The Watership Down Behavioral Neuroscience Project

Pavlov, Ivan Petrovich (1849-1936)

D.A. Powell, Ph.D.

Shirley L. Buchanan Neuroscience Laboratory

and

Department of Psychology

University of South Carolina

and

Department of Neuropsychiatry and Behavioral Science

University of South Carolina School of Medicine

Ivan Petrovich Pavlov is recognized as one of the most renowned of Russian scientists and is clearly the best known Russian physiologist of his era. His work on the physiology of the digestive system was well-respected by his colleagues worldwide during his lifetime. This respect earned him the first Nobel prize awarded to a physiologist and the first to a Russian scientist in 1905. Although the excellence of his work on the physiology of the digestive system is well recognized, Pavlov is even better known for his investigations into what he termed conditioned reflexes. This work has had a worldwide impact on the fields of learning and memory, psychology, neuroscience, etc. Pavlov's life can be divided roughly into three phases. The first, including his early years, was a phase in which Pavlov received his early training in physiology and medicine. A second investigational phase, alluded to above, was one in which his work on the physiology of the digestive system was done. The third includes his work, for which he became most famous, on conditioned reflexes.

Pavlov's Early Life

Ivan Petrovich Pavlov was born on September 14, 1849 in the small town of Ryazan, about 100 miles southeast of Moscow. He was the eldest of five children. His father was a priest in one of the poorer parishes. Thus, during Pavlov's early life he lived in extreme poverty. Nevertheless, the life of Pavlov and his siblings was apparently intellectually rich and a love of learning was instilled in each of his children by their father. Pavlov entered the ecclesiastical high school of Ryazan, and from there to the local seminary, obstentially to pursue an ecclesiastical career, as his father and other members of his family had done. Pavlov thus entered school during the Russian cultural revolution of the 1860's and therefore was exposed to the leaders of this revolution, such as Turgeanyev, Doskovsky, Tolstoy, etc. However, he was apparently most heavily influenced by Pisarev, from whom he learned of Darwin's theory of natural selection and the famous Russian physiologist Sechenov, who had just published Reflexes of the Brain in 1863. It is clear that these kinds of influences on Pavlov steered him in the direction of science and consequently he left the ecclesiastical seminary and entered the Mathematics-Physics Department at St. Petersburg State University.

In 1875 Pavlov graduated from the University with a degree in natural sciences. However, due to his interest in physiology he started work as an assistant in the Department of Physiology in the Medical Surgery Academy (now the Military Medical Academy) and in 1879 received a medical diploma. He was then recommended for an appointment with Andre Botkin, who was the most renowned clinician in St. Petersburg at the time. Botkin assigned Pavlov the task of heading his recently established experimental research laboratory. Since Botkin had little interest in experimental work, Pavlov was able to work pretty much independently on problems of his choice. He worked here until 1890. He was heavily influenced by Botkin's theories on the role that the nervous system plays in the regulation of physiological function, and it was here that Pavlov began his studies of the peripheral nerves of the heart and where in 1883 he successfully defended his doctoral dissertation in this area.

During this period of time he also became acquainted with a small circle of friends including another university student, Seraphima Vasilievna, who was in her last year at the Pedagogical Institute. They were married in 1881. During the first years of their married life they lived in extreme poverty. After a first miscarriage, Seraphima gave birth to a son but he also died the next summer. They did, however, later have four children (three boys and a girl) and, based on Seraphima's memoirs published after Pavlov's death, apparently enjoyed a happy family life. In 1883 Pavlov spent two years working abroad in the laboratories of Heidenhain and Ludwig in Germany. On his return to St. Petersburg, he resumed his work in Botkin's laboratory and in 1890 was appointed Professor in the Pharmacology Department at the Military Medical Academy. Five years later he joined the Physiology Department there, which he headed for the rest of his career. He was later also appointed the Head of the Department of Physiology in the newly established Institute of Experimental Medicine. Pavlov worked in his laboratory there until his death at the age of 87 in Leningrad February 27, 1936.

