Papez, James Wenceslas

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PAPEZ, JAMES WENCESLAS

(b. Glencoe, Minnesota, 18 August 1883; d. Columbus, Ohio, 13 April 1958), neuroanatomy, emotion and feeling, limbic system, amygdala, hippocampus, thalamus, cingulated cortex.

Papez was one the greatest twentieth-century explorers of brain anatomy. In an effort to explain emotions in the brain, he proposed the existence of a complex set of circuits. Some of the connections proposed were purely speculative because the techniques available at the time were not capable of revealing the detailed connectivity of the brain. The Papez circuit, as it came to be called, was one of the first examples of a network or systems-level explanation of a complex mental function. His speculations about brain wiring, when evaluated with modern techniques, have turned out to be amazingly accurate. Although his theory of the emotional functions of the circuit turned out to not be correct, it was of great heuristic value and led to much research. All subsequent approaches to the emotional brain build upon the Papez circuit theory.

Early Development James Wenceslas Papez was born in the small town of Glencoe, Minnesota, to an American family of Czech descent. His ancestors were members of the Moravian Church, which was based on the teachings of Jan Huss, a Czech reformer of Christianity accused of heresy and burned at the stake. Their religious tradition, as noted by Paul MacLean, a colleague and a collaborator, might have contributed to Papez’s extreme caution in publicly challenging dominant views. According to MacLean there were occasions when Papez even used to whisper when he was about to question prevailing theories.

After completing his undergraduate education, Papez entered the University of Minnesota College of Medicine and Surgery, where he received his MD in 1911. Under the influence of a comparative neuroanatomist, John Black Johnston, Papez began his training in neuroanatomy. The book on comparative anatomy that Johnston had published in 1906, which was accompanied by beautiful illustrations, was an inspiration for Papez when writing his own text more than two decades later.

In 1912 Papez married (Bessie) Pearl Sowden, an artist, with whom he later had three children: James Pitney, Julia, and Loyd. From 1914 to 1920, Papez served as a faculty member at University of Atlanta (now a part of Emory University). In 1920 he joined the Ithaca Division of Cornell University Medical College as assistant professor of anatomy. Burt Green Wilder, the Cornell professor of zoology and a founder of the famous brain collection named after him, was instrumental in bringing Papez to Cornell.

Time in Ithaca: Theory of Emotions Papez spent the most productive years of his professional career at Cornell. There he conducted comparative studies of brain anatomy, which resulted in numerous publications. His research on the diencephalon (thalamus and hypothalamus), which he carried out with Lester Aronson, his student and collaborator, was especially well received, and even admired, among fellow anatomists. In addition, Papez served as a curator of the Wilder Brain Collection. This collection consisted of numerous human brains, including those of famous people. Many of these brains, including the one of the collection’s founder, were examined by Papez himself.

During his time at Cornell, Papez was very active in teaching courses in anatomy, anthropology, and human development. His celebrated lectures, which revealed his skills as an actor and showman, were loved and admired by students: “Dr. Papez’s clinicoanatomical viewpoint and his unforgettable pantomimes of individuals afflicted with neurological disorders of every conceivable kind had great appeal” (Angevine, 1978, p. 23). However, as one of his younger collaborators noted:

the real excitement came during informal discussions after lectures. In conversation it was almost as important to watch the play of expression of his face as it was to hear his words—his squinting skepticism, his lips pursed in puzzlement. On the few occasions I saw Papez I must have been so intent on listening to his words and trying to catch the meaning of his expression that, in retrospect, I retain only the image of his face and his moving hands. (MacLean, 1978, p. 3)

In 1929 James Papez published his Comparative Neurology. This notable textbook, which was based on his famous lectures and which was accompanied by his wife’s intricate illustrations, served later generations of anatomists for some time. However, the greatest acclaim Papez received was for proposing his neural theory of emotions.

