Skip to main content
Log in

Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena

  • Review
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Recent investigations in invertebrate neurobiology have opened up new lines of research into the basic roles of behavioral, neurochemical, and physiological effects in complex behavioral phenomena, such as aggression and drug-sensitive reward. This review summarizes a body of quantitative work, which identifies biogenic amines as a pharmacological substrate for motivated behaviors in the crayfish, Orconectes rusticus. Specifically, this paper details progress that has (1) explored links between serotonin and an individual’s aggressive state, and (2) demonstrated the existence of crayfish reward systems that are sensitive to human drugs of abuse, such as psychostimulants. First, we summarize a set of experimental approaches that explore aggression in crayfish and the significance of aminergic systems in its control. Agonistic behavior in crustaceans can be characterized within a quantitative framework; different types of behavioral plasticity in aggressive behavior are in need of physiological explanation, and pharmacological intervention involving serotonergic systems bring about characteristic changes in behavior. A second set of experiments demonstrates that psychostimulants (cocaine and D-amphetamine) serve as rewards when an intra-circulatory infusion is coupled to a distinct visual environment. Work in novel model systems such as crayfish constitutes a useful comparative approach to the study of aggression and drug addiction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Andretic R, Hirsh J (2000) Circadian modulation of dopamine receptor responsiveness in Drosophila melanogaster. Proc Natl Acad Sci USA 97:1873–1878

    Article  Google Scholar 

  • Andretic R, Chaney S, Hirsh J (1999) Requirement of circadian genes for cocaine sensitization in Drosophila. Science 285:1066–1068

    Article  Google Scholar 

  • Ase AR, Reader TA, Hen R, Riad M, Descarries L (2000) Altered serotonin and dopamine metabolism in the CNS of serotonin 5-HT1A or 5-HT1B receptor knockout mice. J Neurochem 75:2415–2426

    Article  Google Scholar 

  • Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641–688

    Article  Google Scholar 

  • Belthoff JR, Gowaty PA (1996) Male plumage coloration affects dominance and aggression in female house finches. Bird Behav 11:1–7

    Google Scholar 

  • Beltz BS, Kravitz EA (1986) Aminergic and peptidergic neuromodulation in crustacea. J Exp Biol 124:115–141

    Google Scholar 

  • Beltz BS, Kravitz EA (1987) Physiological identification, morphological analysis, and development of identified serotonin-proctolin containing neurons in the lobster ventral nerve cord. J Neurosci 7:533–546

    Google Scholar 

  • Beyer C, Feder HH (1987) Sex steroids and afferent input—their roles in brain sexual differentiation. Annu Rev Physiol 49:349–364

    Article  Google Scholar 

  • Bicker G, Menzel R (1989) Chemical codes for the control of behavior in arthropods. Nature 337:33–39

    Article  Google Scholar 

  • Bolyard KJ, Rowland WJ (2000) The effects of spatial context and social experience on the territorial aggression of male threespine stickleback. Behavior 137:845–864

    Article  Google Scholar 

  • Borowsky B, Adham N, Jones KA, Raddatz R, Artymyshyn R, Ogozalek KL, Durkin MM, Lakhlani PP, Bonini JA, Pathirana S, Boyle N, Pu XS, Kouranova E, Lichtblau H, Ochoa FY, Branchek TA, Gerald C (2001) Trace amines: identification of a family of mammalian G protein-coupled receptors. Proc Natl Acad Sci USA 98:8966–8971

    Article  Google Scholar 

  • Cases O, Seif I, Grimsby J, Gaspar P, Chen K, Pournin S, Muller U, Aguet M, Babinet C, Shih JC, Demaeyer E (1995) Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268:1763–1766

    Google Scholar 

  • Chan Y-M, Jan YN (1999) Conservation of neurogenic genes and mechanisms. Curr Opin Neurobiol 9:582–588

    Article  Google Scholar 

  • Chen S, Lee AY, Bowens N, Huber R, Kravitz EA (2002) Fighting fruit flies: a model system for the study of aggression. Proc Natl Acad Sci USA 99:5664–5668

