Behavioral Biology

Neuroendocrine Axis

Trevor Archer, Stefan Hansen, Trevor Archer, Stefan Hansen

• Publisher: Psychology Press
• Year: 2013
• ISBN:
  9781134761258
• Edition: 1
• Topic: Psicología
• Subtopic: Historia y teoría en psicología

This book is the result of an international symposium in biological psychology, held in honor of Knut Larsson. This renowned researcher -- in his search for the true meaning of "mind vs. matter" -- became involved in many divergent areas of the field, such as the neurobiology of sexual behavior and sexual differentiation, aspects of functional neuroanatomy, behavioral endocrinology, and psychopharmacology. Through experimentation and much consultation with other area specialists, Larsson observed such phenomena as the adaptation of behavior-determining neuroendocrine events to the physical environment and the hormonal regulation of sexual behavior and differentiation. This tribute to his research presents important features of necessary paradigms for the analysis and study of experimental psychology within the biological perspective.

1 Introduction: My Journey into Biological Psychology

Knut Larsson

University of Göteborg

I entered the University of Göteborg just after the end of World War II and decided to devote the first year to study philosophy with Gunnar Aspelin, a well-known professor of philosophy. I had become interested in the problem of mind and matter during my philosophy studies in high school and wanted to know what ‘mind’ really meant before I began to study zoology or psychology. I was quickly confronted with the concept of the gestalt psychologists of an isomorphy between the phenomenon perceived and its underlying physiological substrates. Köhler (1929), the leading gestalt psychology theorist, told me that experience and matter are only different sides of the same coin. Since experienced order is a representation of a corresponding physiological order, a true description of the experience would also give access to the physiological processes determining this order. I was intrigued by this idea of an isomorphy between matter and experience, although somewhat surprised that the laws of nature would be so easily accessible.

I soon discovered, however, that the thought of an isomorphy between mind and matter was not new but had occupied philosophers for centuries (Kaila, 1944). Further, the verbal description of the immediately-given experience turned out to be far from an easy task to accomplish. For instance, when, participating in the laboratory course of psychology, I was asked to describe what I perceived as immediately presented to me in the periphery of retina, I found this task quite difficult, because the phenomenon perceived altered with the language I was using. In fact, the language did not seem to accommodate the communication of such types of experiences.

After much reading, discussion, and thinking, I concluded that the concept of an isomorphy between behavior and its physiological substrate cannot be maintained. I began, vaguely, to grasp the basic truth that each method used to investigate nature must be applied according to its own rules, having its own limitations as well as advantages.

The problem of mind and matter did not stop troubling me and I continued my readings, now confronted with the American learning theorists, at that time, the leading theorists in psychology. I read Tolman, Hull, and Skinner, and other behaviorists. Tolman called his book ”Purposive Behavior in Animals and Man”. He described the learning of rats in the maze as a formation of cognitive maps. However, the problem was, as it appeared to me, not to find the purpose in the behavior of the rat but rather the mechanisms determining the behavior. In vain, I looked for such mechanisms in the works of Tolman. Hull’s book, ”Principles of Behavior”, was no less promising than that of Tolman, and, in one respect, this approach was easier to understand. A physiological language was used which attracted me, but, again, I discovered a gap between the empirical data presented and the concepts used. On the other hand, there was Skinner, who had written a book entitled ”The Behavior of Organisms”. He, an ardent critic of the bulk of theorizing by his fellow behaviorists, could not easily be accused of making the same blunder as they did. He claimed that the task of behavioral research was to achieve control of the environment and having reached this goal as Skinner certainly had, by using bar-pressing behavior, the goal of the scientific analysis set by him was apparently achieved. But then, I wondered, why not perform the behavioral analysis directly on man? Obviously, rats and doves are not equal to man, and what allows one to generalize from animal to man?