For centuries, it was thought that feelings trigger bodily responses such as shaking, sweating, changes in heart rate, and respiration. This traditional view was questioned in the 1890s by the James-Lange theory. William James in his 1884 paper titled “What Is an Emotion?” suggested a reverse order, namely that feelings arise from the bodily expression of emotions, the commotion in inner organs and in behavior. A similar view was independently formulated in 1885 by a Danish anatomist, Carl G. Lange, who studied physiological responses accompanying emotions. The James-Lange “peripheral” theory of emotions, while appealing to many psychologists, was not supported by much experimental data. On the contrary, anatomical and clinical findings were suggesting the opposite. Observations of patients with severed spinal cord, as well as experiments on animals with disrupted major sensory pathways, indicated the presence of emotional reactions despite the apparent disconnection between the brain and periphery. Such findings led to severe criticism of the James-Lange theory. Among the critics were Walter B. Cannon and Charles L. Dana.

Cannon in particular proposed that the James-Lange theory could not be correct because bodily responses, especially of the autonomic nervous system, would be too slow and would lack the specificity needed to distinguish fear from anger from joy and so on. From his own research with Philip Bard, Cannon proposed that the hypothalamus plays a key role in emotions. It receives sensory information about external stimuli and then sends signals to the body to control emotional responses and sends signals to the cortex to define feelings. Another line of argument against the James-Lange theory came from Dana, a neurologist who based on his observations of the symptoms accompanying brain damage in humans, emphasizing the importance of the cortex itself, as opposed to body feedback to the cortex, in generating conscious feelings.

Although Papez never did research on emotions, he was fascinated with the topic and was aware of Cannon’s critique of the James-Lange theory as well as of the Cannon-Bard alternative. Rumor has it that when Papez learned that a prominent private foundation in the United States had donated a large sum of money to a British laboratory for the purpose of studying the nature of emotions, Papez became annoyed: “I was mad, because the English proposal seemed to ignore what was already known about this subject” (quoted in MacLean, 1978, p.5). In particular, it seemed to ignore the research that had been done in the United States. In a fit of national pride, Papez wrote, in few days, his famous paper “A Proposed Mechanism of Emotion,” which was published in Archives of Neurology and Psychiatry in 1937.

This influential review article largely was a product of speculative thinking. He took the classic findings about brain organization and function from animal research by Cannon, Bard, C. Judson Herrick, and others, and synthesized them with observations about the consequences of brain damage in humans. The result was a proposal about the organization of neural circuitry involved in emotional processing, starting at the point of sensory input up to the level of subjective feeling. According to Papez, this plausible emotional circuit involved sensory areas of the thalamus and cortex, the hypothalamus, anterior thalamus, cingulate cortex, hippocampus, and mammillary bodies.

Why did he include these brain regions? Some were included because of experimental findings. The hypothalamus was on his list because of Bard’s research in Cannon’s laboratory at Harvard, which showed that the hypothalamus was essential for the expression of emotional responses. The sensory thalamus was included for two reasons. First, the standard view held that the sensory thalamus transfers information to the cortex for perception, thought, and memory. But Cannon had noted that sensory pathways diverge in the thalamus, with a second component going directly to the hypothalamus. This component was viewed as important in activating the emotional functions of the hypothalamus. The key area of the hypothalamus was thought to be the mammillary bodies (breastlike protrusions at the ventral part of the brain). These were pinpointed in part because Papez knew about a report of monkeys with damage in the area. The behavior of these animals was characterized by a lack of emotional responsiveness. The anterior thalamus was included because it connected the mammillary bodies to the cingulate cortex.