Pavlov's Work on the Digestive System

Pavlov did most of his research on the physiology of digestion during his early years at the Institute for Experimental Medicine. Here he was able to develop his surgical skills with chronic experiments, which he advocated over the acute experiments that were typically done in physiology at that time. Pavlov believed that the study of the entire organism in as normal a state as possible was crucial to understanding physiological systems. Moreover, he was an excellent surgeon and became quite experienced in developing surgical procedures that allowed his dogs to fully recover. In such animals the digestive processes could be studied under normal conditions. As a consequence of this approach to physiology he developed a stomach pouch, which involves isolating a portion of the dog's stomach, so that it can be directly observed by the experimenter. Unlike previous researchers, the nervous input to the isolated portion of the stomach was intact in the Pavlov Pouch. Using this preparation Pavlov could observe the digestive juices and enzymes that occurred as a result of normal food intake, or after direct placement of food into the stomach. It was the comparison of these two states which led to Pavlov's interesting discovery that food placed in the mouth as a normal consequence of eating, produced a significantly larger amount of gastric secretion than when food was placed directly in the stomach. Moreover, when animals were sham fed, viz. when the normal intake of food through the mouth was allowed to take place, but the food was diverted externally, a significant amount of gastric secretion occurred, even though the food never reached the stomach.

It was these types of experiments that led to Pavlov's pioneering discoveries regarding the control of the digestive system by its autonomic nervous input, primarily the vagus nerve. He showed for example that a major consequence of this neural control involves both gastric and pancreatic secretions before any food actually reaches the stomach, by the sight of the food bowl for example, or other stimuli previously associated with eating. These psychic secretions turned out to be of great importance for digestion and led to Pavlov's major conclusions regarding what came to be known as the doctrine of nervism, in which the major tenet states that the physiological control of bodily systems is primarily through its nervous input. This work culminated in the publication of Lectures on The Work of the Digestive Glands in 1897, later translated into English in 1910 (Pavlov, 1910). However, it was during this same period of time that two British physiologists, Wm. Bayliss and E.J. Starling, demonstrated that the secretion of the pancreatic enzymes was primarily due to release of a substance by the intestines during eating, which came to be called secretion. These investigators thus claimed that the doctrine of nervism was invalidated by their discoveries. However, as is typically the case with two opposing theories of biological function, both experimental outcomes were eventually confirmed. The new science of neuroendocrinology thus came to be established, and it is now widely accepted, of course, that nervous control over hormonal output is a ubiquitous aspect of physiological function.

Pavlov's Work on Conditioned Reflexes

As a result of his work on the digestive processes, as noted above, Pavlov also observed that non-food stimuli that became associated with food were able to elicit salivary secretions, and to a lesser extent digestive secretions, even though no food was actually present in the mouth. These psychic secretions came to form the basis for the remainder of Pavlov's work and resulted in his experiments moving in a new direction, which caused an almost complete cessation of work on the digestive system proper. However, Pavlov believed that by studying psychic secretions, which he referred to as conditioned reflexes, he would be able to demonstrate in an objective manner how the brain controls adaptive behaviors. Pavlov developed a salivary fistula, similar to the stomach pouch, in which the release of salivation in the mouth was directed through a tube to a container outside the mouth. Through this technique he was able to discover the amount and kinds of salivary secretions that were produced by different kinds of sensory stimuli.

