How and why humans grow thin skulls: Experimental evidence for systemic cortical robusticity

American Journal of Physical Anthropology

Volumn 101, Issue 2, 1996, Pages 217-236

  Lieberman, Daniel E ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Armadillos; Cortical bone; Homo; Neurocranium; Pigs; Robusticity; Skull

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARMADILLO; ARTICLE; BONE GROWTH; BONE MATURATION; CORTICAL BONE; EXERCISE; FEMALE; HUMAN; HUMAN TISSUE; MALE; NONHUMAN; SKULL; SWINE;

ANIMALS; ARMADILLOS; BONE DEVELOPMENT; EXERCISE; FEMALE; FOSSILS; HUMANS; MALE; SKULL; SPECIES SPECIFICITY; SWINE; SWINE, MINIATURE;

EID: 0029758901     PISSN: 00029483     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-8644(199610)101:2<217::AID-AJPA7>3.0.CO;2-Z     Document Type: Article

References (111)

1. Adeloye A, Kattan K, and Silverman FN (1975) Thickness of the normal skull in the American blacks and whites. Am. J. Phys. Anthropol. 43:23-30.
2. Armstrong PF (1988) Cell kinetics and control of physeal growth. In HK Uhthoff and JK Wiley (eds.): Behavior of the Growth Plate. New York: Raven Press, pp. 233-236.
3. Beaupré GS, Orr TE, and Carter DR (1990) An approach for time-dependent modeling and remodeling-theoretical development. J. Orthop. Res. 8:651-661.
4. Behrents RG, Carlson DS, and Abdelnour T (1978) In vivo analysis of bone strain about the sagittal suture in Macaca mulatto during masticatory movements. J. Dent. Res. 57:904-908.
5. Bhanba JK (1961) Longitudinal and cephalometric roentgenographic study of face and cranium in relation to body height. J. Am. Dent. Assoc. 63:776-799.
6. Biewener AA (1992) Overview of structural mechanics. In A Beiwener (ed.): Biomechanics - Structures and Systems: A Practical Approach. Oxford: Oxford University Press, pp. 1-20.
7. Biewener AA, and Taylor CR ( 1986) Bone strain: A determinant of gait or speed? J. Exp. Biol. 723:383-400.
8. Biewener AA, Swartz SM, and Bertram JEA (1986) Bone modeling during growth: Dynamic strain equilibrium in the chick tibiotarsus. Calcif. Tissue Int. 39:390-395.
9. Borer KT (1980) Characteristics of growth-inducing exercise. Physiol. Behav. 24:713-720.
10. Bouvier M, and Hylander WL (1981) Effect of bone strain on cortical bone structure in macaques (Macaca mulatto). J. Morphol. 167:1-12.
11. Brace CL (1979) The Stages of Human Evolution, 2nd ed. Englewood Cliffs, NJ: Prentice-Hall.
12. Brasel J, Wright J, Wilkins L, and Blizzard R (1965) An evaluation of seventy-five patients with hypopituitarism beginning in childhood. Am. J. Med. 383:484-498.
13. Brook CGD (1989) Growth hormone deficiency: Features, assessment, and management. In L.J. DeGroot (ed.): Endocrinology, Vol. 1, 2nd ed. Philadelphia: W.B. Saunders, pp. 351-361.
14. Brown T, Pinkerton SK, and Lambert W (1979) Thickness of the cranial vault in Australian aboriginals. Arch. Phys. Anthropol. in Oceania 14:54-71.
15. Buchannan CR, and Preece MA (1992) Hormonal control of bone growth. In BK Hall (ed.): Bone, Vol. 6: Bone Growth. Boca Raton: CRC Press, pp. 53-89.
16. Carter DR (1987) Mechanical loading history and skeletal biology. J. Biomech. 20:1095-1109.
17. Coon CS (1962) The Origin of Races. New York: Alfred A. Knopf.
18. Corruccini RS, and Beecher RM (1982) Occlusal variation related to soft diet in a nonhuman primate. Science 218:74-16.