    Article  Google Scholar 

  • Dawkins MS (1995) Unravelling animal behavior. Longman Scientific, Essex

    Google Scholar 

  • Dillon JE, Raleigh MJ, McGuire MT, Bergin-Pollack D, Yuwiler A (1992) Plasma catecholamines and social behavior in male vervet monkeys (Cercopithecus aethiops sabaeus). Physiol Behav 51:973–977

    Article  Google Scholar 

  • Doernberg S, Cromarty SI, Heinrich R, Beltz BS, Kravitz EA (2001) Agonistic behavior in naive juvenile lobsters depleted of serotonin by 5,7-dihydroxytryptamine. J Comp Physiol A 187:91–103

    Article  Google Scholar 

  • Durden DA, Davis BA (1993) Determination of regional distributions of phenylethylamine and meta- and para-tyramine in rat brain regions and presence in human and dog plasma by an ultra-sensitive negative chemical ion gas chromatography-mass spectrometric (NCI-GC-MS) method. Neurochem Res 18:995–1002

    Article  Google Scholar 

  • Edwards DH, Kravitz EA (1997) Serotonin, social status and aggression. Curr Opin Neurobiol 7:812–819

    Article  Google Scholar 

  • Eichelman BS (1990) Neurochemical and psychopharmacologic aspects of aggressive behavior. Annu Rev Med 41:149–158

    Google Scholar 

  • Fickbohm DJ, Spitzer N, Katz PS (2000) Serotonin homeostasis in the brain of Tritonia diomedea. Soc Neurosci Abstr 26(1):3435

    Google Scholar 

  • Hall FS, Devries AC, Fong GW, Huang S, Pert A (1999) Effects of 5,7-dihydroxytryptamine depletion of tissue serotonin levels on extracellular serotonin in the striatum assessed with in vivo microdialysis: relationship to behavior. Synapse 33:16–25

    Article  CAS  PubMed  Google Scholar 

  • Harrison AA, Everitt BJ, Robbins TW (1997) Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacology 133:329–342

    Article  CAS  PubMed  Google Scholar 

  • Harris-Warrick RM, Kravitz EA (1984) Cellular mechanisms for modulation of posture by octopamine and serotonin in the lobster. J Neurosci 4:1976–1993

    Google Scholar 

  • Heinrich R, Wenzel B, Elsner NA (2001) Role for muscarinic excitation: control of specific singing behavior by activation of the adenylate cyclase pathway in the brain of grasshoppers. Proc Natl Acad Sci USA 98:9919–9923

    Article  Google Scholar 

  • Hen R (1992) Of mice and flies: commonalities among 5-HT receptors. Trends Pharmacol Sci 13:160–165

    Article  Google Scholar 

  • Hen R (1993) Structural and functional conservation of serotonin receptors throughout evolution. EXS 63:266–278

    Google Scholar 

  • Hill EM, Newlin DB (2002) Evolutionary psychobiological approaches to addiction. Addiction 97:375–379

    Article  Google Scholar 

  • Hinde RA (1982) Ethology. Oxford University Press, Oxford

    Google Scholar 

  • Huber R, Delago A (1998) Serotonin alters decisions to withdraw in fighting crayfish, Astacus astacus: the motivational concept revisited. J Comp Physiol A 182:573–583

    Article  Google Scholar 

  • Huber R, Orzeszyna M, Pokorny N, Kravitz EA (1997) Biogenic amines and aggression: experimental approaches in crustaceans. Brain Behav Evol 50:60–68

    Google Scholar 

  • Huber R, Smith K, Delago A, Isaksson K, Kravitz EA (1997) Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. Proc Natl Acad Sci USA 94:5939–5942

    Article  Google Scholar 

  • Immelmann K, Beer C (1989) A dictionary of ethology. Harvard University Press, Cambridge

    Google Scholar 

  • Insel TR, Winslow JT (1998) Serotonin and neuropeptides in affiliative behaviors. Biol Psychiatry 44:207–219

