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Revealing the paradox of drug reward in human evolution.

Sullivan RJ, Hagen EH, Hammerstein P - Proc. Biol. Sci. (2008)

Bottom Line: Thus, the human propensity to seek out and consume plant neurotoxins is a paradox with far-reaching implications for current drug-reward theory.We sketch some potential resolutions of the paradox, including the possibility that humans may have evolved to counter-exploit plant neurotoxins.Resolving the paradox of drug reward will require a synthesis of ecological and neurobiological perspectives of drug seeking and use.

View Article: PubMed Central - PubMed

Affiliation: Department of Anthropology, California State University, Sacramento, CA 95819, USA. sullivar@csus.edu

ABSTRACT
Neurobiological models of drug abuse propose that drug use is initiated and maintained by rewarding feedback mechanisms. However, the most commonly used drugs are plant neurotoxins that evolved to punish, not reward, consumption by animal herbivores. Reward models therefore implicitly assume an evolutionary mismatch between recent drug-profligate environments and a relatively drug-free past in which a reward centre, incidentally vulnerable to neurotoxins, could evolve. By contrast, emerging insights from plant evolutionary ecology and the genetics of hepatic enzymes, particularly cytochrome P450, indicate that animal and hominid taxa have been exposed to plant toxins throughout their evolution. Specifically, evidence of conserved function, stabilizing selection, and population-specific selection of human cytochrome P450 genes indicate recent evolutionary exposure to plant toxins, including those that affect animal nervous systems. Thus, the human propensity to seek out and consume plant neurotoxins is a paradox with far-reaching implications for current drug-reward theory. We sketch some potential resolutions of the paradox, including the possibility that humans may have evolved to counter-exploit plant neurotoxins. Resolving the paradox of drug reward will require a synthesis of ecological and neurobiological perspectives of drug seeking and use.

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Data from the US National Survey on Drug Use and Health 2004: drug use in the last year.
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fig1: Data from the US National Survey on Drug Use and Health 2004: drug use in the last year.

Mentions: Second, modern euphoric drugs, like heroin, might represent a genuine evolutionary mismatch—drugs that are vastly more pleasurable than any neurotoxins occurring naturally in ancestral environments (Nesse & Berridge 1997; Smith 1999; Nesse 2002). Yet, in population terms, euphoric drug use is trivial when compared with mundane drugs such as tobacco, cannabis and betel nut. We compiled data from the 2004 annual federal survey of drug use in the USA, to show that regular users of heroin are an extremely small proportion of the population (0.2%) and even the numbers of regular users of cocaine, ‘crack’ and amphetamines are markedly smaller (2.4, 0.5 and 0.6% of the population, respectively) than the proportions of tobacco and cannabis users (34 and 11%, respectively, ‘used in the last year’; figure 1). These data suggest that the exception—use of euphoric drugs by very small proportions of human populations—has been used to prove the ‘rule’ of hedonic drug reward. Stiff legal penalties might partially explain the exceptionally low frequency of euphoric drug consumption (DuPont & Voth 1995), but they obviously cannot explain the high frequency of non-euphoric drug consumption. Euphoric drug use is a poor model for a general theory of human, or mammalian, drug use. We suggest that commonly used non-euphoric drugs should be the basis for new models of human substance use that reflect major, rather than minor, population-use trends.


Revealing the paradox of drug reward in human evolution.

Sullivan RJ, Hagen EH, Hammerstein P - Proc. Biol. Sci. (2008)

Data from the US National Survey on Drug Use and Health 2004: drug use in the last year.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2367444&req=5

fig1: Data from the US National Survey on Drug Use and Health 2004: drug use in the last year.
Mentions: Second, modern euphoric drugs, like heroin, might represent a genuine evolutionary mismatch—drugs that are vastly more pleasurable than any neurotoxins occurring naturally in ancestral environments (Nesse & Berridge 1997; Smith 1999; Nesse 2002). Yet, in population terms, euphoric drug use is trivial when compared with mundane drugs such as tobacco, cannabis and betel nut. We compiled data from the 2004 annual federal survey of drug use in the USA, to show that regular users of heroin are an extremely small proportion of the population (0.2%) and even the numbers of regular users of cocaine, ‘crack’ and amphetamines are markedly smaller (2.4, 0.5 and 0.6% of the population, respectively) than the proportions of tobacco and cannabis users (34 and 11%, respectively, ‘used in the last year’; figure 1). These data suggest that the exception—use of euphoric drugs by very small proportions of human populations—has been used to prove the ‘rule’ of hedonic drug reward. Stiff legal penalties might partially explain the exceptionally low frequency of euphoric drug consumption (DuPont & Voth 1995), but they obviously cannot explain the high frequency of non-euphoric drug consumption. Euphoric drug use is a poor model for a general theory of human, or mammalian, drug use. We suggest that commonly used non-euphoric drugs should be the basis for new models of human substance use that reflect major, rather than minor, population-use trends.

Bottom Line: Thus, the human propensity to seek out and consume plant neurotoxins is a paradox with far-reaching implications for current drug-reward theory.We sketch some potential resolutions of the paradox, including the possibility that humans may have evolved to counter-exploit plant neurotoxins.Resolving the paradox of drug reward will require a synthesis of ecological and neurobiological perspectives of drug seeking and use.

View Article: PubMed Central - PubMed

Affiliation: Department of Anthropology, California State University, Sacramento, CA 95819, USA. sullivar@csus.edu

ABSTRACT
Neurobiological models of drug abuse propose that drug use is initiated and maintained by rewarding feedback mechanisms. However, the most commonly used drugs are plant neurotoxins that evolved to punish, not reward, consumption by animal herbivores. Reward models therefore implicitly assume an evolutionary mismatch between recent drug-profligate environments and a relatively drug-free past in which a reward centre, incidentally vulnerable to neurotoxins, could evolve. By contrast, emerging insights from plant evolutionary ecology and the genetics of hepatic enzymes, particularly cytochrome P450, indicate that animal and hominid taxa have been exposed to plant toxins throughout their evolution. Specifically, evidence of conserved function, stabilizing selection, and population-specific selection of human cytochrome P450 genes indicate recent evolutionary exposure to plant toxins, including those that affect animal nervous systems. Thus, the human propensity to seek out and consume plant neurotoxins is a paradox with far-reaching implications for current drug-reward theory. We sketch some potential resolutions of the paradox, including the possibility that humans may have evolved to counter-exploit plant neurotoxins. Resolving the paradox of drug reward will require a synthesis of ecological and neurobiological perspectives of drug seeking and use.

Show MeSH
Related in: MedlinePlus