Face to face with the social brain

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1597, 2012, Pages 1901-1908

  Dobson, Seth ^a  

^a Dartmouth College   (United States)

Author keywords

Cooperation; Emotional expressivity; Facial motor nucleus; Neocortex; Primates

Indexed keywords

BRAIN; COOPERATIVE BEHAVIOR; GROUP SIZE; HYPOTHESIS TESTING; PRIMATE; PSYCHOLOGY; QUANTITATIVE ANALYSIS; VOLUME;

PRIMATES; SIMIIFORMES; VERTEBRATA;

EID: 84861553377     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0224     Document Type: Review

References (92)

1. Dunbar, R. I. M. & Shultz, S. 2007 Understanding primate brain evolution. Phil. Trans. R. Soc. B 362, 649-658. (doi:10.1098/rstb.2006.2001).
2. Perez-Barberia, F. J., Shultz, S. & Dunbar, R. I. M. 2007 Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61, 2811-2821. (doi:10.1111/j.1558-5646.2007.00229.x).
3. Shultz, S. & Dunbar, R. I. M. 2010 Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc. Natl Acad. Sci. USA 107, 21582-21586. (doi:10.1073/pnas.1005246107).
4. Shultz, S. & Dunbar, R. I. M. 2010 Social bonds in birds are associated with brain size and contingent on the correlated evolution of life history and increased parental investment. Biol. F Linn. Soc. 100, 111-123. (doi: 10. 1111/j.1095-8312.2010.01427.x)
5. Barton, R. A. 1996 Neocortex size and behavioural ecology in primates. Proc. R. Soc. Lond. B 263, 173-177. (doi:10.1098/rspb.1996.0028).
6. Shultz, S. & Dunbar, R. I. M. 2007 The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc. R. Soc. B. 274, 2429-2436. (doi:10.1098/rspb.2007.0693)
7. Dunbar, R. I. M. & Shultz, S. 2007 Evolution in the social brain. Science 317, 1344-1347. (doi:10.1126/ science.1145463)
8. Darwin, C. 1871 The expression of the emotions in man and animals. London, UK: John Murray.
9. van Hooff, J. A. R. A. M. 1967 The facial displays of the catarrhine monkeys and apes. In Primate ethology (ed D. Morris), pp. 7-68. Chicago, IL: Aldine.
10. Preuschoft, S. & van Hooff, J. 1997 The social functions of smile and laughter: variations across primate species and societies. In Where nature meets culture: nonverbal communication in the social interaction (eds U. Segerstrale & P. Molnar), pp. 171-189. Hillsdale, NJ: Erlbaum.
11. Waller, B. M. & Dunbar, R. I. M. 2005 Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 111, 129-142. (doi:10.1111/j.1439-0310.2004.01045.x).
12. Preuschoft, S. 1992 Laughter and smile in Barbary macaques (Macaca sylvanus). Ethology 91, 220-236. (doi:10.1111/j.1439-0310.1992.tb00864.x).
13. Bout, N. & Thierry, B. 2005 Peaceful meaning for the silent bared-teeth displays of mandrills. Int.F. Primatol. 26, 1215-1228. (doi:10.1007/s10764-005-8850-1).
14. De Marco, A., Petit, O. & Visalberghi, E. 2008 The repertoire and social function of facial displays in Cebus capucinus. Int. F Primatol. 29, 469-486. (doi:10.1007/ s10764-007-9174-0)
15. Dunbar, R. I. M. 2010 The social role of touch in humans and primates: behavioural function and neurobiological mechanisms. Neurosci. Biobehay. Rev. 34, 260-268. (doi:10.1016/j.neubiorev.2008.07.001).
16. Burrows, A. M. & Smith, T. D. 2003 Muscles of facial expression in Otolemur, with a comparison to Lemuroidea. Anat. Rec. 274, 827-836. (doi:10.1002/ar.a.10093).
17. Burrows, A. M., Waller, B. M., Parr, L. A. & Bonar, C. J. 2006 Muscles of facial expression in the chimpanzee (Pan troglodytes): descriptive, comparative and phylogenetic contexts. F Anat. 208, 153-167. (doi:10.1111/j. 1469-7580.2006.00523.x)
18. Burrows, A. M. 2008 The facial expression musculature in primates and its evolutionary significance. Bioessays 30, 212-225. (doi:10.1002/bies.20719).
19. Burrows, A. M., Waller, B. M. & Parr, L. A. 2009 Facial musculature in the rhesus macaque (Macaca mulatta): evolutionary and functional contexts with comparisons to chimpanzees and humans. F Anat. 215, 320-334. (doi:10.1111/j.1469-7580.2009.01113.x.Facial).
