Hodgkin AL, Huxley AF (1945): Resting and action potentials in single nerve fibres. J Physiol 104:176-195.
    External Resources
  44. Hut RA, Beersma DGM (2011): Evolution of time-keeping mechanisms: early emergence and adaptation to photoperiod. Philos Trans R Soc Lond B Biol Sci 366:2141-2154.
  45. Kandel ER (2007): In Search of Memory: The Emergence of a New Science of Mind. New York, W. W. Norton & Company.
    External Resources
  46. Katona I, Freund TF (2012): Multiple functions of endocannabinoid signaling in the brain. Annu Rev Neurosci 35:529-558.
  47. Kaun KR, Azanchi R, Maung Z, Hirsh J, Heberlein U (2011): A Drosophila model for alcohol reward. Nat Neurosci 14:1-13.
    External Resources
  48. Kaun KR, Devineni A V, Heberlein U (2012): Drosophila melanogaster as a model to study drug addiction. Hum Genet 131:959-975.
  49. Kayani MZ, Mukhtar T, Hussain MA (2012): Evaluation of nematicidal effects of Cannabis sativa L. and Zanthoxylum alatum Roxb. against root-knot nematodes, Meloidogyne incognita. Crop Protection 39:52-56.
    External Resources
  50. Konopka RJ (1987): Genetics of biological rhythms in Drosophila. Annu Rev Genet 21:227-236.
  51. Koob GF, Volkow ND (2010): Neurocircuitry of addiction. Neuropsychopharmacol 35:217-238.
  52. Kusayama T, Watanabe S (2000): Reinforcing effects of methamphetamine in planarians. Neuroreport 11:2511-2513.
    External Resources
  53. LaPlant Q, Vialou V, Covington HE, Dumitriu D, Feng J, Warren BL, et al (2010): Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13:1137-1143.
  54. Lester D, Freed EX (1973): Criteria for an animal model of alcoholism. Pharmacol Biochem Behav 1:103-107.
  55. Lozada M, Romano A, Maldonado H (1988): Effect of morphine and naloxone on a defensive response of the crab Chasmagnathus granulatus. Pharmacol Biochem Behav 30:635-640.
  56. Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R (2010): The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8:e1000506.
  57. Lyko F, Maleszka R (2011): Insects as innovative models for functional studies of DNA methylation. Trends Genet 27:127-131.
  58. MacCoun R, Reuter P, Schelling T (1996): Assessing alternative drug control regimes. J Policy Anal Manage 15:330-352.
    External Resources
  59. Mackay TFC, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, et al (2012): The Drosophila melanogaster genetic reference panel. Nature 482:173-178.
  60. Makos MA, Han K-A, Heien ML, Ewing AG (2010): Using in vivo electrochemistry to study the physiological effects of cocaine and other stimulants on the Drosophila melanogaster dopamine transporter. ACS Chem Neurosci 1:74-83.
  61. Makos MA, Kim Y-C, Han K-A, Heien ML, Ewing AG (2009): In vivo electrochemical measurements of exogenously applied dopamine in Drosophila melanogaster. Anal Chem 81:1848-1854.
  62. McPartland J, Agraval J, Gleeson D, Heasman K, Glass M (2006): Cannabinoid receptors in invertebrates. J Evol Biol 19:366-373.
  63. McPartland J, Di Marzo V, De Petrocellis L, Mercer A, Glass M (2001): Cannabinoid receptors are absent in insects. J Comp Neurol 436:423-429.
  64. Mori I, Ohshima Y (1995): Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376:344-348.
  65. Morozova T V, Ayroles JF, Jordan KW, Duncan LH, Carbone MA, Lyman RF, et al (2009): Alcohol sensitivity in Drosophila: translational potential of systems genetics. Genetics 183:733-745.
  66. Mustard JA, Beggs KT, Mercer AR (2005): Molecular biology of the invertebrate dopamine receptors. Arch Insect Biochem Physiol 59:103-117.
  67. Nathaniel TI, Panksepp J, Huber R (2009): Drug-seeking behavior in an invertebrate system: evidence of morphine-induced reward, extinction and reinstatement in crayfish. Behav Brain Res 197:331-338.
  68. Nathaniel TI, Panksepp J, Huber R (2010): Effects of a single and repeated morphine treatment on conditioned and unconditioned behavioral sensitization in crayfish. Behav Brain Res 207:310-320.
  69. Nathanson JA, Hunnicutt EJ, Kantham L, Scavone C (1993): Cocaine as a naturally occurring insecticide. Proc Natl Acad Sci USA 90:9645-9648.
  70. Nestler EJ, Hyman SE (2010): Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161-1169.
  71. O'Reilly RC, Rudy JW (2001): Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol Rev 108:311-345.
  72. Panksepp JB, Huber R (2004): Ethological analyses of crayfish behavior: a new invertebrate system for measuring the rewarding properties of psychostimulants. Behav Brain Res 153:171-180.
  73. Perry CJ, Barron AB (2013): Neural mechanisms of reward in insects. Annu Rev Entomol 58:543-562.
  74. Perry CJ, Barron AB, Cheng K (2013): Invertebrate learning and cognition: relating phenomena to neural substrate. Wiley Interdisciplinary Reviews. Cogn Sci 4:561-582.
    External Resources
