The Neurobiology of Behavior

An Introduction

Gordon J. Mogenson

• Publisher: Taylor & Francis
• Year: 2018
• Print ISBN: 9781138559691
• eBook ISBN: 9781351362542
• Edition: 1
• Topic: Psychology
• Subtopic: Cognitive Neuroscience & Neuropsychology
• Index: Psychology

Originally published in 1977, the objective of this book was to examine the mechanisms by which the multiple factors or determinants – homeostatic deficits, hormonal influences, circadian rhythms, experiential and cognitive factors – become translated by the central nervous system into thermoregulatory, feeding, sexual, aggressive, and other behaviours. A conceptual framework has been used that reflects relevant contributions from biology, regulatory physiology, physiological psychology, and other neuroscience disciplines. The final chapter deals with difficulties in brain-behaviour research in relation to experimental strategies and with crucial problems for future investigation.

1

Introduction

This book is concerned with brain function and behavior and specifically with the neural substrates of thermoregulatory, feeding, sexual and aggressive behaviors. These and other behaviors shown in Figure 1.1 are usually designated as motivated behaviors, because they are goal-directed and persistent: a tiger hunts for food; a zebra searches for water; a chimpanzee builds a nest and goes to sleep; a gull drives other birds from its home territory; a child plays with a toy; a mathematician solves a complex problem. Motivation and motivated behaviors are not very satisfactory as scientific terms, however, because they have not been defined precisely, and there have been vigorous controversies about their meaning.¹ These terms are used in this book with some reservation and are used only in a descriptive sense and as a shorthand to facilitate communication. When the neural substrates of these behaviors are better understood, these terms and such inferred concepts as drive will be unnecessary. In the meantime motivation and related terms must be used with caution, the main justification being their role as a reminder to the neurobiologist of the nature and dimension of the task of providing an experimental and theoretical analysis of behavior.

The term motivation was introduced 35 or 40 years ago to recognize that certain behaviors are goal-directed and persistent but more importantly to recognize that the so-called motivated behaviors could not be accounted for in terms of external stimuli—as reflex responses or sequential chains of reflexes. Rather, the initiation of feeding, drinking, sexual, and other behaviors seemed to depend on the current physiological state of the animal, on hormones, and past experience, as well as on events or stimuli in the external environment. When a serious interest in investigating the neural substrates of these behaviors began in the 1940s and 1950s, dramatic experimental observations and the theoretical models to account for them emphasized certain factors (e.g., biological deficits), ignored others (e.g., experiential influences), and directed attention to the hypothalamus as a critical neural integrative site. These empirical and theoretical advances were strongly influenced, as indicated later in this chapter, by important events in biology and in regulatory physiology—feeding, thermoregulatory, and other behaviors were shown to have biological significance in that they contributed to the homeostasis of the internal environment as well as in adapting the animal to the external environment. Accordingly, the theoretical models that emphasized homeostatic factors and hypothalamic integrative mechanisms had a scientific credibility that made them the center of attention for a number of years, and the more nebulous experiential and cognitive determinants of behavior, which are associated with more complex and sophisticated regions of the forebrain about which little is known, were ignored.

FIG. 1.1 These pictures illustrate the variety of behaviors that have been designated as motivated behavior. Top left—Canadian wolves stalk their prey, the buffalo. (From Young & Goldman, 1944.) Top middle-Thirsty dog drinking water from a stream. Top right-Hostile aggressive behavior of a dog toward another dog. (From Darwin, 1872/1965. Reprinted by permission of the University of Chicago Press. ©1965 by The University of Chicago.) Bottom left-A male baboon exposes his large canine teeth to intimidate spectators. (Photo courtesy of Brian Soper). Bottom middle—Monkey engaged in attempting to solve a mechanical puzzle. (Photo courtesy of Dr. H. F. Harlow.) Bottom right—A man endeavouring to scale a mountain peak.

Events of the last few years have indicated the shortcomings of this approach and led to a reassessment of classical concepts and, in some instances, to a reinterpretation of earlier experimental findings. A more balanced approach is needed that takes into account the role of various factors and determinants of behavior. The distinctive feature of this book is the recognition that several factors contribute to thermoregulatory, feeding, aggressive, and other behaviors and that they contribute differentially depending on the species, the sex of the animal, the behavior, the internal physiological state, the circumstances of the environment, past experience, and the stage of ontogenetic development. The major objective is to consider the neural substrates of certain behaviors that have been investigated in the laboratory, but in each case, this is done from the perspective of the characteristics and determinants of the behavior.

