Concepts and Hypotheses

History of Brain Evolution

Dean Falk

Florida State University

    Historically, the study of brain evolution covers many disciplines and is highlighted by a variety of research techniques.  Brain evolution is a central theme in the study of primate (including evolution, and research in primate neuroanatomy has an important impact on theories pertaining to human brain expansion and evolution. Throughout the history of primate brain evolution, certain trends in neuroanatomical research have been important including cortical mapping studies, comparative neurology, comparative studies of the external neuroanatomy of primate brains, analyses of endo casts and cranial capacities, and quantitative algometric studies.  One of two methodologies  have traditionally  been used to study hominid brain evolution : (1) Comparative neuroanatomy, which is based on the study and comparison of a series of extant primate brains, and (2) Paleoneurology, which emphasizes direct study of endocasts and braincases of fossil hominids.  Modern neuroimaging studies on humans using noninvasive computerized tomography (3D-CT - scans), Positron Emission Tomography (PET), and functional magnetic resonance imaging (fMRI) are enhancing our ability to map thinking human brains (and, to a lesser extent, those of nonhuman primates). Because of these recent advances in medical imaging technology, neuroscientists are better able to understand both structure and function in the brain and how specific cortical areas contribute to certain cognitive activities through participation in complex neural networks.  Happily, paleoneurologists are taking advantage of this "information explosion" by applying recent findings to a reinterpretation of early hominid endocasts.  Regardless of the method of study, one question underlies all studies of hominid brain evolution:  what is it about the human nervous system that makes Homo sapiens  different?  Why is it that a five-year-old human child occasionally asks, "where did I come from?" while the most sophisticated communication initiated by a five-year-old language-trained chimp is on the order of, "me eat, drink more"?  Over the last three million years, the ancestors of humans developed vastly complex linguistic and material cultures which are often attributed to not only bigger brains, but also qualitatively better brains.  But in what ways did this happen? 

    Traditionally, theoretical approaches for assessing hominid brain evolution have fallen into two categories: (1) In the past, efforts were made to identify cerebral "rubicons", such as a "critical mass" of 750 cc (suggested by Author Keith) as the brain size that distinguished hominids from other primates.  (2) Classically brain evolution has been analyzed in terms of "residual" brain factors (encephalization factors) such as Harry Jerison's "extra neurons" that remain after body size factors have been accounted for (allometry).  The search for rubicons, however, has typically been unfruitful and features that distinguish hominid from pongid brains have frequently been shown to be the result of allometry rather than natural selection for qualitatively different brains.  Although these two approaches lend themselves to scientific testing, much of the literature on human brain evolution is speculative - i.e., based on efforts to identify "prime movers" such as hunting or warfare, that theoretically were responsible for the marked increase in both absolute and relative brain size that occurred during hominid evolution.  

    Other topics related to primate neuroanatomy have been fashionable at different times during the past decades. Some of the most famous and insightful mapping experiments occurred during the1930's and 1940's when Walter Penfield and his associates uncovered local cortical areas responsible for specific functions by stimulating specific areas in the brains of surgical patients.  Also in the 1930's and 1940's, numerous descriptions of brains that purportedly represented different human "races" were published. However, these reports ceased in the 1950's when papers discussing the merits of brain size and its relationship to intelligence, culture, sex, and social behavior began to appear.  Although often disdained by the popular press and many researchers, this topic is still prevalent in the literature today.  Similarly, methods for determining encephalization quotients and other indices related to allometry that were published during the1960's are still a central theme in brain evolution research.  The 1970's saw the beginnings of a number of studies on endocasts of fossil nonhuman primates that until that time had only been sporadically described.  The 1970's also saw the beginning of research on cerebral asymmetries in nonhuman primates.  Over the past two decades, new discoveries of numerous fossil hominids have allowed paleoneurologists to address specific questions about the extent of brain reorganization in fossil hominids (i.e., debates about the infamous lunate sulcus). 

    Physical anthropologists and primate neuroanatomists have maintained a keen interest in the brains of fossil hominids throughout the past century.  One of the first major events related to human brain evolution and equally important for hominid paleontology came from Raymond Dart's description of the Taung child in 1925.  Taung is a beautifully preserved  juvenile South African australopithecine specimen composed of a face and an associated natural endocast.  However, although Dart's find was impressive, it was controversial (and still is - for different reasons).  Interest in these studies increased with widespread public attention to the excavations at Choukoutien during the 1930's when publications on endocasts of Sinanthropus  (H. erectus ) became prevalent.  During the 1940's and 1950's, endocasts of other australopithecines were described, and the place these hominids would take among hominoids became a controversial subject.  The same can be said about Homo habilis  in the 1960's.  During the 1970's, no one group of fossil hominids was emphasized over others, but cranial capacities were redetermined for various groups, and speculation continued about the relationship of brain size to taxonomy, intelligence, and culture.

