Thursday, April 01, 1999

New Brains from Old Genes

Evolving Brains

By: Melvyn A. Goodale Ph.D.

 rev_v1n1goodale_2

Nature uses only the longest threads to weave her patterns, so each small piece of her fabric reveals the organization of the entire tapestry.

—Richard Feynman

Richard Feynman’s metaphor is particularly apt when applied to John Morgan Allman’s marvelous new book, Evolving Brains. Allman, a professor of psychobiology at the California Institute of Technology, gives an account of the origins of the human brain that emphasizes the startling continuity in the development of nervous systems from the fruit fly to us, despite the obvious discontinuities in behavior. He shows how small changes in one part of the fabric of nature, the genetic code, can give rise to far-reaching changes in the behavior of organisms—and how that behavior is represented in neural tissue. Feynman’s metaphor applies in a broader sense as well; Evolving Brains weaves its story about the origin of the human brain (and human nature) with strands of argument running through disciplines from molecular genetics to psychology.

Although Allman covers topics from developmental genetics to evolutionary biology, and tackles some of the most arcane issues in neuroscience, his straightforward prose and engaging style make the ideas come alive for the lay reader. Another delight of Evolving Brains is its illustrations. Like so many books in the Scientific American Library series, this one is lavish with full-color drawings, photographs, and diagrams that illuminate its ideas. Most of the drawings are by Joyce Powzyk, a gifted artist with a deep appreciation of brain structure and animal behavior. Her drawings are superb.

WHY DO BRAINS DIFFER?

Allman poses a deceptively simple question: “Given that organisms share a common ancestry, why is it that they differ so greatly in their capacities to sense, remember, and respond to the world around them?”  The answer, he argues, “depends crucially on understanding how brains have evolved.” He then offers a basic introduction to the brain and neurons but, happily, not through your obligatory “How Neurons Work” section. Instead, he explores fundamental questions about why organisms might need a brain and why neurons are needed to control the flow of information within the bodies of multicellular animals.

These are not questions always addressed by other authors, who prefer to plod on with yet another explanation of action potentials.

Chapter 2 is a lucid account of how similarities and differences in animal brains, at both the level of gross anatomy and synaptic transmission, reflect similarities and differences in ecology and lifestyle. Take the example of the raccoon and its close relative the coatimundi. Both have highly developed areas in their cortex for somatosensory awareness, reflecting their use of tactile information to probe the environment in search of food. But, as Allman points out, there are clear differences between them in how different body parts are represented in the somatosensory cortex. The raccoon, who relies on the fine sensitivity of its forepaws to detect crayfish and other prey, has an enormous representation of its forepaws in its somatosensory cortex. The coatimundi, who uses its sensitive snout to find food, has a huge representation of that part of its anatomy in its somatosensory cortex.

It is chapter 3, however, that sets Evolving Brains apart from conventional texts on brain evolution. Here Allman offers a primer on modern ideas of genetics, showing how gene duplication can regulate the production of brain segments and mediate the emergence of new brain structures. He introduces the idea of primordial homeotic genes (from the Greek homoios, “like”) that control the development of animals ranging from sea urchins to human beings. Homeotic genes have been duplicated many times during evolution and now control development of different segments of the body and brain. This brief chapter is packed with provocative, exciting ideas that will be new to many behavioral neuroscientists as well as to lay readers.

One of these ideas, to which Allman refers throughout the book, is that development of the brain is tightly coupled with development of the gut, and that this has been so for more than half a billion years (perhaps because of the brain’s pivotal role in controlling what gets into the gut). All-man reminds us that genes controlling development of the brain and gut in fruit flies have mammalian counterparts, expressed in development of the forebrain and in ectodermal tissues that become organs such as the liver, lungs, and intestines.

A WALK THROUGH EVOLUTION

In chapters 4 through 6, Allman takes us through evolution of brains from simple, early animals to modern primates. He moves easily from details of neural connectivity to speculation about the ecological scenarios that might have shaped the structure and function of the brain in different creatures. Along the way, he explores some controversial ideas put forward to account for differences between the brains of different groups of animals. Two of these are Jack Pettigrew’s “flying primate” hypothesis (which Allman abruptly brings down to earth) and Caleb Finch’s notion of “programmed senescence” (for which Allman provides supporting arguments).

Allman also analyzes the costs and benefits of new adaptations to explain some paradoxes in the evolution of coping strategies. For example, the emergence of temperature regulation, or homeostasis, in early mammals came with a cost. Although they became independent of the temperature of their immediate environment, early warm-blooded mammals probably did not live as long as their cold-blooded ancestors. Their short life span, Allman suggests, “was probably related to the very high energy costs of temperature homeostasis in a small animal.” With its large body surface relative to its body size, the small mammal would have a hard time keeping its body temperature up. It would have to eat more to generate enough energy to offset heat loss. Thus early mammals “were at great risk of starvation, which was the price of being able to function independently of variations in environmental temperature.” As we learn later in the book, however, humans escaped this “painful trade-off” between warm blood and long life by developing large brains able to exploit far more options in their environment.

