Behavioral Tolerance
Considerable recent research suggests yet another, quite orthogonal mechanism for tolerance. The concept is simple: When an animal has become accustomed to receiving a drug in a certain situation and is again presented with that same situation, it anticipates the drug administration and makes compensatory responses that serve to reduce the impact of the impending presence of the drug. Given this mobilization of the body's homeostatic processes before the actual drug presentation, the drug is effectively compromised, and the result is less total drug effect or increased drug tolerance. The existence of such tolerance neither excludes the possibility of dispositional or functional tolerance nor requires their existence. Many reviews of this concept have been written (e.g., Eikelboom & Stewart, 1982; Goudie & Demellweek, 1987; O'Brien, 1976; Siegel, 1985, 1989; Siegel, Krank, & Hinson, 1987; Stewart & Eikelboom, 1987). This conceptually new type of tolerance has come to be called behavioral tolerance (Corfield-Sumner & Stolerman, 1978) because its properties easily fit a conditioning paradigm. For example, if the normal biochemistry of the mouth is disrupted by infusion of a mild acidic solution into it, the response is a reflexive increase in the flow rate of saliva to dilute and rinse away the acid. If such an event is repeated and if the organism so insulted can predict when the event will occur, it learns to anticipate it. Hence Pavlov (1927) was able to show that dogs, in the presence of stimuli predicting that acid would soon be put on their tongues, would drool in anticipation. The cues repeatedly associated with the presentation of a drug develop the capacity to elicit compensatory homeostatic responses. Now, consider the case of drugs of abuse such as heroin or alcohol. When alcohol is given and causes hypothermia, homeostatic hyperthermia-producing reflexes are elicited. If the alcohol administration is repeated and if there is some stimulus or cue that is reliably predictive of this event, the animal ought to be able to anticipate receiving the drug, make the appropriate hyperthermic response, and thus circumvent the otherwise inevitable onset of hypothermia. If this indeed happened, it would be an example of behavioral tolerance. My intent in this article is not to convince the reader that conditioning may be the predominant cause of drug tolerance. That can be done in another forum, and indeed the point has been adequately made elsewhere (Siegel, 1983, 1989; Wenger, Tiffany, Bombadier, Nicholls, & Woods, 1981; Wenger & Woods, 1984). Rather, my intent is merely to convince the reader that behavioral tolerance does exist and can become an important part of an animal's behavioral repertoire.
References
Woods, Stephen C. 1991. “The eating paradox: How we tolerate food.” Psychological review 98 (4): 488–505. doi:10.1037/0033-295X.98.4.488.0