    Article  Google Scholar 

  • Ison M, Fachinelli C, Rodriguez-Echandia EL (1996) Effect of the i.c.v. injection of 5,7-di-hydroxytryptamine on the aggressive behavior of dominant and submissive pigeons (Columba livia). Pharmacol Biochem Behav 53:951–955

    Article  Google Scholar 

  • Johanson CE, Balster RL, Bonese K (1976) Self-administration of psychomotor stimulant drugs: the effects of unlimited access. Pharmacol Biochem Behav 4:45–51

    Article  CAS  PubMed  Google Scholar 

  • Koprowska M, Romaniuk A (1997) Behavioral and biochemical alterations in median and dorsal Raphe nuclei lesioned cats. Pharmacol Biochem Behav 56:529–540

    Article  Google Scholar 

  • Kravitz EA (1988) Hormonal control of behavior: amines and the biasing of behavioral output in lobsters. Science 241:1775–1781

    Google Scholar 

  • Kravitz EA (2000) Serotonin and aggression: insights gained from a lobster model system and speculations on the role of amine neurons in a complex behavior. J Comp Physiol A 186:1221–1238

    Article  Google Scholar 

  • Kroeze WK, Roth BL (1998) The molecular biology of serotonin receptors: therapeutic implications for the interface of mood and psychosis. Biol Psychiatry 44:1128–1142

    Article  Google Scholar 

  • Kusayama T, Watanabe S (2000) Reinforcing effects of methamphetamine in planarians. Neuroreport 11:2511–2513

    Google Scholar 

  • Lederhendler I, Shulkin J (2000) Behavioral neuroscience: challenges for the era of molecular biology. Trends Neurosci 23:451–454

    Article  Google Scholar 

  • Lent CM (1984) Quantitative effects of a neurotoxin upon serotonin levels within tissue compartments of the medicinal leech. J Neurobiol 15(5):309–323

    Article  Google Scholar 

  • Libersat F, Pflüger H-J (2004) Monoamines and the orchestration of behavior. Bioscience 54:17–25

    Google Scholar 

  • Lidov HGW, Molliver ME (1982) Immunocytochemical study of the development of serotonergic neurons in the rat. Brain Res Bull 9:559–604

    Article  Google Scholar 

  • Livingstone MS, Harris-Warrick RM, Kravitz EA (1980) Serotonin and octopamine produce opposite postures in lobsters. Science 208:76–79

    Google Scholar 

  • Lopez P, Martin J, Cuadrado M (2002) Pheromone-mediated intrasexual aggression in male lizards, Podarcis hispanicus. Aggr Behav 28:154–163

    Article  Google Scholar 

  • Lorenz KZ (1966) On aggression. Harcourt Brace, New York

    Google Scholar 

  • MacLean PD (1990) The triune brain in evolution: role in palaeocerebral functions. Plenum, New York

    Google Scholar 

  • Mcclung C, Hirsh J (1999) The trace amine tyramine is essential for sensitization to cocaine in Drosophila. Curr Biol 9:853–860

    Article  Google Scholar 

  • Nader K, Bechara A, van-der-Kooy D (1997) Neurobiological constraints on behavioral models of motivation. Annu Rev Psychol 48:85–114

    Article  Google Scholar 

  • Nelson RJ, Chiavegatto S (2001) Molecular basis of aggression. Trends Neurosci 24:713–719

    CAS  PubMed  Google Scholar 

  • Nesse RM, Berridge KC (1997) Psychoactive drug use in evolutionary perspective. Science 278:63–66

    Article  Google Scholar 

  • Nikaido T, Akiyama M, Moriay T, Shibata S (2001) Sensitized increase of period gene expression in the mouse caudate/putamen caused by repeated injection of methamphetamine. Mol Pharmacol 59:894–900

    Google Scholar 

  • O’Connor KI, Metcalfe NB, Taylor AC (1999) Does darkening signal submission in territorial contests between juvenile Atlantic salmon, Salmo salar? Anim Behav 58:1269–1276

    Article  Google Scholar 

  • Palladini G, Ruggeri S, Stocchi F, Depandis MF, Venturini G, Margotta V (1996) A pharmacological study of cocaine activity in Planaria. Comp Biochem Physiol C 115:41–45

