Abstract
Neural systems mediating motivation and reward have been well described in mammalian model systems, especially with reference to reward properties of drugs of abuse. Far less is known of the neural mechanisms underlying motivation and reward in non-mammals. The behavioral procedure conditioned place preference (CPP) is often used to quantify reward properties of psychoactive drugs. The indirect dopamine agonist d-amphetamine (AMPH) is known for its properties for inducing CPP in mammals and for inducing dose-related stereotypic movements. We used the green tree frog, Hyla cinerea, to examine whether AMPH could induce both CPP and a dose response change in motor behaviors. We demonstrated that H. cinerea can show place conditioning to AMPH following 14 days of training and that AMPH can cause reversal of a strong baseline place preference. Amphetamine-treated animals (20 mg/kg b.w.) received the drug paired with the previously non-preferred context, and vehicle paired with the preferred context. Control animals received vehicle in both preferred and non-preferred contexts. Amphetamine-treated animals switched context preference following conditioning, whereas control animals did not. We also demonstrated in an open-field experiment that AMPH did not cause any noticeable changes in motor movement or behaviors across a range of doses (0, 10, 20 mg/kg b.w.). This study represents the first examination of the behavioral effects of AMPH in amphibians. These results may contribute to a better understanding of the function and pharmacology of a reward system that may mediate natural behaviors in frogs and other vertebrates.
References
1.
Agmo A, Federman I, Navarro V, Padua M, Velazquez G (1993): Reward and reinforcement produced by drinking water: role of opioids and dopamine receptor subtypes. Pharmacol Biochem Behav 46:183–194.
2.
Akins CK, Levens N, Prather R, Cooper B, Fritz T (2004): Dose-dependent cocaine place conditioning and d1 dopamine antagonist effects in male Japanese quail. Physiology Behav 82:309–315.
3.
Akins CK, Geary EH (2008): Cocaine-induced behavioral sensitization and conditioning in male Japanese quail. Pharmacol Biochem Behav 88:432–437.
4.
Barbeau A, Dallaire L, Buu NT, Veilleux F, Boyer H, de Lanney LE, Irwin I, Langston EB, Langston JW (1985): New amphibian models for the study of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Life Sci 36:1125–1134.
5.
Bardo M, Bevins R (2000): Conditioned place preference: what does it add to our preclinical understanding of drug reward. Psychopharm 153:31–43.
6.
Berridge KC (1996): Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 20:1–25.
7.
Berridge KC, Robinson TE (1998): What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309–369.
8.
Berridge KC (2007): The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology (Berl) 191:391–431.
9.
Bilbo SD, Day LB, Wilczynski W (2000): Anticholinergic effects in frogs in a Morris water maze analog. Physiol Behav 69:351–357.
10.
Brattstrom BH (1990): Maze learning in the fire-bellied toad, Bombina orientalis. J Herpetol 24:44–47.
11.
Calcagnetti DJ, Schechter MD (1992): Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51:667–672.
12.
Cheng HC, Bhatnagar RK, Long JP (1975): Dopaminergic nature of amphetamine-induced pecking in pigeons. Eur J Pharmacol 33:319–324.
13.
Chu J, Wilczynski W, Wilcox RE (2001): Pharmacological characterization of the d1- and d2-like dopamine receptors from the brain of the leopard frog, Rana pipiens. Brain Behav Evol 57:328–342.
14.
Chu J, Wilczynski W (2007): Apomorphine effects on frog locomotor behavior. Physiol Behav 91:71–76.
15.
Chu J, Rankine N (2008): The effect of dopamine agonists on swimming and climbing behavior in the green tree frog, Hyla cinerea. Soc Neurosci Annul Meeting, Washington, DC.
16.
Cohen JD, Blum KI (2002): Reward and decision. Neuron 36:193–198.
17.
Cole SO (1967): Experimental effects of amphetamine: a review. Psychol Bull 68:81–90.
18.