The cingulate cortex, a region located in the medial wall of the brain, had a long and interesting history in studies of the brain. The great French anatomist Pierre-Paul Broca had in the nineteenth century named this area the limbic cortex, because a significant part of it is situated at the edge dividing the medial and the dorsal parts of each hemisphere (in Latin, limbus means “rim” or “edge”). Herrick, an anatomist who specialized in brain evolution and who was working during the same period as Papez, distinguished between the medial and the lateral cortices. Herrick proposed that the medial cortex, which in lower animals is responsible for processing olfactory information, in the course of evolution gave rise to the lateral cortex, a part of the brain that subserves higher intellectual functions. Papez utilized Herrick’s distinction, as well as clinical observations reporting that brain tumors compressing limbic cortex, as well as occlusion of arteries supplying this region, were accompanied by several emotional disturbances, such as easy irritability, euphoria, and depression.

Finally, the hippocampus, a structure sitting mostly inside the medial temporal lobe, was justified by observations of people suffering from rabies. Papez observed that negri bodies, microscopic changes in the brain tissue which accompany rabies, are localized mainly in the hippocampus. He linked these anatomical findings to the clinical picture of rabies, which involves enhanced repsonsiveness to various stimuli, irritability, and sleeplessness, as well as intense emotions, such as fear and rage. Based on this evidence, Papez hypothesized that the hippocampus plays a crucial role in the production of emotional states (1995, p. 107).

Putting all this information together, Papez proposed three streams of processing that start with the receptor organs and then split at the level of the thalamus into the “stream of movement,” the “stream of thought,” and the “stream of feeling.” The stream of movement projects to the subcortical areas involved in movement control; the stream of thought conducts information from the thalamus to the lateral cerebral cortex and allows sensations to be transformed into perceptions, thoughts, and memories. The stream of feeling transmits sensory information from the ventral thalamus directly to the hypothalamus. Based on available anatomical data, Papez hypothesized that a part of the hypothalamus-mammillary bodies receives the thalamic projections and connects to the cingulate cortex via the anterior thalamus. Thus, the cingulate cortex may be excited either directly by the sensory pathways coming through the hypothalamus or by interconnections with the lateral cortex.

Papez proposed that the cingulate cortex is the site where emotions are experienced. This happens when the impulses coming from the hypothalamus reach the cingulate cortex. In turn, widespread projections from the cingulate cortex to other cortical regions add emotional coloring to various psychological processes. This may explain, thought Papez, two ways, in which emotions arise:(1) a consequence of hypothalamic stimulation and/or (2) a result of mental activity (1995, pp. 104–105).

Papez posited that the cingulate cortex influences emotional processing in the hypothalamus through its outputs to the hippocampus, which via the fornix sends messages to the posterior region of hypothalamus, thus completing the circle of emotion. In Papez’s model, the key role in emotions was assigned to the hippocampus.

The hippocampus and the associated areas were supposed to be a place where original emotive processes arise, and from where they are transferred for further processing to the mammillary bodies, the anterior thalamic nuclei, and the cingulate cortex (1995, p. 104).

Papez’s paper did not receive much interest until 1949, when Paul MacClean published his article revising the organization of emotional circuits proposed by the anatomist from Cornell. Interestingly, even if not yet identified at the time, most of the pathways that Papez posited do exist. Unfortunately, the hippocampus and

other components of Papez’s circuit appear to have very little involvement in emotion. If Papez had waited a bit, he would have learned about the findings of Heinrich Klüver and Paul Bucy from the University of Chicago. In 1939 Klüver and Paul published their observations of emotional changes in monkeys following lesions of the temporal lobe. Later studies by Lawrence Weiskrantz in 1956 showed that the amygdala was the culprit. While for Papez, the amygdala was merely playing an unspecified role in visceral and gustatory functions, the new findings demonstrated a crucial role of this structure in emotions.

Papez never specified what he meant by “emotion.” He was an anatomist, not a psychologist. Emotion, for him, was a tool for thinking about how brain pathways are organized. His very specific suggestion led to much research on both the connections involved and their role in emotion. Though his ideas concerning their role in emotion have not held up, his speculations about connection were remarkably accurate. Papez was aware of the limitations of his emotional hypothesis: “The new interpretation which I propose can be supported by much more data at present available in the literature, but it is evident that any such doctrine will have to stand the test of experimental and clinical experience if it is to be useful in science” (1995, p. 111).