Although the work of the American animal psychologists appealed to me in terms of the intention to understand the organization of behavior, I was deeply dissatisfied with their discussions and concepts. Either the author was a Tolman, a Hull, or a Skinner; nothing more was offered the reader, so it seemed, than descriptions of the physical world in terms of turns to left or right in correct successions performed by the rat. A task to master the physical environment, not exceeding the capacity of the animal, must, by definition, result in organized behavior according to my understanding. Yet, this conformity was of only secondary importance, our scientific object being to reveal the mechanisms behind the behavior. Only by knowing these mechanisms would we be able to generalize from animals to man. These mechanisms, I believed, must be of a biological nature. I was surprised and confused to see that the American behaviorists all presented their own closed universe of concepts and data, largely ignoring studies of animal behavior performed outside their own laboratories, and with complete disregard to the information available, even at that time, of morphology and physiology of the organism.

I decided to leave Copenhagen, where I had spent some years listening to the lectures of Edgar Rubin, a gestalt psychologist famous for his discovery of the figure-ground relationship, and went to Paris to Henri Pieron, the leader of biological psychology in Europe at that time. I spent a Spring semester at the Sorbonne, a tumultuous experience for me, not only because I was exposed for the first time to a biological-oriented teaching of psychology of high standard but also because in Paris, after the war, I saw misery which was beyond all my imagination. I met a Russian physiologist, Popov, a former student of Pavlov. He had a small laboratory of his own in the basement of the Sorbonne where he made electrophysiological recordings of conditioned reflexes. I also became acquainted with Russian work on conditioning of autonomic reflexes by reading a number of translations into French and English. Bykov and his associates conditioned various reflexes in the urinary and intestinal functions. (see Bykov 1953). The Russian research fascinated me, but the unorthodox methods used in analyzing the data and the political jargon in which the results were wrapped made me uncertain about this work. Contributing to my confusion was the lack of analysis of either side on the performances of others. The exception was a book -”Conditioned Reflexes and Neuron Organization” - written by a Polish investigator, Konorski (1948), in which he tried to integrate Pavlovian concepts with those of Sherrington. It was a delight for me to read his book; I almost learned it by heart.

I returned to Copenhagen and spent another year there occupied by attempts to grasp and integrate the different views of behavior, guided and encouraged by my philosophy teacher, Gunnar Aspelin in Lund, to whom I returned now and then and to whom I wrote many letters. After four years of study, I finished my Master’s thesis in philosophy, calling it ”The Problem of Generalization in the Study of Behavior of Animals and Man”. I concluded that nobody, so far, had approached these problems adequately. I was deeply discouraged by what I had learned, and, even worse, I did not know how to find a way out of this confusion.

Among European psychologists, only the gestalt psychologists had been interested in experimental work on animals and most of them had fled Europe long before the war. In Europe, at that time, in the beginning of the fifties, the behavior of animals was studied mainly by the ethologists, Lorentz and Tinbergen, in particular. I knew of this work but read it with disdain, burdened as it was by the heavily criticized concepts of instinct and inborn releasing mechanisms. I was, at this stage of my development, not prepared to understand the significance of this kind of work.

It was then I remembered that in Norway there had been a remarkable man, Schelderup-Ebbe, who in the early thirties had made a study, often cited, of the social life of hens in a hen yard. I heard, even then in 1952, that a small animal colony was maintained by a psychologist, Wulff Rasmussen. I, myself, had never had a rat in my hands. I decided to go to Oslo. Rasmussen studied rat sexual behavior in a Warden obstruction box, a method which, of course, I dismissed as an expression for American learning theory. I was, instead, assigned a task of my own, namely, to study the estrous cycle in the mouse. These studies gave me the key to my paradise. Each night I went to the small colony room for mice and tested their estrous. cycle.

I was fascinated by what I saw; I felt I was glancing right into Nature itself. Behavioral changes were unfolding before my eyes: estrus followed by anestrus, and this by estrus. The importance of gonadal hormones for the behavior under study was wonderfully demonstrated to me, a complete novice in the study of biology of reproduction. The laboratory situation gave me an example of the importance of environmental factors. When I entered the laboratory before 10 o’clock in the evening in the Spring, when sunset was late, none of the animals was in estrus. One hour later, after sunset, the rats showed full estrus. Thus, the neuroendocrine events determining the behavior were, themselves, adapted to the physical environment.

