The evolution of the frontal lobes: a volumetric analysis based on three-dimensional reconstructions of magnetic resonance scans of human and ape brains.

Scenarios regarding the evolution of cognitive function in hominids depend largely on our understanding of the organization of the frontal lobes in extant humans and apes. The frontal lobe is involved in functions such as creative thinking, planning of future actions, decision making, artistic expression, aspects of emotional behavior, as well as working memory, language and motor control. It is often claimed that the frontal lobe is disproportionately larger in humans than in other species, but conflicting reports exist on this issue. The brain of the apes in particular remains largely unknown. In this report we measure the volume of the frontal lobe as a whole and of its main sectors (including cortex and immediately underlying white matter) in living humans, and in post-mortem brains of the chimpanzee, gorilla, orang-utan, gibbon and the macaque using three-dimensional reconstructions of magnetic resonance (MR) scans of the brain. On the basis of these data we suggest that although the absolute volume of the brain and the frontal lobe is largest in humans, the relative size of the frontal lobe is similar across hominoids, and that humans do not have a larger frontal lobe than expected from a primate brain of the human size. We also report that the relative size of the sectors of the frontal lobe (dorsal, mesial, orbital) is similar across the primate species studied. Our conclusions are preliminary, because the size of our sample, although larger than in previous studies, still remains small. With this caveat we conclude that the overall volume of the frontal lobe in hominids enlarged in absolute size along with the rest of the brain, but did not become relatively larger after the split of the human line from the ancestral African hominoid stock. Aspects other than relative volume of the frontal lobe have to be responsible for the cognitive specializations of the hominids.

[1]  G. von Bonin The frontal lobe of primates; cytoarchitectural studies. , 1948, Research publications - Association for Research in Nervous and Mental Disease.

[2]  John C. Russ,et al.  The image processing handbook (3. ed.) , 1995 .

[3]  B. Kushner Descartes' error. , 1998, Journal of AAPOS : the official publication of the American Association for Pediatric Ophthalmology and Strabismus.

[4]  W. Welker Why Does Cerebral Cortex Fissure and Fold , 1990 .

[5]  R. J. Frank,et al.  Three-dimensional in vivo mapping of brain lesions in humans. , 1992, Archives of neurology.

[6]  H. Uylings,et al.  Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. , 1990, Progress in brain research.

[7]  L. V. Van Valen Brain size and intelligence in man. , 1974, American journal of physical anthropology.

[8]  Richard J. Smith Regression models for prediction equations , 1994 .

[9]  H. J. Jerison Brain size and the evolution of mind , 1991 .

[10]  R. Holloway, The evolution of the primate brain: some aspects of quantitative relations. , 1968, Brain research.

[11]  R. Passingham,et al.  Anatomical differences between the neocortex of man and other primates. , 1973, Brain, behavior and evolution.

[12]  G VonBonin,et al.  The frontal lobe of primates; cytoarchitectural studies. , 1948 .

[13]  C. Pantin Problems of Relative Growth , 1932, Nature.

[14]  T. Deacon Human Brain Evolution: II. Embryology and Brain Allometry , 1988 .

[15]  L. Aiello Allometry and the analysis of size and shape in human evolution , 1992 .

[16]  G. E. Smith The Human Brain , 1924, Nature.

[17]  M. Kennard,et al.  FINDINGS AT AUTOPSIES OF SEVENTY ANTHROPOID APES1 , 1941 .

[18]  Andrew Rambaut,et al.  Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data , 1995, Comput. Appl. Biosci..

[19]  D. Hooker JAMES ARTHUR LECTURE ON THE EVOLUTION OF THE HUMAN BRAIN , 1958 .

[20]  Stanley Finger,et al.  Origins of neuroscience: A history of explorations into brain function. , 1994 .

[21]  David Egger,et al.  An Illustrated History of Brain Function , 1974, The Yale Journal of Biology and Medicine.

[22]  C. J. Connolly,et al.  External morphology of the primate brain , 1950 .

[23]  E. J. Field,et al.  Das zentralnervensystem in Zahlen und Tabellen , 1970 .

[24]  Gregor Kjellström The evolution in the brain , 1999, Appl. Math. Comput..

[25]  A. Weil Measurements of cerebral and cerebellar surfaces. Comparative studies of the surfaces of endocranial casts of man, prehistoric men, and anthropoid apes , 1929 .

[26]  Gerhardt von Bonin,et al.  Brain-Weight and Body-Weight of Mammals , 1937 .

[27]  D. Kennedy,et al.  Anatomic segmentation and volumetric calculations in nuclear magnetic resonance imaging. , 1989, IEEE transactions on medical imaging.

[28]  William E. Lorensen,et al.  Marching cubes: A high resolution 3D surface construction algorithm , 1987, SIGGRAPH.

[29]  R. J. A. Berry,et al.  The brain from ape to man , 1931 .

[30]  Warren S. McCulloch,et al.  The isocortex of the chimpanzee. , 1950 .

[31]  John C. Eccles Evolution of the Brain , 1969 .

[32]  H. Frahm,et al.  New and revised data on volumes of brain structures in insectivores and primates. , 1981, Folia primatologica; international journal of primatology.