Using these techniques Pavlov began the study of a new kind of learning, which has come to be known as classical or Pavlovian conditioning. Classical conditioning occurs whenever a neutral stimulus acts as a signal for a forthcoming significant event. Thus, for example, in one of Pavlov's original experiments a pure tone, a metronome, or some other equally neutral stimulus signaled to a dog that it was about to receive an appetitive stimulus, i.e., meat powder (see Pavlov, 1927). In Pavlov's experiments this neutral auditory stimulus was termed the conditioned stimulus (CS) and the meat powder the unconditioned stimulus (US). The US always elicits what Pavlov referred to as an unconditioned response (UR), viz. salivation in response to the meat powder. The behavior in which Pavlov became most interested, however, was not increased salivation in response to the meat powder, which he had previously studied intensively, but the new learned response to the neutral CS. This response also consisted of salivation, but in this case salivation in response to the initial neutral auditory stimulus, which resulted from its consistently preceding the meat powder over many CS/US presentations. This new learned response was referred to as a conditioned response (CR) and was thought to be only temporary and required reinforcement by the US for its maintenance. The US is thus often referred to as a reinforcer, since it reinforces the new response to the CS.

It should be noted that the CR does not, however, always resemble the UR as is the case with the original salivation experiments which Pavlov reported. Indeed often the CR appears to be opposite to the UR. For example, the autonomic changes associated with the contextual cues that signal drug administration, an often-studied type of classical conditioning, are opposite in direction to those produced by the drug itself (Siegel, 1979) and the heart rate CR to CSs that signal aversive USs consist of bradycardia, whereas the UR to these same aversive stimuli alone consists of tachycardia. There are many other experimental operations that have been studied since the time of Pavlov, which produce similar new responses to an original neutral stimulus that is always followed by either a noxious or appetitive event. Pavlov thus developed a new experimental methodology for studying the role of the brain as it initiates new behaviors enabling animals to adapt to their environmental circumstances.

One of Pavlov's greatest contributions to physiology was to emphasize that the nature of the psychic secretions, which were previously thought to be in the realm of psychology, could be objectively studied by physiologists through the conditioned reflex method. He thus believed that the true road to understanding brain function and therefore human behavior was through the objective physiological techniques which he had developed. In fact Pavlov went on to consider a range of higher level functions such as thinking, reading, emotional reactivity, etc. in terms of conditioned reflexes. Using the ideas of cortical excitation and inhibition, which he studied extensively using the conditioned reflex methodology, he was thus able to explain many complicated behavioral phenomena, such as the neuroses and other psychiatric disturbances. Although Pavlov's influence on experimental psychology has been extensive and dramatic, as detailed below, many of the details of his theoretical interpretations have since been found to be lacking. Nevertheless the basic operational procedures for determining the effects of a signal on brain processing has been extremely influential in studying brain function.

Pavlov's Influence on Modern Psychology

During his lifetime and immediately thereafter Pavlov had a tremendous influence on physiology and the study of brain function. Many students were drawn to his laboratory during the early part of the 20th century to study the basic laws governing the activity of the brain, and during this period of time Pavlov received worldwide acclaim and recognition. Pavlov's work was little affected by the Russian Revolution, which was also ongoing during this time. He maintained a skeptical attitude regarding politics and government, but nevertheless his worldwide recognition led the Communists to continue to fund his research at high levels. Thus, the Soviet Union became known for its support of the study of physiology, and it was during this time that a great center for the study of physiology with many distinguished workers was developed in the Soviet Union, primarily under Pavlov's leadership.

It was his influence outside the Soviet Union, however, that resulted in Pavlov's most notable successes in science, primarily in the field of psychology, which Pavlov had previously rejected. Thus the conditioned reflex methodology was instrumental to the development of the behavioristic movement in psychology in the early part of the 20th century. John B. Watson, one of the major pioneers in the development of behaviorism, utilized the conditioned reflex methodology to explain the entire subject field of psychology, which consisted, according to behaviorists, in the study of overt behavior without reference to subjective phenomena such as cognitions, learning, feelings, etc. The publication of Psychology as the Behaviorist Views It in 1913 by Watson thus became instrumental in informing American and English scientists of Pavlov's work. The translation of Pavlov's Conditioned Reflexes by Anrep (1927) made his work available to English speaking scientists. As a result, experimental psychologists began to explore the new conditioned reflex methods for studying behavior at several academic centers in the US. As was noted by Babkin (1949), however, much of the work done by the American researchers focused on skeletal reflexes, as opposed to the visceral reflexes, to which Pavlov and his students had previously devoted most of their work.