Allman also revisits the emergence of binocular vision in primates: why our eyes and the eyes of our monkey relatives face forward rather than to the side, as in animals such as squirrels, deer, and horses. Again he points out the costs and benefits. Front-facing eyes may have given our primate ancestors big advantages in detecting prey and grasping fine branches in the treetops, but severely limited their ability to detect predators approaching from the side or the rear. (One solution may have been to form social groups, so we could watch each other’s backs.)

Many of Allman’s examples are drawn from work on the visual system, reflecting his own important research. He is known for studies of primates that charted areas lying beyond the primary visual cortex and for electrophysiological work on the visual properties of neurons. Most recently he has shown how high-order cortical areas handle information about the size of objects over different viewing distances, a prerequisite for “object constancy”(or experiencing the same object at different viewing distances as equivalent). With Jon Kaas, he has theorized how differences in the layout of the brain’s visual areas may be governed by the need to minimize “wire” length in the nervous system.

SMALL CHANGES, BIG EFFECTS

Time and time again in Evolving Brains, Allman shows how small changes in structure can have big effects on the performance of brains and the behavior they control. A case in point is the octopus. As Allman points out, the octopus is a pretty “brainy” mollusk, one with a ratio of brain to body size on a par with that of some mammals. The big brain and elaborate eye of the octopus, along with its efficient motor and respiratory system, no doubt emerged because its ancestors were predators who had to detect, pursue, and capture fast-moving prey. But although the first cephalopods, the group to which the octopus belongs, appear in the fossil record of the late Cambrian Period, some 500 million years ago, their brains and nervous systems have never evolved as have those of vertebrates. Why?

Allman suggests two critical differences between cephalopods and jawed vertebrates that enabled vertebrates to pull ahead and, at the same time, limited the cephalopod brain. First, the cephalopods never developed an insulating material like myelin, which enables axons in the vertebrate nervous system to conduct information rapidly from one part of the body to another. Without insulation, the only way for the cephalopod to improve its rate of conduction was to have larger axons—a serious constraint, since much space and energy would have to be devoted to them. The large size of the cephalopod axons may have enabled scientists like A. L. Hodgkin and Andrew Huxley to discover the action potential, but in nature these huge cables were no match for the smaller, myelin-insulated axons of the jawed fishes.

Second, the green blood of the cephalopod, which uses a copper-based protein, hemocyanin, to transport oxygen, is no match for the red blood of the vertebrate, which uses iron-based hemoglobin. Hemocyanin can transport only one quarter of the oxygen that can be transported by hemoglobin. Gram for gram, red-blooded vertebrates simply have more oxygen available to support their activity; they can do far more with far less than can the cephalopod.

DO BIG BRAINS MAKE LONG LIVES?

Allman saves his most provocative ideas for his final chapter. (One senses that this may have been the chapter he most enjoyed writing.) Here he explores the big question: Why do humans have such large brains compared to other primates? In answering it, he probes the relationship between big brains and longevity, and thus, by implication, the relationship between big brains and life experiences. Much of the work he reports is his own. His inspiration to delve into this question apparently was a picture on the cover of Science in 1982, showing Bobo, a capuchin monkey, thought at the time to be the oldest living monkey in captivity.

Bobo, who eventually died at age 54, was certainly an old monkey, but All-man soon discovered from conversations with his primatologist colleagues that such longevity was not unusual even in wild capuchins. He knew, too, that capuchins are intelligent, highly social animals whose brains relative to their body size are actually bigger than those of the larger macaque monkeys, whose lives are significantly shorter. Could there be a relationship between brain size and longevity?

To find out, Allman and his colleagues spent years poring over life-span records of primates in zoos around the world. The hard work paid off. They demonstrated a surprisingly strong relationship between the two variables: the longer a species lived, the bigger its brain. (In telling this story, Allman emphasizes that we must look at relative longevity and relative brain size, since almost all smaller species live shorter lives than larger species.) Allman then uses the relationship between longevity and brain size to discuss how variables—including diet, longevity, the size of the birth canal, social structure, parenting, and gender— can influence brain size and organization.

Many of Allman’s ideas seem consistent with those of Owen Lovejoy, a paleoanthropologist who argues that a range of selection variables, from bipedalism to romantic love, reinforced one another in shaping our evolution. This multiple bootstrapping by forces of natural selection eventually led to emergence of the human way of life and our ascendance as the ruling species on the planet. But Allman adds another factor to the mix, one that many will find surprising. He suggests that when early humans first encountered wolves 140,000 years ago, after leaving Africa, they formed a bond that gave both species an enormous advantage over other predators, including other early human species

Wolves, like humans, live in extended families where both males and females care for the young. Both species are held together in groups by strong social bonds maintained through communal vocalizations and elaborate social rituals. Wolves and early humans were both highly successful predators who used intelligence and cooperative hunting to bring down prey much larger than themselves. Allman suggests that this common heritage of social bonding in humans and wolves permitted domestication. Wolf pups could bond with humans. Their social intelligence enabled them to become part of the extended family of the early human nomads. Individuals in both species benefited from this arrangement. Indeed, Allman points out, so successful was this partnership that it may have been responsible for eventual displacement, by the ancestors of modern humans that emerged from Africa, not only of the relic populations of Homo erectus living in the rain forests of southeast Asia but also of the ancestors of Neanderthals living in the colder climes of Europe and western Asia.