19. Corruccini RS, and Beecher RM (1984) Occlusofacial morphological integration lowered in baboons raised on soft diet. J. Craniofac. Gen. Dev. Biol. 4:135-142.
20. Currey J (1984) The Mechanical Adaptations of Bones. Princeton: Princeton University Press.
21. Dally JW, and Riley WF (1978) Experimental Stress Analysis, 2nd ed. New York: McGraw Hill.
22. Daughaday WH (1989) Growth hormone: Normal synthesis, secretion, control, and mechanisms of action. In LJ DeGroot (ed.): Endocrinology, Vol. 1, 2nd ed. Philadelphia: Saunders, pp. 318-329.
23. Duterloo HS, and DH Enlow (1970) A comparative study of cranial growth in Homo and Macaca. Am. J. Anat. 127:357-368.
24. Endo B (1966) Experimental studies on the mechanical significance of the form of the human facial skeleton. J. Facult. Sci. Univ. Tokyo, Section 3, 5:1-106.
25. Enlow DH (1990) Facial Growth, 3rd ed. Philadelphia: Saunders.
26. Felsing NE, Brasel JA, and Cooper D (1992) Effect of low and high intensity exercise on circulating growth hormone in men. J. Clin. Endocrinol. Metab. 75:157-162.
27. Frayer DH, Wolpoff MH, Thorne AG, Smith FH, and G Pope (1993) Theories of modern human origins: The palaeontological test. Am. Anthropol. 95:14-50.
28. Frost HM (1969) Tetracycline based histological analysis of bone remodeling. Calcif. Tissue Int. 3:211-217.
29. Frost HM (1983) Bone histomorphometry: Choice of marking agent and labeling schedule. In HM Frost (ed): Bone Histomorphometry. Boca Raton: CRC Press, pp. 38-52.
30. Frost HM (1986) The Intermediary Organization of the Skeleton. Boca Raton: CRC. Press.
31. Frost HM (1987) Bone "mass" and the "mechanostat": A proposal. Anat. Rec. 279:1-9.
32. Frost HM (1988) Vital biomechanics: Proposed general concepts for skeletal adaptations to mechanical usage. Calcif. Tissue Int. 42:145-156.
33. Garn SM, Lewis AB, and Kerewsky R (1965) Genetic, nutritional and maturational correlates of dental development J. Dent. Res. 44:228-242.
34. Gauld SE (1992) An Allometric Study of Anthropoid Cranial Bone Thickness: Implications of body size estimation in early hominid species. Ph.D. Dissertation, University of California, Los Angeles. Ann Arbor: Michigan Microfilms.
35. Gauld SE (1993) Body size of Asian Homo erectus: Estimation based on prediction models utilizing measures of cranial bone thickness (abstract). Am. J. Phys. Anthropol. Suppl 16:93.
36. Greaves WS (1985) The mammalian post-orbital bar as a torsion-resisting helical strut. J. Zool. Soc. London 207:125-136.
37. Groves CP (1989) A Theory of Human and Primate Evolution. Oxford: Oxford University Press.
38. Heim JL (1982) Les Enfants Neandrthaliens de la Ferrassie. Paris: Masson.
39. Herring SW (1993) Epigenetic and functional influences on skull growth. In J Hanken and BK Hall (eds.): The Skull, Vol 1. Chicago: University of Chicago Press, pp. 153-206.
40. Hylander WL (1986) In vivo bone strain as an indicator of masticatory force in Macaco fascilularis. Arch. Oral Biol. 37:149-157.
41. Hylander WL, and Johnson KR (1992) Strain gradients in the craniofacial region of primates. In Z Davidovitch (ed.): The Biological Mechanisms of Tooth Movement. Columbus, OH: Ohio State University College of Dentistry, pp. 559-569.
42. Hylander WL, Picq P, and Johnson KR (1991) Masticatory-stress hypotheses and the supraorbital region of primates. Am. J. Phys. Anthropol. 86:1-36.