    Google Scholar 

  • Panksepp J (1998) Affective neuroscience. The foundations of human and animal emotions. Oxford University Press, New York

    Google Scholar 

  • Panksepp JB, Huber R (2002) Chronic alterations in serotonin function: dynamic neurochemical properties in agonistic behavior of the crayfish, Orconectes rusticus. J Neurobiol 50:276–290

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Panksepp JB, Yue Z, Drerup C, Huber R (2002) Amine neurochemistry and aggression in crayfish. Microsc Res Tech 60:360–368

    Article  Google Scholar 

  • Panksepp J, Nocjar C, Burgdorf J, Panksepp JB, Huber R (2004) The role of emotional systems in addiction: a neuroethological perspective. In: Bevins RA, Bardo MT (eds) Motivational factors in the etiology of drug abuse. University of Nebraska Press, Lincoln, pp 85–126

    Google Scholar 

  • Patel TD, Azmitia EC, Zhou FC (1996) Increased 5-HT 1A receptor immunoreactivity in the rat hippocampus following 5,7 DHT lesions in the cingulum bundle and fimbria-fornix. Behav Brain Res 73:319–323

    Article  Google Scholar 

  • Peeke HVS, Blank GS, Figler MH, Chang ES (2000) Effects of exogenous serotonin on a motor behavior and shelter competition in juvenile lobsters (Homarus americanus). J Comp Physiol A 186:575–582

    Article  Google Scholar 

  • Peroutka SJ, Howell TA (1994) The molecular evolution of G protein-coupled receptors: focus on 5-hydroxytryptamine receptors. Neuropharmacology 33:319–324

    Article  Google Scholar 

  • Porzgen P, Park SK, Hirsh J, Sonders MS, Amara SG (2001) The antidepressant-sensitive dopamine transporter in Drosophila melanogaster: a primordial carrier for catecholamines. Mol Pharmacol 59:83–95

    Google Scholar 

  • Raab A, Dantzer R, Michaud B, Mormede P, Taghzouti K, Simon H, Le-Moal M (1986) Behavioral, physiological and immunological consequences of social status and aggression in chronically coexisting resident-intruder dyads of male rats. Physiol Behav 36:223–228

    Article  Google Scholar 

  • Raleigh MJ, Mcguire MT, Brammer GL, Pollack DB, Yuwiler A (1991) Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 559:181–190

    Article  CAS  PubMed  Google Scholar 

  • Ratti O (2000) Characteristics and level of aggression by female Pied Flycatchers at different distances from the nest hole. Ornis Fenn 77:11–16

    Google Scholar 

  • Robinson TE, Berridge KC (1993) The neural basis of drug craving—an incentive-sensitization theory of addiction. Brain Res Rev 18:247–291

    Article  CAS  PubMed  Google Scholar 

  • Romaniuk A, Filipczak M, Fryczak J (1987) The influence of injection of 5,6-dihydroxytryptamine to the dorsal raphe nucleus on carbachol-induced defensive behavior and regional brain amine content in the cat. Pol J Pharmacol Pharm 39:17–25

    Google Scholar 

  • Saltzman W, Schultzdarken NJ, Abbott DH (1996) Behavioral and endocrine predictors of dominance and tolerance in female common marmosets, Callithrix jacchus. Anim Behav 51:657–674

    Article  Google Scholar 

  • Seitz A (1940) Die Paarbildung bei einigen Cichliden. Z Tierpsychol 4:40–84

    Google Scholar 

  • Sitte HH, Huck S, Reither H, Boehm S, Singer EA, Pifl C (1998) Carrier-mediated release, transporter rates, and charge transfer induced by amphetamine, tyramine, and dopamine in mammalian cells transfected with the human dopamine transporter. J Neurochem 71:1289–1297

    CAS  PubMed  Google Scholar 

  • Sivam SP (1995) GBR-12909-induced self-injurious behavior: role of dopamine. Brain Res 690:259–263

