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A theory abandoned but still compelling

Yale Medicine Magazine, 2008 - Autumn

Contents

In Paul MacLean’s triune brain, primitive emotions overruled conscious thoughts.

In 1977 readers were enthralled by The Dragons of Eden, a book by the astronomer Carl Sagan that explored the evolution of the human brain. Dragons won the 1978 Pulitzer Prize for general nonfiction and helped to launch Sagan’s celebrity as a spokesman for science in the 1980s.

The real star of the book, however, was a theory of human neural organization that took root some 30 years earlier in writings by Paul D. MacLean, M.D. ’40. MacLean, who died last December at age 94, was a highly original—some say eccentric—thinker whose model of the triune brain, though now discredited, has had a lasting cultural impact.

“Paul never traveled with the herd,” said Thomas R. Insel, M.D., director of the National Institute of Mental Health, who worked alongside MacLean for 10 years at the Laboratory of Brain Evolution and Behavior in Poolesville, Md. Insel remembers his colleague as irreverent and uninhibited. MacLean once roamed through a room, Insel recalled, feeling the scalps of visiting scientists to ascertain the presence or absence of a skull protuberance he had deemed an important factor in the evolution of human intelligence.

The beginnings of MacLean’s theory appeared in a 1949 paper just as he joined the faculty of the School of Medicine as an assistant professor of physiology with a joint appointment in psychiatry. After conducting electroencephalographic recordings in patients with psychosomatic illnesses and epilepsy at Massachusetts General Hospital, MacLean had become convinced that the emotional components of these disorders were seated in deep brain structures that he called the visceral brain (and renamed the limbic system in 1952), which included the hippocampus, amygdala and cingulate gyrus.

Since all mammals possess variants of these structures, MacLean concluded that they are phylogenetically ancient and that the emotional responses they produce are only weakly regulated by such newer, human structures as the neocortex. “Our affective behavior continues to be dominated by a relatively crude and primitive system,” he wrote. Twenty years later, MacLean rounded out his picture of the triune (three in one) brain by adding what he termed the R-complex (for “reptilian”)—structures in the brain’s core and brain stem that govern basic survival functions—to the neocortical and limbic systems he had defined previously.

The theory saw its fullest expression in MacLean’s 1990 magnum opus, The Triune Brain in Evolution, which was based on wide-ranging anatomical studies of brains in animals as diverse as alligators and monkeys. In its casting of a cognitively sophisticated neocortex unable to fully restrain the primal emotional responses of the limbic system, MacLean’s model was a neuroanatomical cousin to Freud’s tripartite view of the mind, with its warring superego, ego and id. The theory’s conceptual beauty and intuitive appeal lent it enormous staying power; it is still covered in many textbooks and course lectures in biological psychology.

But according to Terrence Deacon, Ph.D., an expert on the evolution of human cognition at the University of California, Berkeley, subsequent research has revealed that MacLean’s basic premise—his “‘hats on top of hats’ view” that brain systems were added by accretion over the course of evolution—was mistaken. “Adding on is almost certainly not the way the brain has evolved,” said Deacon. “Instead, the same structures have become modified in different ways in different lineages.”

Nonetheless, Deacon said, the force of MacLean’s personality gave his ideas a special resonance. “His death represents the passing of an era, because he was really the model of the move towards understanding the brain in evolutionary terms,” said Deacon. “A lot of our contemporary advances ride on top of his work, even though in hindsight it was misleading. That happens a lot in the sciences, and we don’t often give credit to the false starts that really push us along the way.”

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