43. Hylander WL, Picq P, and Johnson KR (1992) Bone strain and the supraorbital region of primates. In DS Carlson and SA Goldstein (eds.) Bone Biodynamics in Orthodontic and Orthopaedic Treatment, Vol. 27 Ann Arbor MI: Craniofacial Growth Series, Center for Human Growth and Development, pp. 315-349.
44. Isaakson OGP, Jansson JO, and Cause IAM (1982) Growth hormone stimulates longitudinal bone growth directly. Science 216:1237-1238.
45. Israel H (1973) Age factor and the pattern of change of craniofacial structures. Am. J. Phys. Anthropol. 39:111-128.
46. Israel H (1978) The fundamentals of cranial and facial growth. In F Falkner and JM Tanner (eds.): Human Growth, Vol. 2: Postnatal Growth. New York: Plenum, pp. 357-380.
47. Iwasaki K (1989) Dynamic responses in adult and infant monkey craniums during occlusion and mastication. J. Osaka Dent. Univ. 23:77-97.
48. Jones HH, Priest JD, Hayes WC, Tichenor CC, and Nadel A (1977) Humeral hypertrophy in response to exercise. J. Bone Joint Surg. [Am.] 59:204-208.
49. Kennedy GE (1985) Bone thickness in Homo erectus. J. Hum. Evol. 14:699-708.
50. Lane JM, Healy JH, Vigorita VJ, and Werntz JR (1986) Orthopedic management of osteoporosis: Effects of nutrition and exercise on the skeleton. In HK Uhthoff (ed.): Current Concepts on Bone Fragility. Berlin: Springer-Verlag, pp. 429-447.
51. Lanyon LE (1984) Functional strain as a determinant for bone remodeling. Calcif. Tissue Int. 36:556-561.
52. Lanyon LE, Rubin CT, and Banst G (1986) Modulation of bone loss during calcium insufficiency by controlled dynamic loading. Calcif. Tissue Int. 38:209-216.
53. Lassarre C, Girard F, Durand J, and Raynaud J (1974) Kinetics of human growth hormone during submaximal exercise. J. Appl. Physiol. 37:826-830.
54. LeGros Clark WE (1978) The Fossil Evidence for Human Evolution, 3rd ed. Chicago: University of Chicago Press.
55. Lieberman DE (1993) The rise and fall of hunter-gatherer seasonal mobility: The case of the southern Levant. Curr. Anthropol. 34:599-631.
56. Lieberman DE (1995) Testing hypotheses about recent human evolution from skulls: Integrating development, function, and phylogeny. Curr. Anthropol. 36:159-197.
57. Lieberman DE, and Crompton AW (in press) Responses of vertebrate bones to stress. In CR Taylor and E Weibel (eds.): Optimality in Biology: Controversies Over Symmorphosis. Cambridge: Cambridge University Press.
58. Lieberman DE, and Shea JJ (1994) Behavioral differences between archaic and modern humans in the Levantine Mousterian. Am. Anthropol. 96:300-332.
59. Loitz BJ, and Zernicke RF (1992) Strenuous exercise-induced remodeling of mature bone: Relationships between in vivo strains and bone mechanics. J. Exp. Biol. 170:1-18.
60. Lumley, MA de (1973) Anténéanderthaliens et Néanderthaliens du Bassin Mediterranean Occidental Européen. Etudes Quaternaires, Mémoires 2. Marseilles: Université de Provence.
61. Martin RB (1992) A theory of fatigue damage accumulation and repair in cortical bone. J. Orthop. Res. 10:818-825.
62. Martin RB, and Burr DB (1989) Structure, Function, and Adaptation of Compact Bone. New York: Raven Press.
63. Minugh-Purvis N (1988) Patterns of Craniofacial Growth and Development in Upper Pleistocene Hominids. Ph.D. Dissertation, University of Pennsylvania. Ann Arbor: Michigan Microfilms.
