Comparative microanatomy of the orbicularis oris muscle between chimpanzees and humans: Evolutionary divergence of lip function

Journal of Anatomy

Volumn 214, Issue 1, 2009, Pages 36-44

  Rogers, Carolyn R ^a   Mooney, Mark P ^b   Smith, Timothy D ^b,c   Weinberg, Seth M ^b   Waller, Bridget M ^d   Parr, Lisa A ^e   Docherty, Beth A ^f   Bonar, Christopher J ^g   Reinholt, Lauren E ^c   Deleyiannis, Frederic W B ^h   Siegel, Michael I ^b   Marazita, Mary L ^b   Burrows, Anne M ^b,f  

^a University of Wisconsin Health   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c SLIPPERY ROCK UNIVERSITY   (United States)

^d UNIVERSITY OF PORTSMOUTH   (United Kingdom)

^e EMORY UNIVERSITY   (United States)

^f DUQUESNE UNIVERSITY   (United States)

^g Duquesne University ^*  (United States)

^h UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Chimpanzee; Evolution; Histomorphometrics; Lips; Orbicularis oris; Speech; Wadging

Indexed keywords

ANIMAL TISSUE; ARTICLE; CHIMPANZEE; COMPARATIVE ANATOMY; CONNECTIVE TISSUE; CONTROLLED STUDY; EVOLUTION; FACIAL EXPRESSION; FEEDING; HISTOLOGY; HUMAN; HUMAN TISSUE; MORPHOMETRICS; MUSCLE CELL; MUSCLE FUNCTION; MUSCLE TISSUE; NONHUMAN; OBJECT MANIPULATION; ORBICULARIS ORIS MUSCLE; PRIORITY JOURNAL; SPEECH DEVELOPMENT; THICKNESS; VOCALIZATION;

ADULT; ANIMALS; EVOLUTION; FACIAL EXPRESSION; FACIAL MUSCLES; FEMALE; HUMANS; LIP; MALE; MUSCLE FIBERS, SKELETAL; PAN TROGLODYTES;

PAN; PAN TROGLODYTES; PRIMATES;

EID: 58149357462     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2008.01004.x     Document Type: Article

References (92)