20. Diogo, R., Wood, B. A., Aziz, M. A. & Burrows, A. 2009 On the origin, homologies and evolution of primate facial muscles, with a particular focus on hominoids and a suggested unifying nomenclature for the facial muscles of the Mammalia. F. Anat. 215, 300-319. (doi:10. 1002/ar.21355)
21. Burrows, A. M., Diogo, R., Waller, B. M., Bonar, C. J. & Liebal, K. 2011 Evolution of the muscles of facial expression in a monogamous ape: evaluating the relative influences of ecological and phylogenetic factors in hylobatids. Anat. Rec. 294, 645-663. (doi:10.1002/ar.21355).
22. Sherwood, C. C., Holloway, R. L., Gannon, P. J., Semendeferi, K., Erwin, J. M., Zilles, K. & Hof, P. R. 2003 Neuroanatomical basis of facial expression in monkeys, apes, and humans. In Emotions inside out-130 years after Darwin's the expression of the emotions in man and animals (eds P. Ekman, J. J. Campos, R. J. Davidson & F. B. M. DeWaal), pp. 99-103. New York, NY: New York Academy of Sciences.
23. Sherwood, C. C., Holloway, R. L., Erwin, J. M. & Hof, P. R. 2004 Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II. Stereologic analysis of chemoarchitecture. Brain Behay. Evol. 63, 82-106. (doi:10.1159/000075673).
24. Sherwood, C. C., Holloway, R. L., Erwin, J. M., Schleicher, A., Zilles, K. & Hof, P. R. 2004 Cortical orofacial motor representation in old world monkeys, great apes, and humans-I. Quantitative analysis of cytoarchitecture. Brain Behav. Evol. 63, 61-81. (doi:10.1159/000075672).
25. Sherwood, C. C. 2005 Comparative anatomy of the facial motor nucleus in mammals, with an analysis of neuron numbers in primates. Anat. Rec. 287A, 1067-1079. (doi:10.1002/ar.a.20259).
26. Sherwood, C. C., Hof, P. R., Holloway, R. L., Semendeferi, K., Gannon, P. J., Frahm, H. D. & Zilles, K. 2005 Evolution of the brainstem orofacial motor system in primates: a comparative study of trigeminal, facial, and hypoglossal nuclei. F. Hum. Evol. 48, 45-84. (doi:10.1016/j.jhevol.2004.10.003).
27. Dobson, S. D. & Sherwood, C. C. 2011 Correlated evolution of brain regions involved in producing and processing facial expressions in anthropoid primates. Biol. Lett. 7, 86-88. (doi:10.1098/rsb1.2010.0427).
28. Dobson, S. D. 2009 Socioecological correlates of facial mobility in nonhuman anthropoids. Am. F Phys. Anthropol. 139, 413-420. (doi:10.1002/ajpa.21007).
29. Ekman, P. & Friesen, W. V. 1976 Measuring facial movement. Environ. Psychol. Nonverb. Behav. 1, 56-75. (doi:10.1007/BF01115465).
30. Ekman, P., Friesen, W. V. & Hager, J. C. 2002 Facial action coding system: the manual on CD-ROM. Salt Lake City, UT: Research Nexus.
31. Waller, B. M., Vick, S. J., Parr, L. A., Bard, K. A., Pasqualini, M. C. S., Gothard, K. M. & Fuglevand, A. J. 2006 Intramuscular electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended. Emotion 6, 367-382. (doi:10. 1037/1528-3542.6.3.367)
32. Dobson, S. D. 2009 Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression. Am. F Phys. Anthropol. 138, 70-81. (doi:10.1002/ajpa.20902).
33. Simons, G., Ellgring, H. & Pasqualini, M. C. S. 2003 Disturbance of spontaneous and posed facial expressions in Parkinson's disease. Cogn. Emotion 17, 759-778.
34. Simons, G., Pasqualini, M. C. S., Reddy, V. & Wood, J. 2004 Emotional and nonemotional facial expressions in people with Parkinson's disease. F Int. Neuropsych. Soc. 10, 521-535. (doi:10.10170S135561770410413X).
35. Zuckerman, M., Defrank, R. S., Hall, J. A. & Rosenthal, R. 1976 Encoding and decoding of spontaneous and posed facial expressions. F. Pers. Soc. Psychol 34, 966-977. (doi:10.1037/0022-3514.34.5.966).
36. Berenbaum, H. & Rotter, A. 1992 The relationship between spontaneous facial expressions of emotion and voluntary control of facial muscles. F. Nonverb. Behay. 16. 179-190. (doi:10.1007/BF00988033).
37. Dunbar, R. I. M. 1992 Neocortex size as a constraint on group size in primates. F. Hum. Evol 22, 469-493. (doi:10.1016/0047-2484(92)90081-J).
