Nicotine behavioral pharmacology: clues from planarians - PubMed (original) (raw)
Nicotine behavioral pharmacology: clues from planarians
Scott M Rawls et al. Drug Alcohol Depend. 2011.
Abstract
Background: Nicotine is one of the world's most addictive substances and the primary reason that humans inhale tobacco smoke. The pharmacological effects of nicotine can be investigated in planarians, aquatic flatworms that possess an integrated neural network including cephalic ganglia that some consider the earliest 'brain' and spinal cord. Here, we tested the hypothesis that nicotine exposure elicits mammalian-like behaviors in planarians.
Methods: Planarian motility and stereotypy (C-shape hyperkinesias) were quantified following acute nicotine exposure. During repeated nicotine exposure, we investigated the presence of withdrawal, tolerance, behavioral sensitization, and environmental place conditioning.
Results: Acute nicotine exposure increased stereotypical activity and elicited biphasic effects on motility. A low concentration (0.01 mM) increased motility whereas higher concentrations (0.3-10mM) elicited the opposite effect. Planarians exposed to nicotine (0.03 mM) for 60 min and then tested in water displayed reduced motility that was not observed during exposure to water, acute nicotine, or continuous nicotine. Nicotine-treated planarians withdrawn from the drug for 3 days before being challenged with nicotine displayed behavioral sensitization at low concentrations (0.1, 0.3mM) but tolerance at higher concentrations (1, 3mM). Planarians conditioned with nicotine in the ambient light (non-preferred environment) displayed a reduction in their natural preference for a dark environment.
Conclusions: The present results suggest nicotine elicits mammalian-like effects in planarians, including decreased motility and increased stereotypy following acute administration and abstinence-induced withdrawal, behavioral sensitization, tolerance, and place conditioning during repeated exposure.
Copyright © 2011 Elsevier Ireland Ltd. All rights reserved.
Figures
Fig. 1
Acute nicotine administration increases planarian motility and stereotypy. Planarians were exposed to different concentrations of nicotine (0.01, 0.03, 0.1, 0.3, 1, 3, 5, 10 mM). Motility and stereotypical activity was quantified during 5 min of nicotine exposure and presented as mean activity counts + S.E.M in 5 min. **p < 0.01 compared to water control for stereotypical activity and ++p < 0.01 compared to water control for motility. N = 8 planarians per group.
Fig. 2
Nicotine (0.03 mM) produces abstinence-induced withdrawal behavior in planarians. Planarians pre-treated with nicotine (N) or water (W) for 60 min were then tested in N or water (W) for 5 min. Data are presented as mean motility counts + S.E.M in 5 min. *p < 0.05 compared to W/W and ++p < 0.01 compared to N/W. N = 8 planarians per group.
Fig. 3
Low concentrations of nicotine produce sensitization of stereotypical activity and high concentrations of nicotine produce tolerance to stereotypical activity. Planarians were exposed to nicotine (0.1, 0.3, 1, 3 mM) twice on day 1 (120 min apart) and then re-exposed to the same concentration of nicotine for 5 min on day 4. Data are expressed as mean stereotypy counts + S.E.M. during 5 min of nicotine exposure versus day (1, 1’, 4). **p < 0.01 compared to the stereotypy counts produced by initial drug exposure (day 1). N = 8 planarians per group. Box) The percentage of the initial nicotine response (day 1) produced by nicotine challenge on day 4 is plotted versus log nicotine concentration.
Fig. 4
Nicotine elicits environmental place conditioning in planarians. Table) The conditioning phase paired nicotine (N) (0.1 mM) or water (W) with the ambient light (L) or dark (D) for 10 min. Preference testing was conducted 2 h later when planarians were placed for 10 min at the center of a petri dish containing water (half of dish was covered on the top and bottom by paper to create a dark side and ambient light side). Data are presented as the (A) number of planarians (out of 20) that spent a greater amount of time in the dark and (B) mean preference score (s) + S.E.M. **p < 0.01, *p < 0.05 compared to W(L)/W(D). N = 20 planarians per group.
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References
- Boileau I, Dagher A, Leyton M, Gunn RN, Baker GB, Diksic M, Benkelfat C. Modeling sensitization to stimulants in humans: an [11C]raclopride/positron emission tomography study in healthy men. Arch. Gen. Psychiatry. 2006;63:1386–1395. - PubMed
- Buttarelli FR, Pontieri FE, Margotta V, Palladini G. Acetylcholine/dopamine interaction in planaria. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 2000;125:225–231. - PubMed
- Chae Y, Yeom M, Han JH, Park HJ, Hahm DH, Shim I, Lee HS, Lee H. Effect of acupuncture on anxiety-like behavior during nicotine withdrawal and relevant mechanisms. Neurosci. Lett. 2008;430:98–102. - PubMed
- Collins SL, Izenwasser S. Chronic nicotine differentially alters cocaine-induced locomotor activity in adolescent vs. adult male and female rats. Neuropharmacology. 2004;46:349–362. - PubMed
- Domino EF. Nicotine induced behavioral locomotor sensitization. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2001;25:59–71. - PubMed
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