One of the basic experiments developed by American psychologists was the classical eyeblink conditioning paradigm. Using this methodology human or animal subjects are presented with a corneal airpuff, which causes reflexive closure of the eyelids. However, when this unconditioned stimulus is preceded by a conditioned stimulus such as a light or pure tone, eventually subjects began to show anticipatory eyeblinks during the conditioned stimulus, which occur even though the corneal airpuff is not presented. This paradigm came to be used extensively in the early 1940's and 50's as behaviorism began to gather momentum. Its success in the hands of the American psychologists led to the de-emphasis on visceral changes as conditioned responses in America. However, Horsley Gantt, who had previously studied with Pavlov, demonstrated in his Johns Hopkins laboratory that both visceral and skeletal responses could be studied in the same organisms, and that the two responses differed greatly in their acquisition and the conditioning parameters required to elicit learning (Gantt, 1960). Much of this early work on classical conditioning was, however, overshadowed by the emphasis given to operant conditioning by other behaviorists, such as B.F. Skinner and Clark Hull. Thus, it was only during the early 1960's that classical conditioning became a popular technique for studying behavior. This was due to the development by I. Gormezano of the classically conditioned nictitating membrane response in the rabbit (Gormezano, 1966). The nictitating membrane is a third laterally-moving eyelid found in the rabbit and some other mammals (e.g., cat). Using this animal preparation Gormezano and his students were able to demonstrate the parametric circumstances under which this kind of learning takes place and what kinds of visceral changes accompany them, e.g., conditioned changes in heart rate, blood pressure, etc. The popularity of this technique became even greater when integrated with the simultaneously developing field of behavioral neuroscience. Classical conditioning offers several advantages for studying concomitant brain function as well as new learned behaviors. For example, concomitant electrophysiological recording from single neurons in specific parts of the brain have led to the discovery that different brain structures are involved in visceral versus skeletal learning (Thompson, 1988). Moreover, more recent brain scanning techniques in humans have demonstrated that even during simple classical eyeblink conditioning activation of several specific areas of the brain, which are known to be involved in learning and memory processes, occurs (e.g., Blaxton et al, 1966).

Thus the use of the conditioned reflex techniques originally developed by Pavlov has come to be one of the major methods used in studying brain-behavior relationships in modern psychology. Pavlov's contribution to this new technology was at a basic level and much of his earlier conclusions regarding the results of his manipulations were, of course, erroneous. However, his contributions we now know were instrumental to the development of modern psychology.

References

Babkin B P (1949). Pavlov: A Biography. University of Chicago Press, Chicago, IL

Blaxton T A, Zeffiro T A, Gabrieli J D E, Bookheimer S Y, Carrillo M C, Theodore W H & Disterhoft J F(1996). Functional mapping of human learning: a positron emission tomography activation study of eyeblink conditioning. J. Neurosci. 16:4032-4040

Gantt W H (1960). Cardiovascular component of the conditional reflex to pain, food, and other stimuli. Physiolog. Rev. 40:266-291

Gormezano I (1966). Classical conditioning. In: Sidowski J B (ed.) Experimental Methods and Instrumentation in Psychology. McGraw Hill, New York, NY

Pavlov I P (1910). Lectures on the Work of the Digestive Glands. (2nd Edition) translated by W H Thompson. Charles Griffin and Co., London, England

Pavlov I P (1927). Conditioned Reflexes translated by G V Anrep. Oxford University Press, London, England

Sechenov I (1935). Selected Works. State Publishing House, Moscow and Leningrad, USSR

Siegel S (1979). The role of conditioning in drug tolerance and addiction. In Keehn J D (ed.) Psychopathology in Animals. Academic Press, New York, NY.

Thompson R F (1991). Are memory traces localized or distributed? Neuropsychologia 29:571-582.

Watson J B (1913). Psychology as the behaviorist views it. Psychol. Rev. 20:158-177