THE NATURE AND DETERMINANTS OF MOTIVATED BEHAVIORS

Characteristics of Motivated Behaviors

The behaviors considered in this book, such as seeking water or food, building a shelter from the cold, escaping from a predator, or defending a “home territory,” are typically goal-directed. It was Charles Darwin (1859), in the middle of the nineteenth century, who suggested that such behaviors are “purposive” because of their biological significance in that they are adaptive to the habitat and “life style” of the animal and directed toward goals: feeding behavior has a preservative function; sleep a restorative function; aggression a protective function; and sexual behavior contributes to species perpetuation. Darwin suggested that the evolution of these species-specific adaptive behaviors is as important to the survival of the animal as the evolution of morphological characteristics. The biological significance of behavioral responses was further demonstrated more than 75 years later in a series of experiments by Curt Richter (1943), who showed that a number of behaviors contribute to homeostasis (Cannon, 1932)—they are “self-regulatory”.²

Another prominent characteristic of many motivated behaviors is their strength and persistence (Figure 1.1): A wolf will pursue its prey for hours; a zebra will go for miles to reach water; a mother rat will cross an electrified grid tolerating very painful shock to reach her pups; a mountain climber struggles for days to reach the summit; a young man studies for several years for a medical degree in order to practice medicine. When behavior becomes intense, erratic, and difficult to inhibit, such as aggressive behavior, the designation emotional behavior is frequently used. It has been suggested that behaviors of this sort are associated with higher levels of arousal or activation of the central nervous system (Lindsley, 1951; Hebb, 1955).

A number of motivated behaviors occur in a periodic fashion: A rat feeds every few hours; a cow drinks water two or three times a day; a female dog mates twice a year; a bear hibernates in the late fall. Such periodicity may be the result of the disappearance or removal of the internal or external stimuli that initiated the behavior and the occurrence of other stimuli, or it may be due to hormonal changes, or to the operation of a “biological clock.” Under certain conditions, two or more motivated behaviors may compete with one another; “timesharing” is a prominent feature of motivated behaviors (McFarland, 1974). For example, feeding may be postponed in the presence of strong “hunger signals” because of the higher priority of another activity, such as escape by the buffalo from a predator or sexual behavior in the receptive female rat. The Great Tit Papus Major, which eats two or three meals per hour during the day, does not feed at night and is presumably very hungry in the morning. Yet feeding is postponed while it engages in territorial behavior (McFarland, 1975). It appears from these examples that “motivational time-sharing” may operate on a competitive basis. There is, however, an overall organization of motivated behaviors so that they contribute to “biological fitness” and survival (McFarland, 1974).

In summary, motivation—a rather unsatisfactory term from the scientific point of view—refers to a heightened level of consciousness or arousal resulting from alterations in CNS activity and usually accompanied by responses of the whole animal in its external environment (behavioral responses). These behavioral responses are frequently characterized by their purposiveness, persistence, and periodicity. Because several factors that initiate various motivated behaviors may be present at the same time, the particular behavior observed may reflect priorities and compromises in accordance with changes in the internal and external environments; this is “motivational time-sharing.’’

Many investigators of the neural substrates of feeding, drinking, copulation, and aggression have only a secondary interest in behavior. They are concerned primarily with trying to understand how the brain works. Physiologists in particular, but also a number of physiological psychologists, interested in how the brain controls feeding, drinking, sleep, and waking, have not been very sophisticated and thorough in the behavioral aspects of their investigations and in the techniques of behavioral analysis (for further discussion, see Chapter 10). It is not uncommon to designate an inferred central state (e.g., the animal is attentive or fearful) rather than to objectively describe a particular behavioral pattern. Even Charles Darwin sometimes departed from providing a description of the actual behavior of animals. A number of examples may be found in Chapter 3 of Darwin’s The Descent of Man (1874); for example, “In the Zoological Gardens I saw a baboon who always got into a furious rage when his keeper took out a letter or book and read it aloud to him [p.87].”

Therefore, before going on to deal with the determinants of motivated behaviors, it seems appropriate to consider briefly what is actually observed or measured when behavior is being investigated.

The Observation and Description of Motivated Behaviors

According to Hinde (1970), there are two ways to describe behavior: in terms of the “strength, degree, and patterning of muscular contractions [p. 11]” or in terms of the “consequences” of the sequence of muscular contractions.