At last, I felt I had found a solution to my problem of mind and matter. The mouse estrous cycle belonged to the animal’s repertoire of inborn behaviors, a part of the morphological and physiological characteristics of the animal itself, depending on the hormones acting upon the brain and environmental stimuli as well. The estrous cycle was just a window for me, letting me observe a behavior that seemed to be a direct expression of the forces governing the organism. For the first time, I had a tool with which I could continue my search for relationship between behavior and physiology.

Naturally, not all the scientific problems were solved for me. Names like Calvin Stone or Frank Beach were still unknown to me. Reproductive biology was an area of research entirely new to me and nobody could guide me into this literature. The estrous cycle fascinated me, indeed, but here, so I believed, no problems remained and I had to go elsewhere. In this situation, I had the good fortune to meet a French neurologist and physiologist, André Soulairac. He studied masculine sexual behavior in rats and had performed exciting studies on effects of hormones and drugs in sexual behavior. He reported that distinct behavioral traits were related to specific physiological events, i.e., he seemed to have answers to exactly those kinds of questions which I had, in vain, been looking for when reading Hull and Tolman. Soulairac invited me to his laboratory in Paris. I spent the Spring of 1953 in Paris, less confused than I had been four years earlier, learning some elementary skills which I needed.

I then returned to Sweden, obtained permission from the head of the Department of Psychology, John Elmgren, to use part of the cellar in the Psychology Department as a colony room and laboratory, bought some rats from a private rat dealer in the outskirts of Copenhagen, where rats were cheaper than in Stockholm - in Gothenburg such animals were unavailable - and then began to study sexual behavior in rats. My intention was to study the effects of cortical lesions upon masculine sexual behavior, but the months went by and I was confronted with new methodological problems which I felt must be solved before going any further. I studied the influence of environmental factors, like the light/dark periodicity, and the importance of the testing situation, including social grouping. I studied the importance of sexual experience and the interaction of sexual behavior with conditioned responses. I investigated how often I could test each individual rat so that I would not exhaust them sexually. Carefully, I observed the unfolding sexual responses, trying to uncover stimulatory and inhibitory factors determining the appearance of the pattern. Since I had no money to buy new rats, they aged during the course of the experimentation. Thus, a chapter was added, describing age changes in the behavior. After two years, my funds were depleted. I closed the lab, wrote down the results, and sent them to the printer. I entitled the book ”Conditioning and Sexual Behavior”, and soon after I became a Doctor of Philosophy.

It may be proper, at this stage, to give a picture of the research going on in my field in the latter half of the fifties. In the U.S., there were two dominating figures, Frank Beach and William Young. In Europe, nobody, other than Soulairac, worked in this field, as far as I knew. Beach and his students had studied most aspects of reproductive behavior in male and female rodents since the end of the thirties. He had written a timely book on hormones and behavior, and every other month another important contribution left his lab. Young was recognized as the leading expert on the ovarian regulation of the estrous cycle in rodents, problems with which he had been working since the early thirties. Now, in the fifties, he, together with his brilliant students, Gerall, Goy, Phoenix, Valenstein, Riss and others, was deeply engaged in studying the hormonal regulation of sexual behavior, preparing for a major contribution on the hormonal regulation of sexual differentiation. Beach had been working at the Museum of Natural History in New York during the forties, and there a laboratory had been established for the study of reproductive behavior which included, among others, T.C. Schneirla, Lester Aronson, Dan Lehrman, Jay Rosenblatt, and Barry Komisaruk. The study of species-specific behavior analysis as an approach to the study of physiological substrates of behavior was the focus of interest. Schneirla and Lehrman were the central figures in these discussions around inborn and experiential factors determining behavior. In contrast to Lorentz and Tinbergen, they maintained that the manifested behavior was neither an expression for inborn, nor for acquired factors, but rather for an interaction between these both classes of factors, the relative importance of which only being accessible by way of experimental analysis. The studies of the reproductive behavior of the ring dove performed by Dan Lehrman (1955) were viewed as a model for a study of the interaction of environmental and hormonal factors in the behavior.