But there is a price to pay for domestication. Dogs have brains about two-thirds the size of wolf brains, even when adjusted for body size—perhaps in part because domestic dogs, living with caretaking humans, are buffered against the vicissitudes of natural selection. In the last paragraph of Evolving Brains, Allman adds that the human brain, too, is smaller than it was some 35,000 years ago. He wonders if the change from a nomadic to an agrarian existence buffered us, too, against forces of natural selection. This is all quite speculative, of course, as Allman readily acknowledges, but it is a fitting tale with which to end the book, weaving the disciplines of comparative neuroanatomy, development, and evolutionary biology into a wonderful synthesis.

THROUGH ANTHROPOLOGY TO THE BRAIN

This synthesis sets Evolving Brains apart from other books on evolution of the brain. Earlier books concentrated on the details of comparative neuroanatomy—giving short shrift to evolutionary biology and behavior—or speculated wildly on the behavior of our primate ancestors without relating these behavior patterns to functional organization of our brains today. In other words, we have had to choose between dry-as-dust anatomy texts and “just so” stories.

The absence of any sensible discussion of evolution in many earlier texts is perhaps not that surprising. Neuroscience, particularly “systems” neuroscience, has tended to ignore evolutionary biology. In this respect, neuroscience is not so different from classical physiology (one of its founding disciplines, after all), which historically grew out of medicine, not biology. Unlike the biological sciences, physiology did not look to natural selection to explain its disparate observations; its approach—a highly successful one—was determinedly mechanistic. Physiologists made great progress in understanding the complexities of human physiology but spent little time pondering the origins of those complexities. This became the legacy of most systems-level neuroscientists, who constructed their theories without much thought about the origins of the brain through natural selection.

The difference is that John Morgan Allman came to neuroscience not via physiology or psychology (two popular routes) but through physical anthropology, where natural selection is a unifying principle. Thus, when Allman went off to a physiology laboratory to pursue his interests in brain evolution, he had an appreciation of the explanatory power of natural selection—and a mind open to new developments in genetics and evolutionary biology. This is evident not only in his distinguished career in neuroscience but also in Evolving Brains.

The reader will have gathered that I am enthusiastic about this book. Allman has written an account of brain evolution that is both scholarly and accessible to lay readers. Evolving Brains has set a high bar for those to come whose topic is the origins of that most remarkable of organs.

EXCERPT

From Evolving Brains by John Morgan Allman. © 1999 by W. H. Freeman and Company. Used with permission.

Building on the Past

In 1971, when we contemplated the emerging evidence that there were many cortical maps, Jon Kaas and I suggested that evolution of cortical areas proceeded by replication of pre-existing areas. We were inspired by the paleontologist William King Gregory, who in 1935 suggested that a major mechanism in evolution has been the replication of body parts due to genetic mutation in a single generation that was then followed in subsequent generations by the gradual divergence of structure and functions of the duplicated parts.

Why are separate cortical areas maintained in evolution? One reason for the retention of older mechanisms occurred to me during a visit to an electrical power-generation plant belonging to a public utility. The plant had been in operation for many decades, and I noticed that there were numerous systems for controlling the generators. There was an array of pneumatic controls, an intricate maze of tiny tubes that opened and closed various valves; there was a system of controls based on vacuum tube technology; and there were several generations of computer-based control systems. All these systems were being used to control processes at the plant. When I asked why the older control systems were still in use, I was told that the demand for the continuous generation of power was too great to allow the plant to be shut down for the complete renovation that would be required to shift to the most up-to-date computer-based control system, and thus there had been a progressive overlay of control technologies, the pneumatic, vacuum tube, and computer systems integrated into one functional system for the generation of electrical power.

I realized that the brain has evolved in the same manner as the control systems in this power plant. The brain, like the power plant, can never be shut down and fundamentally reconfigured, even between generations. All the old control systems must remain in place, and new ones with additional capacities are added on and integrated in such a way as to enhance survival. In biological evolution, genetic mutations produce new cortical areas that are like new control systems in the power plant, while the old areas continue to perform their basic functions necessary for the survival of the animal just as the older control systems continue to sustain some of the basic functions of the power plant.



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Scientific Advisory Board
Joseph T. Coyle, M.D., Harvard Medical School
Kay Redfield Jamison, Ph.D., The Johns Hopkins University School of Medicine
Pierre J. Magistretti, M.D., Ph.D., University of Lausanne Medical School and Hospital
Robert Malenka, M.D., Ph.D., Stanford University School of Medicine
Bruce S. McEwen, Ph.D., The Rockefeller University
Donald Price, M.D., The Johns Hopkins University School of Medicine

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