This distinction is illustrated by the classical studies by Tinbergen (1951) of courtship behavior in the stickleback (Figure 1.2). The left part of the figure illustrates the sequential response components, and the lower right portion of the figure illustrates the final consequence. Whether the behavior is dealt with in terms of “spatio-temporal patterns of muscle contractions” or “description by consequence” may sometimes depend on whether one is concerned with the appetitive phase or the consummatory phase of motivated behavior.³ The con-summatory phase is usually more stereotyped—for example, rats lap at a water spout at a stable rate of seven laps per second—and an account in terms of spatio-temporal patterns of skeletomotor responses is possible. The appetitive phase is typically more complex and variable, and, because it is difficult to provide a description in terms of patterns of muscle contractions, it is, according to Hinde, more feasible and appropriate to use description by consequence.

FIG. 1.2 Courtship behavior of the three-spined stickleback illustrating the mutually releasing actions of the male and female partners. Ethologists refer to the highly stereotyped and stable sequence of motor responses as fixed action patterns, and one of their major tasks has been to try to identify the specific stimuli (sign stimuli or releasers) that trigger the fixed action patterns. Releasing stimuli, like the fixed action patterns they initiate, are assumed to be species-specific and include the odor or some visual stimulus provided by another behaving animal, and in particular such stimuli provided by a member of the same species as shown here. (From Tinbergen, 1951, as adapted by Eibl-Eibesfeldt, 1970. By permission of the Oxford University Press.)

Behavior is frequently “measured” by the cumulative record of lever presses to turn on a heat lamp, number of grams of food eaten, number of laps at a water spout, or for sexual behavior, number of intromissions and ejaculations. For some of these “measures of behavior,” it is not even necessary to observe the animal directly; an account or description of “spatio-temporal patterns of muscle contractions” is not being used, rather a quantitative measure of the consequences of the behavior. However, relying on “description by consequence” can result in the erroneous interpretation of experimental observations, and, as indicated in later chapters, it may be necessary to use other behavioral measures including analysis of sequential response components.

To assist in scientific investigation, the strategy of “simplification of phenomenon” is frequently used. The experimental study of behavior has been no exception, and because behavior is exceedingly complex, this approach is useful and often essential. An effective and widely used procedure for simplifying an animal’s behavior is to simplify its environment—a strategy of research used to great advantage by Skinner (1938) and his followers (see Teitelbaum, 1976). The animal is provided an opportunity to make an arbitrary response to obtain food or other appropriate reward, usually by placing a manipulandum in the experimental chamber, such as a lever to be pressed or a disk to be pecked (see Figures 1.3 and 3.8). The rate of making the operant response is used as a criterion and quantitative index of motivation. Although this research strategy enables the investigator to perform a well-controlled study of behavior and to obtain quantitative measures that are highly reliable, it has the shortcoming that the behavior is often rather artificial and that certain factors or determinants that normally initiate or influence the behaviors are operative only to a minimal extent or are even absent. Some ethologists have been particularly critical of these limitations of laboratory studies of behavior, suggesting that they are sometimes analogous to the study of behavior in “solitary confinement” (see Collier et al., 1976, p. 31). They point out that an understanding of behavior must take into account an animal’s evolutionary history and its habitat and ecological niche, as well as its physiological state and present environmental circumstances. This is one of the major reasons why the neural substrates of behavior are considered, in subsequent chapters of this book, from the perspective of the various factors or determinants of the behaviors.

FIG. 1.3 A porpoise jumps out of the water to receive a food reward from the keeper’s hand.

FACTORS THAT INITIATE AND INFLUENCE MOTIVATED BEHAVIOR

It was noted in the introduction to this chapter that a number of factors initiate and contribute to thermoregulatory, feeding, drinking, sexual, and other behaviors. They include internal deficit signals, hormones, circadian rhythms, external stimuli, and experiential and cognitive factors. In this section the role of these...

Table of contents

• Cover
• Half Title
• Title Page
• Copyright Page
• Table of Contents
• Preface
• 1. INTRODUCTION
• 2. BIOLOGICAL FOUNDATIONS, EXPERIMENTAL STRATEGIES, AND TECHNIQUES FOR THE STUDY OF MOTIVATED BEHAVIORS
• 3. THERMOREGULATORY BEHAVIOR
• 4. FEEDING BEHAVIOR
• 5. DRINKING BEHAVIOR
• 6. SEXUAL BEHAVIOR: by Boris Gorzalka and Gordon Mogenson
• 7. SLEEP AND WAKING
• 8. BRAIN SELF-STIMULATION BEHAVIOR: by E. T. Rolls and G. J. Mogenson
• 9. EMOTIONAL BEHAVIORS
• 10. PROBLEMS AND STRATEGIES FOR FUTURE RESEARCH
• References
• Glossary
• Author Index
• Subject Index