    In general, research in the earlier decades was basically descriptive, with little in the way of sophisticated techniques for quantitative analyses.  However, the 1950's marked a turning point in primate neuroanatomy from the physical anthropologist's point of view.  Much of the earlier descriptive work was summarized in monographs, while certain types of descriptive studies simply ceased.  From the 1950's on, quantitative functional analyses became increasingly important to studies of primate brain evolution.  However, despite the voluminous amount of research in primate neuroanatomy that has transpired during the past century, physical anthropologists are only beginning to provide reasonable hypotheses regarding specific qualitative (i.e., not merely size related) changes in the brain that occurred during primate, including human, evolution.  However, this may largely reflect the fragmentary and crude nature of the paleoneurological evidence.  Although a great deal of work throughout the past decades has been carried out by paleoneurologists, comparative neurology and the advent of advanced medical imaging technology in the neurosciences are becoming increasingly important for the study of primate, including human, brain evolution.  It is to be hoped that, with continued communication between subfields, as well as development of new quantitative approaches for collecting and analyzing data, physical anthropologists' understanding of primate brain evolution will improve and, in turn, provide new hypotheses for future exploration.

• Falk, D. (1980) Hominid Brain Evolution: The Approach From Paleoneurology.  Yrbk of Phsy. Anthro. 23:93-107.

• Falk, D. (1982) Primate Neuroanatomy: An Evolutionary Perspective.  A History of American Physical Anthropology, 1930-1980.

Updating the Radiator Hypothesis

By Dean Falk

Florida State University

During a workout (e.g., while running, doing aerobics, or kickboxing), the face becomes flushed as vessels dilate and perspiration increases and evaporates against the air. This cools the blood in the vessels of the face and in the vast network of tiny veins that riddle the bones of the skull ­ the cranial "radiator" (Fig. 1). As Michel Cabanac and Heiner Brinnel have shown, the radiator kicks-in and delivers cooled blood into the braincase when humans are over-heated (hyperthermic). Such "selective brain cooling" helps maintain the temperature of the brain (which is exquisitely heat-sensitive) within acceptable limits. This is a good thing too, because "it may be that the temperature of the brain is the single most important factor limiting the survival of man and other animals in hot environments" (Mary Ann Baker (1979:136).

Figure 1.  The existence of a vast network of veins that serves to cool the brain in hyperthermic humans was controversial until 1996, when Wolfgang Zenker and Stefan Kubik demonstrated the anatomical basis.  This photograph of the cranial radiator is from their landmark paper (1996:4).

    A few of the larger vessels in the radiator penetrate through recognized holes in the skull -- known as emissary foramina. Well-known examples include the parietal and mastoid emissary veins (Fig. 2), which occur in relatively high frequencies in humans (Hauser & De Stefano, 1989) compared to apes (Falk, 1986;Falk & Gage, 1998). The frequencies of the parietal and mastoid emissary foramina increased dramatically as brain size increased from Australopithecus africanus to Homo sapiens (Fig. 3). If one views the emissary veins that penetrate these foramina as a "window" into the wider network of cranial veins, it appears that the cranial radiator increased in complexity as brain size increased during the course of hominin evolution. According to the radiator hypothesis, evolution of the cranial radiator released a thermal constraint that previously kept brain size within ape ranges. Since larger brains are associated with greater cooling needs, they were selected for in conjunction with elaboration of a vascular mechanism for keeping brain temperature within safe limits. In a sense, the human brain (like the engine of a car) has a radiator that prevents overheating (Falk, 1990).

Figure 2.  The parietal (P) and mastoid (M) emissary veins penetrate the skull through foramina of the same names.  The named emissary veins (there are others) are relatively large compared to the vessels pictured in Fig. 1, but contribute to the same widespread network of veins that participate in selective brain cooling when humans are over-heated.  The named emissary veins also have the advantage of penetrating named foramina that may be scored in the fossilized skulls of our ancestors.

Figure 3.   The frequencies of parietal (green triangles) and mastoid (blue diamonds) emissary foramina (and therefore veins) increased along with cranial capacity (red dots) as hominins evolved from a gracile ancestor that lived some 3.0 million years ago.  The black squares represent frequencies of a specialized route for delivering blood from the cranium (an enlarged occipital/marginal venous sinus) that occurred in robust australopithecines (who are not our ancestors) but is very rare in living humans.