Even if his emotional model did not stand the scrutiny of empirical verification, the conceptual framework of his theory is still commonly applied. Papez’s intuitions that brain structures are anatomically and functionally interrelated, such that a disturbance in one area also affects other brain regions became a common way of thinking in neuroscience. The metaphors “stream of thought,” “stream of movement,” “stream of feeling,” or “emotional coloring,” originally introduced by the neuroanatomy professor, took on a life of their own (Neylan, 1995, p. 102).

After the Cornell Medical School moved from Ithaca to New York City in the 1940s, Papez remained on the Ithaca campus as professor of anatomy in the Department of Zoology. He began to spend more time on other interests: anthropology and development. However, in 1941, he published another remarkable article, a synthesis of his observations on the basal ganglia and their connections. In this review, Papez described neural pathways linking basal ganglia with each other and with other brain areas.

Late Work and Retirement In 1951, after thirty-one years at Cornell, Papez retired and left Ithaca. He and Pearl moved to Ohio to take the position of director of the newly established Laboratory for Biological Research in the Department of Mental Hygiene and Corrections at the Columbus State Hospital. He was involved there in studying slowly developing degenerative changes in the brains of people suffering from chronic neurological and psychiatric disorders. He developed a special method to detect inclusion-like bodies.

He collaborated, as during his entire career, with Pearl, who did the drawings of changes observed using the microscope. Papez’s findings led him to suspect that the changes had been caused by viruses or other microbial organisms. However, neuropathologists who used conventional methods of staining strongly rejected Papez’s hypothesis. His research was considered controversial, and Papez was even very close to losing his job. Yet, it is possible that Papez might have been partially correct; a few decades later, stronger evidence was presented to support the hypothesis of parasitic causation of degenerative changes in the brain.

During his time in Ohio, Papez dedicated himself to his other passion: poetry. In 1957 he published his volume of poems Fragments of Verse. One of the poems, “My Girl on Broad Street,” describes his loneliness at their house on Broad Street, while Pearl was away:

It’s Pearl, my girl on Broad Street

That I miss.

(MacLean, 1978, p. 7)

On Sunday, 13 April 1958, while having breakfast with his wife, Papez felt sudden chest pain. He said, “This is it,” and went to lie down on the couch. Soon after, he died. James Wenceslas Papez was one of greatest anatomists of the twentieth century, but he was also remembered as a husband, father, scholar, and poet.

BIBLIOGRAPHY

For the collection of James Wenceslas Papez’s papers, contact: Archives and Modern Manuscripts Program, History of Medicine Division, U.S. National Library of Medicine, 8600 Rockville Pike, Bethesda, MD 20894; http://www.nlm.nih.gov/hmd/manuscripts/ead/papez.html.

WORKS BY PAPEZ

“Reticulo-Spinal Tracts in the Cat: Marchi Method.” Journal of Comparative Neurology 41 (1926): 365–399. “The Brain of Helen H. Gardner (Alice Chenoweth Day).”

American Journal of Physical Anthropology 11 (1927): 29–79. “Subdivisions of the Facial Nucleus.” Journal of Comparative

Neurology 43 (1927): 159–191. “The Brain of Burt Green Wilder (1841–1925).” Journal of Comparative Neurology 47 (1929): 285–341.

Comparative Neurology. New York: Thomas Y. Crowell, 1929. “The Brain of Sutherland Simpson, 1863–1926.” Journal of

Comparative Neurology 51 (1930): 165–196. “The Thalamic Nuclei of the Nine-Banded Armadillo (Tatusia novemcincta).” Journal of Comparative Neurology 56 (1932): 49–103.