    Article  Google Scholar 

  • van Staaden M, Huber R (2001) Multidisciplinary dissection of behavioral arousal: the role of muscarinic acetylcholine stimulation in grasshopper stridulatory behavior (invited commentary). Proc Natl Acad Sci USA 89(17):9468–9470

    Article  Google Scholar 

  • Stachowiak MK, Stricker EM, Jacoby JH, Zigmond MJ (1986) Increased tryptophan hydroxylase activity in serotonergic nerve terminals spared by 5,7-dihydroxytryptamine. Biochem Pharmacol 35:1241–1248

    Article  Google Scholar 

  • Summers CH, Greenberg N (1994) Somatic correlates of adrenergic activity during aggression in the lizard, Anolis carolinensis. Horm Behav 28:29–40

    Article  CAS  PubMed  Google Scholar 

  • Tierney AJ (2001) Structure and function of invertebrate 5-HT receptors a review. Comp Biochem Physiol A 128:791–804

    Google Scholar 

  • Tinbergen N (1951) The study of instinct. Oxford University Press, Oxford

    Google Scholar 

  • Torres G, Horowitz JM (1998) Activating properties of cocaine and cocaethylene in a behavioral preparation of Drosophila melanogaster. Synapse 29:148–161

    Google Scholar 

  • Vernier P, Cardinaud B, Valdenair O, Philippe H, Vincent J-D (1995) An evolutionary view of drug-receptor interaction: the bioamine receptor family. Trends Pharm Sci 16:375–381

    Article  Google Scholar 

  • Vernier P, Cardinaud B, Philippe H, Vincent J-D (1997) The classification of bioamine receptors. How helpful are molecular phylogenies? Ann N Y Acad Sci 812:141–143

    Google Scholar 

  • Walker RJ, Brooks HL, Holdendye L (1996) Evolution and overview of classical transmitter molecules and their receptors. Parasitology 113:S3-S33

    Google Scholar 

  • Wazlavek BE, Figler MH (1989) Territorial prior residence size asymmetry and escalation of aggression in convict cichlids (Cichlasoma nigrofasciatum Guenther). Aggr Behav 15:235–244

    Google Scholar 

  • Weiger WA (1997) Serotonergic modulation of behaviour: a phylogenetic overview. Biol Rev 72:61–95

    Article  Google Scholar 

  • Wieczorek M, Romaniuk A (1994) The effects of dorsal and ventral noradrenergic system lesions with DSP-4 on emotional-defensive behavior and regional brain monoamines content in the cat. Behav Brain Res 63:1–9

    Article  Google Scholar 

  • Wise RA (1998) Drug-activation of brain reward pathways. Drug Alcohol Depend 51:13–22

    Article  CAS  PubMed  Google Scholar 

  • Woo CC, Wilson DA, Sullivan RM, Leon M (1996) Early locus coruleus lesions increase the density of B-adernergic receptors in the rat main olfactory bulb of rats. Int J Dev Neurosci 14(7/8):913–919

    Article  Google Scholar 

  • Yang EJ, Phelps SM, Crews D, Wilczynski W (2001) The effects of social experience on aggressive behavior in the Green Anole Lizard (Anolis carolinensis). Ethology 107:777–793

    Article  Google Scholar 

  • Yodyingyuad U, de-la-Riva C, Abbott DH, Herbert J, Keverne EB (1985) Relationship between dominance hierarchy, cerebrospinal fluid levels of amine transmitter metabolites (5-hydroxyindole acetic acid and homovanillic acid) and plasma cortisol in monkeys. Neuroscience 16:851–858

    Google Scholar 

Download references

Acknowledgements

We are grateful to members of the Huber lab (K. Davis, K. Hock, A. Pytel, A. St ocker, K. Drerup, J Panksepp, and Dr. A. Daws) for their contributions to this work. These projects benefited immensely from the constructive criticism and creative input of Dr. Moira van Staaden. Studies reported in this paper were supported by grants NSF IBN-9874608, NSF DBI-0070334, and NIH MH62557-01.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert Huber.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huber, R. Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena. J Comp Physiol A 191, 231–239 (2005). https://doi.org/10.1007/s00359-004-0585-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-004-0585-5

Keywords

Navigation