Ecology and neurobiology of toxin avoidance and the paradox of drug reward

• Published in: Neuroscience Vol. 160; no. 1; pp. 69 - 84
• Main Authors: Hagen, E.H, Sullivan, R.J, Schmidt, R, Morris, G, Kempter, R, Hammerstein, P
• Format: Journal Article
• Language: English
• Published: Amsterdam Elsevier Ltd 21.04.2009; Elsevier
• Subjects: Animals; aversive learning; Avoidance Learning - physiology; Biological and medical sciences; Biological Evolution; Brain - drug effects; Brain - physiopathology; dopamine; Dopamine - metabolism; Ecology; Fundamental and applied biological sciences. Psychology; Humans; Models, Biological; Models, Neurological; Neurology; Neurons - drug effects; Neurons - physiology; Neurotoxins - administration & dosage; nicotine; Nicotine - administration & dosage; Nicotine - pharmacology; Nicotinic Agonists - administration & dosage; Nicotinic Agonists - pharmacology; pharmacophagy; Plants; psychoactive substance use; Reward; reward learning; Substance-Related Disorders - physiopathology; Substance-Related Disorders - psychology; Vertebrates: nervous system and sense organs; VTA; peripheral nervous system; THC; pharmacophagy; NAc; psychoactive substance use; conditioned stimulus; PNS; mesocorticolimbic dopamine system; nAChR; aversive learning; conditioned taste-aversion; MDS; US; nicotinic acetylcholine receptor; nicotine; delta-9-tetrahydrocannabinol; SNc; nucleus accumbens; CS; CTA; substantia nigra pars compacta; unconditioned stimulus; ventral tegmental area; reward learning; dopamine; DA; Dopamine; Catecholamine; Learning; Toxin; Acquisition process; Neurotransmitter; Reward; Avoidance; Nicotine
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/j.neuroscience.2009.01.077

Abstract Current neurobiological theory of drug use is based on the observation that all addictive drugs induce changes in activity of dopaminergic circuitry, interfering with reward processing, and thus enhancing drug seeking and consumption behaviors. Current theory of drug origins, in contrast, views almost all major drugs of abuse, including nicotine, cocaine and opiates, as plant neurotoxins that evolved to punish and deter herbivores. According to this latter view, plants should not have evolved compounds that reward or reinforce plant consumption. Mammals, in turn, should not have evolved reinforcement mechanisms easily triggered by toxic substances. Situated in an ecological context, therefore, drug reward is a paradox. In an attempt to resolve the paradox, we review the neurobiology of aversive learning and toxin avoidance and their relationships to appetitive learning. We seek to answer the question: why does aversive learning not prevent the repeated use of plant drugs? We conclude by proposing alternative models of drug seeking and use. Specifically, we suggest that humans, like other animals, might have evolved to counter-exploit plant neurotoxins.