64. Moss ML (1954) Growth of the cal varia in the rat. Am. J. Anat. 98:191-204.
65. Moss ML, and Young RW (1960) A functional approach to craniology. Am. J. Phys. Anthropol. 18:281-292.
66. Muir WM, and Hubbell JAE (1989) Handbook of Veterinary Anesthesia. St. Louis: CV Mosby.
67. Naveri H (1985) Blood hormone and metabolic levels during graded cycle ergometer exercise. Scand. J. Lab. Clin. Invest. 45:559-603.
68. Nawrocki SP (1991) A Biomechanical Model of Cranial Vault Thickness in Archaic Homo. Ph.D. Dissertation, SUNY Binghamton.
69. Nawrocki SP (1992) Cranial thickness and skull biomechanics in Archaic Homo, Am. J. Phys. Anthropol. Suppl. 14:127.
70. Nelson AJ, and Gauld SE ( 1994) Covariance relationship between measures of cranial and post-cranial bone thickness and body mass. Am. J. Phys. Anthropol. Suppl. 18:151-152.
71. Ohtsuki F (1977) Developmental changes of the cranial bone thickness in the human fetal period. Am. J. Phys. Anthropol. 46:141-154.
72. Picq PG, and Hylander WL (1989) Endo's stress analysis of the primate skull and the functional significance of the supraorbital region. Am. J. Phys. Anthropol. 79:393-398.
73. Pirinen S, Majurin A, Lenko HL, and Koski K (1994) Craniofacial features in patients with deficient and excessive growth hormone. J. Craniofac. Genet. Dev. Biol. 14:144-152.
74. Poehlman ET, and Copeland KG (1990) Influence of physical activity on insulin-like growth factor I in healthy younger and older men. J. Clin. Endocrinol. Metab. 71:1468-1473.
75. Randall RV (1989) Acromegaly and gigantism. In LJ DeGroot (ed.): Endocrinology, Vol. 1, 2nd ed. Philadelphia: W.B. Saunders, pp. 330-350.
76. Ravosa MJ (1988) Browridgc development in Cercopithecidae: A test of two models. Am. J. Phys. Anthropol. 76:535-555.
77. Ravosa MJ (1991) Interspecific perspective on mechanical and nonmechanical models of primate circumorbital morphology. Am. J. Phys. Anthropol. 86:369-396.
78. Rawlinson CF, Mosley JR, Suswillo RFL, Pitsillides AA, and Lanyeon LE (1995) Calvarial and limb bone cells in organ and monolayer culture do not show the same early responses to dynamic mechanical strain. J. Bone Miner. Res. 10:1225-1232.
79. Roche AF (1953) Increase in cranial thickness during growth. Hum. Biol. 25:81-92.
80. Rubin CT, and Lanyon LE (1984) Regulation of bone formation by applied dynamic loads. J. Bone Joint Surg. 66:397-402.
81. Rubin CT, and Lanyon LE (1985) Regulation of bone mass by mechanical strain magnitude. Calcif. Tissue Int. 37:411-417.
82. Ruff CF (1992) Biomechanical analysis of archaeological human skeletal samples. In SR Saunders and A Katzenberg (eds.): Skeletal Biology of Past Peoples: Research Methods. New York: Wiley-Liss, pp. 37-58.
83. Ruff CB, and Hayes WC (1983a) Cross-sectional geometry of Pecos Pueblo femora and tibiae - a biomechanical investigation: I. Method and general pattern of variation. Am. J. Phys. Anthropol. 60:359-381.
84. RuffCB, and Hayes WC (1983b) Cross-sectional geometry of Pecos Pueblo femora and tibiae - a biomechanical investigation: II. Sex, age, and side differences. Am. J. Phys. Anthropol. 60:383-400.
85. Ruff CB, Trinkaus E, Walker A, and Larsen CS (1993) Postcranial robusticity in Homo I: Temporal trends and mechanical interpretation. Am. J. Phys. Anthropol. 91:21-53.
86. Ruff CB, Walker, A, and Trinkaus E (1994) Postcranial robusticity in Homo III: Ontogeny. Am. J. Phys. Anthropol. 93:35-54.