1. Abbs JH, Gracco VL, Blair C (1984) Functional muscle partitioning during voluntary movement: Facial muscle activity for speech. Exp Neurol 85, 469-479.
2. Anapol F, Barry K (1996) Fiber architecture of the extensors of the hindlimb in semiterrestrial and arboreal guenons. Am J Phys Anthropol 99, 429-447.
3. Anapol FC, Gray JP (2003) Fiber architecture of the intrinsic muscles of the shoulder and arm in semiterrestrial and arboreal guenons. Am J Phys Anthropol 122, 51-65.
4. Anapol FC, Jungers WL (1986) Architectural and histochemical diversity within the quadriceps femoris of the brown lemur (Lemur fulvus). Am J Phys Anthropol 69, 355-375.
5. Antón SC (1999) Macaque masseter muscle: Internal architecture, fiber length and cross-sectional area. Int J Primatol 20, 441-462.
6. Antón SC (2000) Macaque pterygoid muscle: Internal architecture, fiber length and cross-sectional area. Int J Primatol 21, 131-156.
7. Bard KA (2003) Development of emotion expressions in chimpanzees (Pan troglodytes). Ann NY Acad Sci 1000, 88-90.
8. Barlow SM, Muller EM (1991) The relationship between interangle span and in vivo resultant force in the perioral musculature. J Speech Lang Hear Res 34, 252-259.
9. Briedis J, Jackson IT (1980) The anatomy of the philtrum: Observations made on dissections in the normal lip. Br J Plast Surg 34, 128-132.
10. Burrows AM (2008) The facial expression musculature in primates and its evolutionary significance. BioEssays 30, 212-225.
11. Burrows AM, Smith TD (2003) Muscles of facial expression in Otolemur, with a comparison to Lemuroidea. Anat Rec 274A, 827-836.
12. Burrows AM, Waller BM, Parr LA, Bonar CJ (2006) Muscles of facial expression in the chimpanzee (Pan troglodytes): Descriptive, comparative and phylogenetic contexts. J Anat 208, 153-167.
13. Calvert GA, Campbell R (2003) Reading speech from still and moving faces: The neural substrates of visible speech. J Cogn Neurosci 15, 57-70.
14. Caviness JN, Liss JM, Adler C, Evidente V (2006) Analysis of high-frequency electroencephalographic-electromyographic coherence elicited by speech and oral nonspeech tasks in Parkinson's disease. J Speech Lang Hear Res 49, 424-438.
15. Chen FC, Li WH (2001) Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am J Hum Genet 68, 444-456.
16. Darwin CR (1872) The Expression of Emotions in Man and Animals. London: J. Murray.
17. Delaire J, Precious D (1986) Influence of the nasal septum on maxillonasal growth in patients with congenital labiomaxillary cleft. Cleft Pal J 23, 270-277.
18. Diogo R (2004) Muscles versus bones: Catfishes as a case study for an analysis on the contribution of mycological and osteological structures in phylogenetic reconstructions. Anim Biol 54, 373-391.
19. Docherty BA, Cray JJ Jr, Smith TD, Reinholt LE, Burrows AM (2008) Comparative microanatomy of primate facial musculature: Facing up to function. Am J Phys Anthropol Suppl 46, 91.
20. Dubowitz V (1985) Muscle Biopsy: A Practical Approach, 2nd edn. London: Bailliere Tindall Press.
21. Ekman P, Oster H (1979) Facial expression of emotion. Ann Rev Psych 20, 527-554.
22. van Eijden TMGJ, Koolstra JH, Brugman P (1996) Three-dimensional structure of the human temporalis muscle. Anat Rec 246, 565-572.
23. Gangstead SW, Scheyd GJ (2005) The evolution of human physical attractiveness. Annu Rev Anthropol 34, 523-548.
24. Gans C (1982) Fiber architecture and muscle function. Exercise Sport Sci Rev 10, 160-207.
25. Gasser RF (1967) The development of the facial muscles in man. Am J Anat 120, 357-376.
26. Ghassemi A, Prescher A, Riediger D, Axer H (2003) Anatomy of the SMAS revisited. Aesth Plast Surg 27, 258-264.
27. Gibbs S, Collard M, Wood B (2002) Soft-tissue anatomy of the extant hominoids: A review and phylogenetic analysis. J Anat 200, 3-49.
28. Goodall J (1986) The Chimpanzees of Gombe: Patterns of Behavior. Cambridge: Harvard University Press.
29. Goodmurphy CW, Ovalle WK (1999) Morphological study of two human facial muscles: Orbicularis oculi and corrugator supercilii. Clin Anat 12, 1-11.
30. Groves C (2001) Primate Taxonomy. Washington, DC: Smithsonian Institution.
31. Herring SW, Grimm AF, Grimm BR (1984) Regulation of sarcomere number in skeletal muscle: A comparison of hypotheses. Muscle Nerve 7, 161-173.
