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

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.

Psychotropic substance-seeking: evolutionary pathology or adaptation?

According to a conventional evolutionary perspective, the human propensity for substance use is the product of a 'mismatch' between emotional mechanisms that evolved in a past without pure drugs or direct routes of drug administration, and the occurrence of these phenomena in the contemporary environment. The primary purpose of this review is to assert that, contrary to the conventional view, humans have shared a coevolutionary relationship with psychotropic plant substances that is millions of years old. We argue that this 'deep time' relationship is self-evident both in the extant chemical-ecological adaptations that have evolved in mammals to metabolize psychotropic plant substances and in the structure of plant defensive chemicals that have evolved to mimic the structure, and interfere with the function, of mammalian neurotransmitters. Given this evidence, we question how emotional mechanisms easily triggered by plant toxins can have evolved. Our argument is also supported with archeological and historical evidence of substance use in antiquity suggesting that, for people in the past, psychotropic plant substances were as much a mundane everyday item as they are for many people today. Our second, and more speculative objective is to suggest provisional hypotheses of human substance-using phenomena that can incorporate the evolutionary implications of a deep time relationship between psychotropic substances and people. We discuss hypotheses of selective benefits of substance use, including the idea that neurotransmitter-analog plant chemicals were exploited as substitutes for costly, nutritionally constrained endogenous neurotransmitters. However, even if substance seeking was adaptive in the environment of our hominid ancestors, it may not still be so in the contemporary environment. Thus, the implications of our argument are not that the mismatch concept does not apply to human substance-using phenomena, but that it must be reconsidered and extended to incorporate the implications of a substance-rich, rather than substance-free, evolutionary past.

Parental investment and child health in a Yanomamö village suffering short-term food stress.

The 1998 El Niño significantly reduced garden productivity in the Upper Orinoco region in Venezuela. Consequently, parents were forced to allocate food carefully to their children. Nutrition data collected from village children combined with genealogical data allowed the determination of which children suffered most, and whether the patterns of food distribution accorded with predictions from parental investment theory. For boys, three social variables accounted for over 70% of the variance in subcutaneous fat after controlling for age: number of siblings, age of the mother's youngest child, and whether the mother was the senior or junior co-wife, or was married monogamously. These results accord well with parental investment theory. Parents experiencing food stress faced a trade-off between quantity and quality, and between investing in younger versus older offspring. In addition, boys with access to more paternal investment (i.e. no stepmother) were better nourished. These variables did not account for any of the variance in female nutrition. Girls' nutrition was associated with the size of their patrilineage and the number of non-relatives in the village, suggesting that lineage politics may have played a role. An apparent lack of relationship between orphan status and nutrition is also interesting, given that orphans suffered high rates of skin flea infections. The large number of orphans being cared for by only two grandparents suggests that grooming time may have been the resource in short supply.