    Selection for bipedalism also entered the evolutionary mix. Because of the constraints that gravity exerts on blood (and other) vessels, altered gravitational (hydrostatic) pressures associated with the refinement of bipedalism in hominins necessitated a rearrangement in cranial blood vessels. (This is not surprising, since vascular plumbing has been tailored to different postural or locomotion patterns during the course of evolution in a variety of animals including snakes and giraffes.) Although gracile (A. africanus) and robust (Paranthropus) australopithecines were both bipedal, their cranial vasculature re-plumbed in different ways relative to the pattern seen in apes. Like A. afarensis ("Lucy’s kind"), blood flowed from the cranium of Paranthropus through several large routes including the well-known accessory or enlarged occipital/marginal (O/M) sinus (Fig. 4). Examination of fossil skulls, however, suggests that these routes were not supplemented by a network of tiny cranial veins like those that began to evolve in A. africanus and, through time, blossomed into the cranial radiator that serves us -- their descendants (Falk, et al., 2000) -- so well in the gymnasium today!

Figure 4.  Posterior views of braincases of (left) humans and (right) robust australopithecines (Paranthropous) and the Hadar early hominins (“A. afarensis”).  In humans, cranial blood flows through the transverse (T)-sigmoid (S) sinuses and then exits the skull through the internal jugular veins.  This route may or may not be present in robust australopithecines (dashed lines), which always manifest enlarged occipital (O)/marginal (M) sinuses on one or both sides of the foramen magnum.   Thus, the O/M system of these hominins is the primary route for draining cranial blood, which may or may not be supplemented by the T/S pathway.  The enlarged O/M system delivers blood to a network of veins surrounding the spinal column.

    What accounts for the different pattern of cranial blood flow that occurred in A. africanus compared to other early hominins in response to altered gravitational pressures associated with bipedalism? Possibly, gracile australopithecines slept in trees at night, and ventured into "mosaic" regions that included open grasslands during the day. Bipedalism would have allowed these little hominins to minimize the amount of body surface that was exposed to overhead sun, thereby reducing heat loads and facilitating adaptation to thermally stressful savanna habitats (Wheeler, 1988). If so, the vasculature of gracile australopithecines became modified in response to gravitational and thermal pressures that were associated with refinement of bipedalism in hot, open habitats. The result was the beginning of a cranial radiator network of veins that could help cool the brain under conditions of intense exercise. More important, once in place, this system was itself modifiable and capable of keeping up with the increasing thermolytic needs of an evolving (enlarging) brain.

    The radiator hypothesis is mechanistic, i.e., it suggests that the dramatic increase in brain size that occurred in Homo was facilitated (rather than directly caused) by the release of thermal constraints that previously kept brain size in check. The radiator network of veins is thus seen as a prime releaser, not a prime mover of human brain evolution (Falk, 1992). One must therefore look elsewhere (Falk et al., 2000) for the behaviors that were selected for once the brain had acquired an adjustable radiator and could get bigger.

References

·         Baker, M. A. 1979. A brain-cooling system in mammals. Sci Am 240:130-139.

·         Cabanac, M. & H. Brinnel 1985. Blood flow in the emissary veins of the human head during hyperthermia. Euro. J. Appl. Physiol. 54:172-176.

• Falk, D. 1986. Evolution of cranial blood drainage in hominids: enlarged occipital/marginal sinuses and emissary foramina. Am. J. Phys. Anthropol. 70:311-324.
• Falk, D. 1990. Brain evolution in Homo: the "radiator" theory (target article, commentaries and response). Behav. Brain Sci. 13:333-381.

·         Falk, D. 1992. Evolution of the Brain and Cognition in Hominids. The sixty-second James Arthur Lecture. New York: The American Museum of Natural History.

·         Falk, D. & T. B. Gage 1998. Radiators are cool: A response to Braga & Boesch’s published paper and reply. J. hum. Evol. 35:307-312.

·         Falk, D., Redmond, J. C., Jr., Guyer, J., Conroy, G. C., Recheis, W., Weber, G. W. and H. Seidler. 2000. Early hominid brain evolution: A new look at old endocasts, J. Hum. Evol., in press.

·         Hauser, G. & G. F. De Stefano 1989. Epigenetic Variants of the Human Skull. Stuttgart: E. Schweizerbartısche Veerlagsbuchhandlung.

·         Wheeler, P. 1988. Stand tall and stay cool. New Sci. 12 (May):62-65.

·         Zenker, W. & S. Kubik 1996. Brain cooling in humans ­anatomical considerations Anat Embryol 193:1-13.

    A progressive enlargement of the hominid brain started about 2 million years ago, probably from a bipedal, australopithecine form with a brain size comparable to that of a modern chimpanzee. Since then, a threefold increase in endocranial volume has taken place, leading to one of the most complex and efficient structures in the animated universe, the human brain. In view of the central importance placed on brain evolution in explaining the success of our species, one may wonder whether there are physical limits that constrain its processing power and evolutionary potential.