32. Hinton VA, Arokiasamy WMC (1997) Maximum interlabial pressures in normal speakers. J Speech Lang Hear Res 40, 400-404.
33. van Hooff JARAM (1973) A structural analysis of the social behaviour in a semi-captive group of chimpanzees. In Nonverbal Communication (ed. Hinde RA), pp. 209-241. Cambridge: Cambridge University Press.
34. Hopkins WD, Bard KA, Jones A, Bales S (1993) Chimpanzee hand preference for throwing and infant cradling: Implications for the origin of human handedness. Curr Anthropol 34, 786-790.
35. Huber E (1931) Evolution of Facial Musculature and Expression. Baltimore: The Johns Hopkins University Press.
36. Hwang K, Kim DJ, Hwang SH (2007a) Immunohistochemical study of differences between the muscle fiber types in the pars peripheralis and marginalis. J Craniofac Surg 18, 591-593.
37. Hwang K, Kim DJ, Hwang SH (2007b) Musculature of the pars marginalis of the upper orbicularis oris muscle. J Craniofac Surg 18, 151-154.
38. Ito T, Murano EZ, Gomi H (2004) Fast force-generation dynamics of human articulatory muscles. J Appl Physiol 96, 2318-2324.
39. Jacinto-Gonçalves SR, Gavio MB, de Oliveira AS, Semeguini TA (2004) Electromyographic activity of perioral muscle in breastfed and non-breastfed children. J Clin Pediatr Dent 29, 57-62.
40. Jones D (1999) An evolutionary perspective on physical attractiveness. Evol Anthropol 5, 97-109.
41. Kraus BS, Kitamura H, Latham RA (1966) Atlas of Developmental Anatomy of the Face. New York: Harper & Row.
42. Lambert JE (1999) Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. Am J Phys Anthropol 109, 365-386.
43. Larrabee WF Jr, Makielski KH (1993) Surgical Anatomy of the Face. New York: Raven Press.
44. Latham RA, Deaton TG (1976) The structural basis of the philtrum and the contour of the vermilion border: A study of the musculature of the upper lip. J Anat 121, 151-160.
45. Lieberman DE, Ross CF, Ravosa MJ (2000) The primate cranial base: ontogeny, function, and integration. Ybk Phys Anthropol 43, 117-169.
46. Lieberman P (2007) The evolution of human speech. Curr Anthropol 48, 39-66.
47. Lightoller GS (1925) Facial muscles: The modiolus and muscles surrounding the rima oris with some remarks about the panniculus adiposus. J Anat 60 (1), 1-85.
48. Lightoller GS (1928) The facial muscles of three orang utans and two cercopithecidae. J Anat 63, 19-81.
49. McGurk H, MacDonald J (1976) Hearing lips and seeing voices. Nature 264, 746-748.
50. Mooney MP, Siegel MI, Kimes KR, Todhunter J (1988) Development of the orbicularis oris muscle in normal and cleft lip and palate human fetuses using three-dimensional computer reconstruction. Plast Reconstr Surg 81, 336-345.
51. Nakamura M (2003) 'Gatherings' of social grooming among wild chimpanzees: Implications for evolution of sociality. J Hum Evol 44, 59-71.
52. Namnoum JD, Hisley KC, Graepel S, Hutchins GN, Vander Kolk CA (1997) Three-dimensional reconstruction of the human fetal philtrum. Ann Plast Surg 38, 202-208.
53. Nishida T, Kano T, Goodall J, McGrew W, Nakamura M (1999) The ethogram and ethnography of Mahale chimpanzees. Anthropol Sci 107, 141-188.
54. Nishida T, Mitani JC, Watts DP (2004) Variable grooming behaviours in wild chimpanzees. Folia Primatol 75, 31-36.
55. Nishimura T, Mikami A, Suzuki J, Matsuzawa T (2003) Descent of the larynx in chimpanzee infants. Proc Natl Acad Sci USA 100, 6930-6933.
56. Nishimura T, Mikami A, Suzuki J, Matsuzawa T (2006) Descent of the hyoid in chimpanzees: Evolution of face flattening and speech. J Hum Evol 51, 244-254.
57. O'Rahilly R, Müller F (2007) The development of the neural crest in the human. J Anat 211, 335-351.
58. Oster H (2004) The repertoire of infant facial expressions: An ontogenetic perspective. In Emotional Development: Recent Research Advances (eds Nadel J, Muir D), pp. 261-292. New York: Oxford University Press.
59. Otten E (1988) Concepts and models of functional architecture in skeletal muscle. Exercise Sport Sci Rev 16, 89-137.
60. Parr LA (2003) The discrimination of faces and their emotional content by chimpanzees (Pan troglodytes). Ann NY Acad Sci 1000, 56-78.
61. Parr LA, de Waal FBM (1999) Visual kin recognition in chimpanzees. Nature 399, 147-148.
62. Parr LA, Hopkins SD, de Waal FBM (1998) The perception of facial expressions by chimpanzees, Pan troglodytes. Evol Comm 2, 1-23.
63. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D (2006) Genetic evidence for complex speciation of humans and chimpanzees. Nature 441, 1103-1108.
64. Pellatt A (1979) The facial muscles of three African primates, contrasted with those of Papio ursinus. S Afr J Sci 75, 436-440.
65. Raphael LJ, Borden GJ, Harris KS (2007) Speech Science Primer: Physiology, Acoustics, and Perception of Speech, 5th edn. Philadelphia: Lippincott, Williams & Wilkins.
66. Rastatter M, DeJarnette G (1984) EMG activity with jaw fixed of orbicularis oris superior, orbicularis oris inferior and masseter muscles of articulatory disordered children. Percep Motor Skills 58, 191-196.
67. Rastatter M, McGuire R, Blair B (1987) EMG activity of orbicularis oris superior, orbicularis oris inferior, and masseter muscles of mild and moderate articulatory disordered children. Percept Mot Skills 64, 725-726.
68. Regalo SCH, Vitti M, Moraes MTB, et al. (2005) Electromyographic analysis of the orbicularis oris muscle in oralized deaf individuals. Braz Dent J 16, 237-242.
69. Rowlerson A, Raoul G, Daniel Y, et al. (2005) Fiber-type differences in masseter muscle associated with different morphologies. Am J Orthod Dentofacial Orthop 127, 37-46.
70. Sanz CM, Morgan DB (2007) Chimpanzee tool technology in the Goualougo Triangle, Republic of Congo. J Hum Evol 52, 420-433.
71. Schmidt KL, Cohn JF (2001) Human facial expressions as adaptations: evolutionary questions in facial expression research. Yearb Phys Anthropol 44, 3-24.
72. Schwartz JL, Berthommier F, Savariaux C (2004) Seeing to hear better: evidence for early audio-visual interactions in speech identification. Cognition 93, B69-78.
73. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. New York: W.H. Freeman and Company.
74. Sonntag CF (1923) On the anatomy, physiology, and pathology of the chimpanzee. Proc Zool Soc Lond 23, 323-429.
75. Standring S (2004) Gray's Anatomy: The Anatomical Basis of Clinical Practice, 39th edn. London: Churchill Livingstone.
76. Tamura Y, Matsushita S, Shinoda K, Yoshida S (1998) Development of perioral muscle activity during suckling in infants: A cross-sectional and follow-up study. Dev Med Child Neurol 40, 344-348.
77. Taylor AB, Vinyard CJ (2004) Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. J Morphol 261, 276-285.
78. Taylor AB, Jones KE, Kunwar R, Ravosa MJ (2006) Dietary consistency and plasticity of masseter fiber architecture in postweaning rabbits. Anat Rec 288, 1105-1111.
79. Thaller SR, Kim S, Patterson H, Widman M, Daniller A (1990) The submuscular aponeurotic system (SMAS): A histologic and comparative anatomy evaluation. Plast Reconstr Surg 86, 690-696.
80. The Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69-87.
81. Titze IR (1994) Principles of Voice Production. Englewood Cliffs, NJ: Prentice-Hall.
82. Tomasello M, Hare B, Lehmann H, Call J (2007) Reliance on head versus eyes in the gaze following of great apes and human infants: The cooperative eye hypothesis. J Hum Evol 52, 314-320.
83. Vick SJ, Waller BM, Parr LA, Smith Pasqualini MC, Bard KA (2007) A cross-species comparison of facial morphology and movement in humans and chimpanzees using the facial action coding system (FACS). J Nonverb Behav 31, 1-20.
84. Waller BM, Dunbar RIM (2005) Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 111, 129-142.
85. Waller BM, Vick SJ, Parr LA, et al. (2006) Intramuscular electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended. Emotion 6, 367-382.
86. Waller BM, Parr LA, Gothard KM, Burrows AM, Vick SJ, Fuglevand AJ (2008) Intramuscular electrical stimulation of facial muscles in the rhesus macaque. Phys Beh 95, 93-100.
87. van Wassenbergh S, Herrel A, Adriaens D, Aerts P (2007) Interspecific variation in sternohyoideus muscle morphology in clariid catfishes: functional implications for suction feeding. J Morphol 268, 232-242.
88. Whiten A, Boesch C (2001) The cultures of chimpanzees. Sci Am 284, 60-67.
89. Whiten A, Goodall J, McGrew WC, et al. (1999) Cultures in chimpanzees. Nature 399, 682-685.
90. Wrangham RW, Conklin NL, Etot G, et al. (1993) The value of figs to chimpanzees. Int J Primatol 14, 243-256.
91. Wrangham RW, Chapman CA, Chapman LJ (1994) Seed dispersal by forest chimpanzees in Uganda. J Trop Ecol 10, 355-368.
92. Young JZ (1957) The Life of Mammals. Oxford: Clarendon Press.