With Lester R. Aronson. “Thalamic Nuclei of Pithecus (Macacus) Rhesus I. Ventral Thalamus.” Archives of Neurology and Psychiatry 32 (1934): 1–26.———. “Thalamic Nuclei of Pithecus (Macacus) Rhesus II.

Dorsal Thalamus.” Archives of Neurology and Psychiatry 32 (1934): 27–44. “Thalamus of Turtles and Thalamic Evolution.” Journal of

Comparative Neurology 61 (1935): 433–475. “Evolution of the Medial Geniculate Body.” Journal of

Comparative Neurology 64 (1936): 41–61. “A Proposed Mechanism of Emotion.” Archives of Neurology and

Psychiatry 38 (1937): 725–743. This work was reprinted by the Journal of Neuropsychiatry and Clinical Neurosciences 7 (1995): 103–112. “Connections of the Pulvinar.” Archives of Neurology and

Psychiatry 41 (1939): 277–289. “A Summary of Fiber Connections of the Basal Ganglia with

Each Other and with Other Portions of the Brain.” Research Publications, the Association for Research in Nervous and Mental Disease 21 (1941): 21–68. “Neuronal Disease Associated with Intracytoplasmic Inclusion

Bodies.” Archives of Neurology and Psychiatry 52 (1944): 217–229. “Fiber Tracts of the Amygdaloid Region in the Human Brain, from a Graphic Reconstruction of Fiber Connections and Nuclear Masses.” Anatomical Record 91 (1945): 294.

With J. F. Bateman. “Cytological Changes in Nerve Cells in Dementia Preacox.” Journal of Nervous and Mental Disease 110 (1949): 425–437. “Changes in Nerve Cells and Hypophysis in Old Psychotic

Patients: A Review of 90 Cases.” Journal of Gerontology 9 (1954): 363.

Fragments of Verse. Los Angeles: New Age Publishing, 1957. With Pearl Papez. “Mycotic Nature of Brain-Damage in Mental

Deficiency.” American Journal of Psychology 70 (1957): 333–346. “Visceral Brain, Its Component Parts and Their Connections.” Journal of Nervous and Mental Disease 126 (1958): 40–56.

OTHER SOURCES

Angevine, Jay B., Jr. “Embryogenesis and Phylogenesis in the Limbic System.” In Limbic Mechanisms: The Continuing Evolution of the Limbic System Concept, edited by Kenneth E. Livingston and Oleh Hornykiewicz. New York and London: Plenum Press, 1978.

Finger, Stanley. “Defining and Controlling the Circuits of Emotion.” In Origins of Neuroscience: A History of Explorations into Brain Function. New York and Oxford: Oxford University Press, 1994.

Haymaker, Webb, and Francis Schiller. The Founders of Neurology. Springfield, IL: Charles C. Thomas, 1970. LeDoux, Joseph E. Emotional Brain:The Mysterious

Underpinnings of Emotional Life. New York: Simon & Schuster, 1996. See especially Chapter 4, “The Holy Grail.” MacLean, Paul D. “Challenges to the Papez Heritage.” In Limbic Mechanisms: The Continuing Evolution of the Limbic System Concept, edited by K. E. Livingston and O. Hornykiewicz. New York and London: Plenum Press, 1978.

Mettler, Fred. “James Wenceslas Papez: August 18, 1883–April 13, 1958.” Anatomical Record (1958): 279–282.

Neylan, Thomas C. “Classic Articles in Neuropsychiatry: Introduction to the Series.” Journal of Neuropsychiatry and Clinical Neurosciences 7 (1995): 102–103.

Yakovlev, Paul I. (as told to Ken Livingston).“Recollections of James Papez and Comments on the Evolution of the Limbic System Concept.” In Limbic Mechanisms: The Continuing Evolution of the Limbic System Concept, edited by K. E. Livingston and O. Hornykiewicz. New York and London: Plenum Press, 1978.

Jacek D biec
Joseph E. LeDoux

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