    The evolution of the brain in mammals has been accompanied by a reorganization of the brain as a result of differential growth of certain brain regions (Finlay and Darlington, 1995; Rakic, 1995). Consequently, the geometry of the brain has changed notably since the late Cretaceous (Jerison,1990), and particularly in species with large brains, like in humans, the brain has become disproportionately composed of neocortex (Allman, 1990; Northcutt and Kaas, 1995). Analysis of the brain in anthropoid primates revealed that the volume of the neocortex is highly predictable from absolute brain size. The volume of the neocortical gray matter is basically a linear function of brain volume, whereas the mass of interconnections, forming the underlying white matter, increases disproportionaly with brain size. As a result, the volume of gray matter expressed as a percentage of total brain volume is about the same for all anthropoid primates.

    The relative white matter volume, on the other hand, increases with brain size, from 9% in pygmy marmosets (Cebuella pygmaea) to 34% in humans, the highest value in primates. In fact, the evolutionary process of neocorticalization in primates is mainly due to the progressive expansion of the mass of interconnecting nerve fibers, rather than to the increase in the number of cortical neurons (Hofman, 1989; 2000). The high correlation between both variables ensures that the mathematical model, desribing the relationship between brain size and white matter volume, can be used for predictive purposes to estimate the mass of myelinated nerve fibers for a hypothetical primate.

    The model, for example, predicts a white matter volume of about 1470 cm³ for an anthropoid primate with a brain size of 3000 cm³ . In other words, in such a large brained primate, white matter would comprise about half of the entire brain volume, compared to one-third in modern man. Predictions of neocortical growth at different brain sizes, using a conservative scenario, revealed that at a brain size of about 3.5 kg the total volume of the subcortical areas (i.e., cerebellum, brain stem, diencephalon, etc.) reaches a maximum (Fig. 1). Increasing the size of the brain beyond that point, following the same design principle, would lead to a further increase in the size of the neocortex, but to a reduction of the subcortical volume.

Fig. 1. Relative subcortical volume as a function of brain volume. The predicted subcortical volume (i.e. brain volume - predicted neocortex volume) must be zero at zero brain size. Likewise, the subcortical volume will be zero when the brain is exclusively composed of cortical gray and white matter. At a brain size of 3575 cm³ the subcortical volume has a simulated maximum of 366 cm³, which is taken as 100%. The larger the brain grows beyond this critical size the less efficient it will become. Assuming constant design, it follows that this model predicts an upper limit to the brainıs processing power.

 

    Once the brain has grown to a point where the bulk of its mass is in the form of connections, further increases will be unproductive, due the declining capability of neuronal integration and increased conduction time (Ringo et al., 1994; Prothero, 1997; Hofman, 2000). At this point, corresponding to a brain size two to three times that of modern man, the brain reaches its maximal processing power. The larger the brain grows beyond this critical size, the less efficient it will become, thus limiting any improvement in processing power.

    One cannot exclude the possibilty of new structures evolving in the brain, or a higher degree of specialization of existing brain areas, but within the limits of the existing ŒBauplanı there does not seem to be an incremental improvement path available to the human brain. This implies that, as a species, Homo sapiens is nearly at the end of the road for brain evolution.

• Allman, J.M. (1990). Evolution of neocortex. In Cerebral Cortex, Vol. 8A (eds. Jones E.G. & Peters A.) 269-283. Plenum Press, NewYork, N.Y.
• Finlay, B.L. & Darlington, R.B. (1995). Linked regularities in the development and evolution of mammalian brains. Science 268, 1578-1584.
• Hofman, M.A. (1989). On the evolution and geometry of the brain in mammals. Prog. Neurobiol. 32, 137-158.
• Hofman, M.A. (2000). Brain evolution in hominids: are we at the end of the road? In Evolutionary Anatomy of the Primate Cerebral Cortex (eds. Falk, D. & Gibson, K.) Cambridge Univ. Press, in press.
• Jerison, H.J. (1990). Fossil evidence on the evolution of the neocortex. In Cerebral Cortex, Vol. 8A (eds. Jones E.G. & Peters A.) 285-309. Plenum Press, New York, N.Y.
• Northcutt, R.G. & Kaas, J.H. (1995). The emergence and evolution of mammalian cortex. Trends Neurosci. 18, 373-379.
• Prothero, J. (1994). Scaling of cortical neuron density and white matter volume in mammals. J. Brain Res. 38, 513-524.
• Rakic, P. (1995). A small step for the cell, a giant leap to mankind: a hypothesis of neocortical expansion during evolution Trends Neurosci. 18, 383-388.
• Ringo, J.L., Doty, R.W., Demeter, S. & Simard, P.Y. (1994). Time is of essence: a conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cerebral Cortex 4, 331-343.