  75. Pohl JB, Baldwin BA, Dinh BL, Rahman P, Smerek D, Prado FJ, et al. (2012): Ethanol preference in Drosophila melanogaster is driven by its caloric value. Alcohol Clin Exp Res 36:1903-1912.
  76. Rattan RS (2010): Mechanism of action of insecticidal secondary metabolites of plant origin. Crop Protection 29:913-920.
    External Resources
  77. Robinson TE, Berridge KC (2008): The incentive sensitization theory of addiction: some current issues. Philos Trans R Soc Lond B Biol Sci 363:3137-3146.
  78. Roeder T (1999): Octopamine in invertebrates. Prog Neurobiol 59:533-561.
  79. Roeder T (2005): Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447-477.
  80. Samaha A-N, Robinson TE (2005): Why does the rapid delivery of drugs to the brain promote addiction? Trends Pharmacol Sci 26:82-87.
  81. Sanchis-Segura C, Spanagel R (2006): Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict Biol 11:2-38.
  82. Sandhu SK, Ross LS, Gill SS (2002): A cocaine insensitive chimeric insect serotonin transporter reveals domains critical for cocaine interaction. Eur J Biochem 269:3934-3944.
  83. Schneider A, Ruppert M, Hendrich O, Giang T, Ogueta M, Hampel S, et al (2012): Neuronal basis of innate olfactory attraction to ethanol in Drosophila. PLoS One 7:e52007.
  84. Scholz H, Mustard JA (2013): Invertebrate models of alcoholism. Curr Top Behav Neurosci 13:433-457.
  85. Seeley TD (1995): The Wisdom of the Hive. Cambridge, Harvard University Press.
  86. Sehgal A (1995): Molecular genetic analysis of circadian rhythms in vertebrates and invertebrates. Curr Opin Neurobiol 5:824-831.
  87. Sellami A, Isabel G, Veenstra JA (2010): Expression of the mu opioid receptor in Drosophila and its effects on trehalose and glycogen when expressed by the AKH neuroendocrine cells. Peptides 31:1383-1389.
  88. Shapiro H (1931): The rate of oviposition in the fruit fly, Drosophila. Biol Bull 63:456-471.
    External Resources
  89. Shimada T, Kato K, Kamikouchi A, Ito K (2005): Analysis of the distribution of the brain cells of the fruit fly by an automatic cell counting algorithm. Physica A: Statistical Mech Applications 350:144-149.
    External Resources
  90. Siegel RK (2005): Intoxication: The Universal Drive for Mind-Altering Substances. Rochester, Park Street Press.
  91. Spanagel R, Pendyala G, Abarca C, Zghoul T, Sanchis-Segura C, Magnone MC, et al (2005): The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nat Med 11:35-42.
  92. Stephan FK, Zucker I (1972): Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69:1583-1586.
  93. Strausfeld NJ, Hirth F (2013): Deep homology of arthropod central complex and vertebrate basal ganglia. Science 340:157-161.
  94. Sullivan RJ, Hagen EH, Hammerstein P (2008): Revealing the paradox of drug reward in human evolution. Proc R Soc Lond B 275:1231-1241.
  95. Tomer R, Denes AS, Tessmar-Raible K, Arendt D (2010): Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 142:800-809.
  96. Tzschentke TM (2007): Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227-462.
  97. Uylings HBM, Groenewegen HJ, Kolb B (2003): Do rats have a prefrontal cortex? Behav Brain Res 146:3-17.
  98. Vickrey TL, Condron B, Venton BJ (2009): Detection of endogenous dopamine changes in Drosophila melanogaster using fast-scan cyclic voltammetry. Anal Chem 81:9306-9313.
  99. Waddell S (2013): Reinforcement signalling in Drosophila; dopamine does it all after all. Curr Opin Neurobiol 23:324-329.
  100. Waldhoer M, Bartlett SE, Whistler JL (2004): Opioid receptors. Annu Rev Biochem 73:953-990.
  101. Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R, et al (2006): Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
  102. White JG, Southgate E, Thomson JN, Brenner S (1986): The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1-340.
  103. Witthöft W (1967): Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Zoomorphology 61:160-184.
    External Resources
  104. Wolf FW, Heberlein U (2003): Invertebrate models of drug abuse. J Neurobiol 54:161-178.
  105. World Health Organization (1993): The ICD-10 classification of mental and behavioural disorders: diagnostic criteria for research. Geneva, World Health Organization.
  106. Yanik MF, Cinar H, Cinar HN, Chisholm AD, Jin Y, Ben-Yakar A (2004): Neurosurgery: functional regeneration after laser axotomy. Nature 432:822.
  107. Young JM, Wessnitzer J, Armstrong JD, Webb B (2011): Elemental and non-elemental olfactory learning in Drosophila. Neurobiol Learn Mem 96:339-352.
  108. Young JZ (1963): The numbers and sizes of nerve cells in octopus. Proc Zool Soc Lond 140:229-254.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Review

Received: June 24, 2013
Accepted: September 03, 2013
Published online: October 28, 2013
Issue release date: November 2013

Number of Print Pages: 13
Number of Figures: 0
Number of Tables: 2

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.