Having completed my doctoral thesis in 1956, I had to make new decisions about my future. My experimental work was meant to be a contribution to the study of conditioning. As a phenomenon of conditioning, I considered, for instance, the delay in the reversal of the circadian cyclicity occurring after a reversal of the light/dark stimulation. I had studied the interaction between a conditioned operant response and sexual behavior and made some observations of what the ethologist would call displacement effects. In vain, I had tried to condition the enforced interval effect, i.e., the reduction of the number of intromissions to ejaculation produced by experimental prolongation of the inter-intromission intervals in the masculine sexual behavior pattern. I was curious about the relationship between sexual behavior and pain, having noticed that sexual behavior might increase the pain threshold. On the other hand, the neuroendocrine regulation of masculine sexual behavior itself called for a study, as did feminine sexual behavior, apart from its tool to study conditioning. In the journals, studies of the physiological mechanisms of sexual behavior began to appear. Paul MacLean (1959) reported localization of genital functions using electrical stimulation by implanted electrodes, James Olds (1958) reported effects of testosterone on brain self stimulation behavior, and Harris (1955) studies of the brain regulation of the pituitary gland. Sawyer, Everett, and their associates combined morphological, endocrine, neurophysiological, and morphological techniques in studying the mechanisms controlling ovulation in rats and rabbits (Sawyer, 1959).

As I hesitated between these many different ways to continue my research, I received an invitation from Frank Beach to be with him for the year of 1959 at Berkeley. Ron Rabedeau and Dick Whalen were graduate students in Beach’s laboratory and later we were joined by Thomas McGill. I traveled extensively during this year, visiting several laboratories in the United States engaged in physiological behavior research. With initial help from Karl Pribram and Gilbert French, I performed a study of effects of neocortical lesions on the sexual behavior. I returned to Sweden where, in the meantime, I had received new laboratory locations in the Anatomy Department. My hesitation was gone and my intention now was to study the neural regulation of the masculine sexual behavior, using morphological and pharmacological methods.

I was now also ready to take on students. My first student was Ernest Hård. A former school teacher, he was interested in behavior ontogenesis: he observed how the rat mothered her pups, licked them, lactated them, defended them, and warmed them. He chose one of the components: licking. Licking, like mating, was a species-typical behavior, depending upon the bodily needs of liquid and food. It was also a behavior highly sensitive to taste stimuli and greatly dependent upon experience. Like mating, it was a behavior which one should be able to record and quantify, at least in principle. Ernest soon got into difficulties when trying to record suckling in newborn pups, and instead began to study suckling in the adult mother. A method was developed for the microanalysis of the licking behavior. A very important branch of research, concerned with behavior ontogenesis and taste preference behavior, began to grow. In addition to these studies, he and I worked together on the ontogenesis of various behaviors, a subject almost entirely undeveloped at that time. One of our ideas was to establish a time table for the behavioral development which then could be used for studies of teratogenic influences on development.

My second student was Sven Carlsson, a former medical student. He was interested in the problems of arousal and activity levels, problems in fashion at that time, after the discovery of the role of the reticular system in the brain stem. Sven developed a method to study arousal by measuring habituation of the startle response. Unfortunately, he was more attracted to human beings than rats and left us to make a pioneering contribution to problems of psychosomatics.

A third person soon appeared in the laboratory, Lennart Heimer, a medical student and a devoted teacher in neuroanatomy. We immediately became close friends. We designed a stereotaxic instrument of our own, developed a technique for localizing the electrode with X-ray measurements, and Lennart began to work on his own variant of silver impregnation, later called the Fink-Heimer method. Together we explored the brain of the rat for its role in regulating sexual behavior. Our collaboration continued for almost ten years and ended when he left for the United States of America.

During these years, in the early sixties, I met Arvid Carlsson and Nils-Åke Hillarp, and their students: Kjell F...