Darland T, Dowling JE (2001): Behavioral screening for cocaine sensitivity in mutagenized zebrafish. Proc Natl Acad Sci USA 98:11691–11696.
19.
Douglas LA, Varlinskaya EI, Spear LP (2004): Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45:153–162.
20.
Endepols H, Schul J, Gerhardt HC, Walkowiak W (2004): 6-hydroxydopamine lesions in anuran amphibians: a new model system for Parkinson’s disease? J Neurobiology 60:395–410.
21.
Gerhardt HC, Daniel RE, Perrill SA, Schramm S (1987): Mating behaviour and male mating success in the green tree frog. Anim Behav 35:1490–1503.
22.
Glagow M, Ewert J (1999): Apomorphine alters prey-catching patterns in the common toad: behavioral experiments and (14)c-2-deoxyglucose brain mapping studies. Brain Behav Evol 54:223–242.
23.
Gonzalez A, Tuinhof R, Smeets WJ (1993): Distribution of tyrosine hydroxylase and dopamine immunoreactivities in the brain of the south African clawed frog Xenopus laevis. Anat Embryol (Berl) 187:193–201.
24.
Goodman IJ (1981): Amphetamine and apomorphine induced stereotyped behavior in adult pigeons. Pharmacol Biochem Behav 15:701–704.
25.
Grubb JC (1976): Maze orientation by Mexican toads, Bufo valliceps (Amphibia, anura, bufonidae), using olfactory and configurational cues. J Herpetol 10:97–104.
26.
He X, Xiao L, Sui N (2009): Effects of sch23390 and spiperone administered into medial striatum and intermediate medial mesopallium on rewarding effects of morphine in day-old chicks. Eur J Pharmacol 2010;627:136–141.
27.
Heatwole H, Sullivan B (eds) (1995): Amphibian Biology, vol 2: Social Behavior. Australia, Surrey Beatty & Sons.
28.
Hinde RA (1982): Ethology: Its Nature and Relations with Other Sciences. New York, Oxford University Press.
29.
Idemudia SO, McMillan DE (1984): Effects of d-amphetamine on spontaneous motor activity in pigeons. Psychopharmacology (Berl) 84:315–317.
30.
Insel TR, Fernald RD (2004): How the brain processes social information: searching for the social brain. Annu Rev Neurosci 27:697–722.
31.
James JR, Young R, Rosecrans JA (2000): Conditioned place preference: an approach to evaluating positive and negative drug-induced stimuli; in Buccafusco JJ (ed): Methods of Behavior Analysis in Neuroscience. Boca Raton, CRC Press, pp 81–90.
32.
Jarosz PA, Kessler JT, Sekhon P, Coscina DV (2007): Conditioned place preferences (CPPS) to high-caloric ‘snack foods’ in rat strains genetically prone vs. resistant to diet-induced obesity: resistance to naltrexone blockade. Pharmacol Biochem Behav 86:699–704.
33.
Kelley AE, Berridge KC (2002): The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22:3306–3311.
34.
Lanuza E, Novejarque A, Martinez-Ricos J, Martinez-Hernandez J, Agustin-Pavon C, Martinez-Garcia F (2008): Sexual pheromones and the evolution of the reward system of the brain: the chemosensory function of the amygdala. Brain Res Bull 75:460–466.
35.
Lett BT, Grant VL (1989): The hedonic effects of amphetamine and pentobarbital in goldfish. Pharmacol Biochem Behav 32:355–356.
36.
Levens N, Akins CK (2001): Cocaine induces conditioned place preference and increases locomotor activity in male Japanese quail. Pharmacol Biochem Behav 68:71–80.
37.
Levens N, Akins CK (2004): Chronic cocaine pretreatment facilitates Pavlovian sexual conditioning in male Japanese quail. Pharmacol Biochem Behav 79:451–457.
38.
Liu Y, Wang ZX (2003): Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121:537–544.
39.
Marin O, Gonzalez A, Smeets WJ (1995): Evidence for a mesolimbic pathway in anuran amphibians: a combined tract-tracing/immunohistochemical study. Neurosci Lett 190:183–186.