87. Russell MD (1985) The supraorbital torus: "A most remarkable peculiarity." Curr. Anthropol. 26:337-360.
88. Shea BT (1985) On aspects of skull form in African apes and orangutans, with implications for hominid evolution. Am. J. Phys. Anthropol. 68:329-342.
89. Skinner HC, and Nalbadian J (1975) Tetracyclines and mineralized tissues: Review and perspectives. Yale J. Biol. Med. 48:377-393.
90. Sperber GH (1989) Craniofacial Embryology, 4th ed. London: Wright.
91. Stringer CB (1984) The definition of the species Homo erectus and the existence of the species in Africa and Europe. Cour. Forsch. Ins. Senckenberg 69:131-143.
92. Stringer CB (1987) A numerical cladistic analysis for the genus Homo. J. Hum. Evol. 16:135-146.
93. Stringer CB (1988) Homo sapiens. In I Tattersall, E Delson, and W Van Couvering(eds.): The Encyclopedia of Human Evolution and Prehistory. New York: Garland, pp. 267-274.
94. Sugimura T, Inada J, Sawa S, and Kakudo Y (1984) Dynamic responses of the skull caused by loss of occlusal force J. Osaka Dent. Univ. 18:29-42.
95. Thorne AG, and Wolpoff JMH (1981) Regional continuity in Australian Pleistocene hominid evolution. Am. J. Phys. Anthropol. 55:337-349.
96. Todd TW (1924) Thickness of the white male cranium Anat. Rec. 27:245-256.
97. Turner AS (1992) Functional determinants of bone structure: Beyond Wolff's law of bone transformation. Bone 13:403-409.
98. Twiesselmann F (1941) Méthode pour l'évaluation de l'épaisseur des parois cranienne. Bull. Musée Royal d'Histoire Nat. Belgique 17:1-33.
99. Van Helder WP, Casey K, Goode RC, and Radomski WM (1986) Growth hormone regulation in two types of exercise of equal oxygen uptake. Eur. J. Appl. Physiol. 55:236-239.
100. Vogl Ç, Atchley WR, Cowley DR, Crenshaw P, Murray J, and Pomp D (1993) The epigenetic influence of growth hormone on skeletal development. Growth Dev. Aging 57:163-182.
101. Wainright SA, Biggs BA, Currey JD, and Gosline JM (1976) Mechanical Design in Organisms. Princeton: Princeton University Press.
102. Washburn SL (1947) The relation of the temporal muscle to the form of the skull. Anat. Rec. 99:239-248.
103. Webb S (1990) Cranial thickening in an Australian hominid as a possible palaeoepidemiological indicator. Am. J. Phys. Anthropol. 52:403-411.
104. Weidenreich F (1941) The brain and its rôle in the phylogenetic transformation of the human skull. Trans. Am. Phil. Soc. 37:321-442.
105. Weidenreich F (1943) The skull of Sinanthropus pekinensis: A comparative study of a primitive hominid skull. Palaeontologica Sinica, NS D 10:1-484.
106. Williams PL, Warwick R, Dyson M, and Bannister LH (1989) Gray's Anatomy, 37th edition. Edinburgh: Churchill Livingstone.
107. Wolpoff MH (1980) Paleoanthropology. New York: Knopf.
108. Woo SLY, Kuei SC. Amiel D, Gomez MA, Hayes WC, White FC, and Akeson WH (1981) The effect of prolonged physical training on the properties of long bone: A study of Wolff's law. J. Bone Joint Surg. 63:780-787.
109. Yamada K, and Rimmel DB (1991) The effect of dietary consistency on bone mass and turnover in the growing rat mandible. Arch. Oral Biol. 36:129-138.
110. Young RW (1957) Postnatal growth of the frontal and parietal bones in white males. Am. J. Phys. Anthropol. 15:367-386.
111. Zollikofer CPE, Ponce de Leon MS, Martin RS, and Stucki P (1995) Neanderthal computer skulls. Nature 375:283-285.