Some new speculative ideas about the “behavioral homeostasis theory” as to how the simple learned behaviors of habituation and sensitization improve organism survival throughout phylogeny

Abstract

This paper explores further the “behavioral homeostasis theory” (BHT) regarding the evolutionary significance for organism survival of the two simple non-associative rapidly learned behaviors of habituation and sensitization. The BHT postulates that the evolutionary function of habituation and sensitization throughout phylogeny is to rapidly maximize an organism’s overall readiness to cope with new stimuli and to minimize unnecessary energy expenditure. These behaviors have survived with remarkable similarity throughout phylogeny from aneural protozoa to humans. The concept of “behavioral homeostasis” emphasizes that the homeostatic process is more than just maintaining internal equilibrium in the face of changing internal and external conditions. It emphasizes the rapid internal and external effector system changes that occur to optimize organism readiness to cope with any new external stimulus situation. Truly life-threatening stimuli elicit instinctive behavior such as fight, flee, or hide. If the stimulus is not life-threatening, the organism rapidly learns to adjust to an appropriate level of overall responsiveness over stimulus repetitions. The rapid asymptotic level approached by those who decrease their overall responsiveness to the second stimulus (habituaters) and those who increase their overall responsiveness to an identical second stimulus (sensitizers) not only optimizes readiness to cope with any new stimulus situation but also reduces unnecessary energy expenditure. This paper is based on a retrospective analysis of data from 4 effector system responses to eight repetitive tone stimuli in adult human males. The effector systems include the galvanic skin response, finger pulse volume, muscle frontalis and heart rate. The new information provides the basis for further exploration of the BHT including new predictions and proposed relatively simple experiments to test them.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Acknowledgments

The senior author is greatly indebted to the late Professor E.N. Sokolov of Moscow State Lomonosov University for his insightful and supportive comments and thoughts on the original “BHT”. I would like to thank Prof. R. Reep of the University of Florida and his colleague, Prof. G. Bauer, of the New College of Florida for their helpful comments. I wish to thank the anonymous reviewers for their insightful comments and suggestions which greatly improved this paper. I also would like to thank the VA Greater Los Angeles Health Care System for its support in the preparation of this article.

Notes

a A recent paper on neuronal homeostasis²⁰ notes that “homeostatic mechanisms fit into a hierarchy which operates on the levels of single proteins, protein networks, whole cells, cellular networks, organs and ultimately entire organisms.” This article is very relevant to the BHT.

b The galvanic skin response (GSR) consists of the difference function derived by subtracting the palmar skin conductance level (SCL) immediately before stimulus onset from the highest skin conductance level (SCL) reached within 10 sec after stimulus onset for each subject on each trial.

c Many words have been used to signify what we term “alertness level”. They include “awareness”, “vigilance”, “activity level”, “detection”, “wakefulness”, and “readiness”. In this paper, when discussing human responsiveness to a new stimulus, we use the term “alertness level” as measured by the SCL prior to the new stimulus.

d A recently published paper on circadian rhythmicity in mammals suggests that the suprachiasmatic nucleus (SCN) in the hypothalamus functions as the body’s “master clock.” It synchronizes all of the body’s peripheral clocks. Thus, such a higher brain center or “master clock” could play a major role in determining the “initial direction of overall body energy expenditure change” of the combined body effector systems, i.e., habituation or sensitization from trial 1 to trial 2 in mammals, depending on the phase of the circadian cycle, i.e., the “level of alertness,” at the start of a new repetitive stimulus.²⁷