38. Dunbar, R. I. M. 1995 Neocortex size and group size in primates: a test of the hypotheses. F Hum. Evol 28, 287-296. (doi:10.1006/jhev.1995.1021).
39. Joffe, T H. & Dunbar, R. I. M. 1997 Visual and sociocognitive information processing in primate brain evolution. Proc. R. Soc. Land B. 264, 1303-1307. (doi:10. 1098/rspb.1997.0180)
40. Dunbar, R. I. M. The social brain hypothesis. Evol. Anthropol 6, 178-190. (doi:10.1002/(SICI)1520-6505 (1998)6:5 < 178::AID-EVAN5 > 3.0.0O;2-8)
41. Barton, R. A. 1998 Visual specialization and brain evolution in primates. Proc. R. Soc. Lond. B 265, 1933-1937. (doi:10.1098/rspb.1998.0523).
42. Barton, R. A. 2006 Primate brain evolution: integrating comparative, neurophysiological, and ethological data. Evol. Anthropol 15, 224-236. (doi:10.1002/evan.20105).
43. Kudo, H. & Dunbar, R. I. M. 2001 Neocortex size and social network size in primates. Anim. Behay. 62, 711-722. (doi:10.1006/anbe.2001.1808).
44. Lehmann, J., Korstjens, A. H. & Dunbar, R. I. M. 2007 Group size, grooming and social cohesion in primates. Anim. Behay. 74, 1617-1629. (doi:10.1016/j.anbehay. 2006.10.025)
45. Lehmann, J. & Dunbar, R. I. M. 2009 Network cohesion, group size and neocortex size in female-bonded Old World primates. Proc. R. Soc. Lond. B. 276, 4417-4422. (doi:10.1098/rspb. 2009.1409)
46. Pawlowski, B., Lowen, C. B. & Dunbar, R. I. M. 1998 Neocortex size, social skills and mating success in primates. Behaviour 135, 357-368. (doi:10.1163/15685 3998793066285)
47. Byrne, R. W. & Corp, N. 2004 Neocortex size predicts deception rate in primates. Proc. R. Soc. Lond. B 271, 1693-1699. (doi:10.1098/rspb.2004.2780).
48. Deaner, R. O., Isler, K., Burkart, J. & van Schaik, C. 2007 Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behay. Evol. 70, 115-124. (doi:10.1159/000102973).
49. Shultz, S. & Dunbar, R. I. M. 2010 Species differences in executive function correlate with hippocampus volume and neocortex ratio across nonhuman primates. F. Comp. Psychol. 124, 252-260. (doi:10.1037/a0018894).
50. Barton, R. A. 2004 Binocularity and brain evolution in primates. Proc. Natl Acad. Sci. USA 101, 10113-10115. (doi:10.1073/pnas.0401955101).
51. Tsao, D. Y., Freiwald, W. A., Knutsen, T. A., Mandeville, J. B. & Tootell, R. B. H. 2003 Faces and objects in macaque cerebral cortex. Nat. Neurosci. 6, 989-995. (doi:10.1038/nn1111)
52. Moeller, S., Freiwald, W. A. & Tsao, D. Y. 2008 Patches with links: a unified system for processing faces in the macaque temporal lobe. Science 320, 1355-1359. (doi:10.1126/science.1157436)
53. Parr, L. A., Hecht, E., Barks, S. K., Preuss, T M. & Votaw, J. R. 2009 Face processing in the chimpanzee brain. Curr. Bid. 19, 50-53. (doi:10.1016/j.cub.2008.11.048).
54. Haxby, J. V., Hoffman, E. A. & Gobbini, M. I. 2000 The distributed human neural system for face perception. Trends Cogn. Sci. 4, 23-33. (doi:10.1016/S1364-6613 (00)01482-0)
55. Adolphs, R. 2000 Neural systems for recognizing emotion. Curr. Opin. Neurobiol 12, 169-177. (doi:10.1016/S0959-4388(02)00301-X)
56. Tsao, D. Y., Schweers, N., Moeller, S. & Freiwald, W. A. 2008 Patches of face-selective cortex in the macaque frontal lobe. Nat. Neurosci. 11, 877-879. (doi:10.1038/ nn.2158)
57. Dunbar, R. I. M. 2003 The social brain: mind, language, and society in evolutionary perspective. Annu. Rev. Anthropol 32, 163-181. (doi:10.1146/annurev.anthro.32.061002.093158)
58. Morecraft, R., Louie, J. & Herrick, J. 2001 Cortical inner-vation of the facial nucleus in the non-human primate. Brain 124, 176-208. (doi:10.1093/brain/124.1.176).
59. Barton, R. A. & Harvey, P. H. 2000 Mosaic evolution of brain structure in mammals. Nature 405, 1055-1058. (doi:10.1038/35016580).
60. de Winter, W. & Oxnard, C. E. 2001 Evolutionary radiations and convergences in the structural organization of mammalian brains. Nature 409, 710-714. (doi:10.1038/35055547)