40.
Marin O, Smeets WJ, Gonzalez A (1997): Basal ganglia organization in amphibians: catecholaminergic innervation of the striatum and the nucleus accumbens. J Comp Neurol 378:50–69.
41.
Marler CA, Chu J, Wilczynski W (1995): Arginine vasotocin injection increases probability of calling in cricket frogs, but causes call changes characteristic of less aggressive males. Horm Behav 29:554–570.
42.
Martinez I, Paredes RG (2001): Only self-paced mating is rewarding in rats of both sexes. Horm Behav 40:510–517.
43.
Martof BS (1962): Some observations on the role of olfaction among salientian amphibia. Physiol Zool 35:270–272.
44.
McKeever S, French FE (2000): Corethrellidae (diptera), vectors of present and perhaps some of the earliest anuran trypanosomes. Third Ann Virtual Conf Vet Med: Diseases of Reptiles and Amphibians.
45.
Meerts SH, Clark AS (2007): Female rats exhibit a conditioned place preference for nonpaced mating. Horm Behav 51:89–94.
46.
Munro AD (1986): The effects of apomorphine, d-amphetamine and chlorpromazine on the aggressiveness of isolated Aequidens pulcher (Teleostei, Cichlidae). Psychopharmacology (Berl) 88:124–128.
47.
Ninkovic J, Bally-Cuif L (2006): The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse. Methods 39:262–274.
48.
Numan M (2007): Motivational systems and the neural circuitry of maternal behavior in the rat. Dev Psychobiol 49:12–21.
49.
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.
50.
Panksepp JB, Lahvis GP (2006): Social reward among juvenile mice. Genes Brain Behav 6:661–671.
51.
Pfaus JG, Kippin TE, Centeno S (2001): Conditioning and sexual behavior: a review. Horm Behav 40:291–321.
52.
Rebec G (1998): Behavioral pharmacology of amphetamine; in Tarter R, Ott P, Ammerman R (eds): Handbook of Substance Abuse: Neurobehavioral Pharmacology. New York, Springer, pp 515–528.
53.
Sanchez-Camacho C, Lopez JM, Gonzalez A (2006): Basal forebrain cholinergic system of the anuran amphibian Rana Perez: evidence for a shared organization pattern with amniotes. J Comp Neurol 494:961–975.
54.
Segal DS, Kuczenski R (1994): Behavioral pharmacology of amphetamine; in Cho AK, Segal DS (eds): Amphetamine and Its Analogs. Academic Press, pp 115–150.
55.
Seiden LS, Sabol KE, Ricaurte GA (1993): Amphetamine: effects of catecholamine systems and behavior. Annu Rev Pharmacol Toxicol 32:629–677.
56.
Sherman JE, Roberts T, Roskam SE, Holman EW (1980): Temporal properties of the rewarding and aversive effects of amphetamine in rats. Pharmacol Biochem Behav 13:597–599.
57.
Smeets WJ (1994): Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates. New York, University of Cambridge Press.
58.
Smeets WJ, Gonzalez A (2000): Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res Brain Res Rev 33:308–379.
59.
Ten Eyck GR (2008): Serotonin modulates vocalizations and territorial behavior in an amphibian. Behav Brain Res 193:144–147.
60.
Tzschentke TM (2007): Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462.
61.
Wang Z, Aragona BJ (2004): Neurochemical regulation of pair bonding in male prairie voles. Physiol Behav 83:319–328.
62.
Watson KK, Platt ML (2008): Neuroethology of reward and decision-making. Philos Trans R Soc Lond B Biol Sci 363:3825–3835.
63.
Wells KB (2001): The energetics of calling in frogs; in Ryan MJ (ed): Anuran Communication. Washington, Smithsonian Institution Press, pp 45–60.
64.
Zhao B, Debski EA (2005): Serotonergic reticular formation cells in Rana pipiens: categorization, development, and rectal projections. J Comp Neurol 487:441–456.
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