61. Barton, R. A. 2007 Evolutionary specialization in mammalian cortical structure. F. Evol Biol 20, 1504-1511. (doi:10.1111/j.1420-9101.2007.01330.x).
62. Dobson, S. & Sherwood, C. 2011 Mosaic evolution of brainstem motor nuclei in catarrhine primates. Anatomy Research International, 2011 (doi:10.1155/2011/236894).
63. Whiting, B. A. & Barton, R. A. 2003 The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution. F Hum. Evol 44, 3-10. (doi:10.1016/S0047-2484(02)00162-8)
64. Martins, E. P. & Hansen, T F. 1997 Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646-667. (doi:10.1086/286013).
65. Pagel, M. 1999 Inferring the historical patterns of biological evolution. Nature 401, 877-884. (doi:10.1038/44766).
66. Garland, T & Ives, A. R. 2000 Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346-364. (doi:10.1086/303327).
67. Dunbar, R. I. M. 1991 Functional significance of social grooming in primates. Folia Primatol 57, 121-131. (doi:10.1159/000156574).
68. Schino, G. 2007 Grooming and agonistic support: a meta-analysis of primate reciprocal altruism. Behay. Ecol. 18, 115-120. (doi:10.1093/beheco/ar1045).
69. Seyfarth, R. M. 1977 Model of social grooming among adulate female monkeys. F. Theor. Biol. 65, 671-698. (doi:10.1016/0022-5193(77)90015-7).
70. Seyfarth, R. M. 1980 The distribition of grooming and related behaviors among adult female vervet monkeys. Anim. Behay. 28, 798-813. (doi:10.1016/S0003-3472(80)80140-0)
71. Schino, G. 2001 Grooming, competition and social rank among female primates: a meta-analysis. Anim. Behay. 62, 265 -271. (doi:10.1006/anbe.2001.1750).
72. Schino, G. & Aureli, F. 2008 Grooming reciprocation among female primates: a meta-analysis. Biol. Lett. 4, 9-11. (doi:10.1098/rsb1.2007.0506).
73. Dunbar, R. I. M. & Shultz, S. 2010 Bondedness and sociality. Behaviour 147, 775-803. (doi:10.1163/000579510X501151)
74. Boone, R. T. & Buck, R. 2003 Emotional expressivity and trustworthiness: the role of nonverbal behavior in the evolution of cooperation. F Nonverb. Behay. 27, 163-182. (doi:10.1023/A:1025341931128)
75. Schug, J., Matsumoto, D., Horita, Y., Yamagishi, T. & Bonnet, K. 2010 Emotional expressivity as a signal of cooperation. Evol. Hum. Behay. 31, 87-94. (doi:10. 1016/j.evolhumbehay.2009.09.006)
76. Mehu, M., Grammer, K. & Dunbar, R. I. M. 2007 Smiles when sharing. Evol. Hum. Behay. 28, 415-422. (doi:10.1016/j.evolhumbehay.2007.05.010).
77. Krumhuber, E., Manstead, A. S. R., Cosker, D., Marshall, D., Rosin, P. L. & Kappas, A. 2007 Facial dynamics as indicators of trustworthiness and cooperative behavior. Emotion 7, 730-735. (doi:10.1037/1528-3542.7.4.730).
78. Stouten, J. & De Cremer, D. 2010 'Seeing is believing': the effects of facial expressions of emotion and verbal communication in social dilemmas. F Behay. Decis. Making 23, 271-287. (doi:10.1002/bdm)
79. Wubben, M. J. J., De Cremer, D. & van Dijk, E. 2011 The communication of anger and disappointment helps to establish cooperation through indirect reciprocity. F. Econ. Psychol. 32, 489-501. (doi:10.1016/j.joep.2011.03.016)
80. Grinevich, V., Brecht, M. & Osten, P. 2005 Monosynaptic pathway from rat vibrissa motor cortex to facial motor neurons revealed by lentivirus-based axonal tracing. Neurosci. 25, 8250-8258. (doi:10.1523/JNEUR-OSCI.2235-05.2005).
81. Hattox, A., Li, Y. & Keller, A. 2003 Serotonin regulates rhythmic whisking. Neuron 39, 343-352. (doi:10.1016/S0896-6273(03)00391-X)
82. van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C. D., Singleton, I., Suzuki, A., Utami, S. S. & Merrill, M. 2003 Orangutan cultures and the evolution of material culture. Science 299, 102-105. (doi:10.1126/science.1078004)
83. Maestripieri, D. & Wallen, K. 1997 Affiliative and submissive communication in rhesus macaques. Primates 38, 127-138. (doi:10.1007/BF02382003).
84. Parr, L. A., Cohen, M. & de Waal, F. 2005 Influence of social context on the use of blended and graded facial displays in chimpanzees. Int. F Primatol. 26, 73-103. (doi:10.1007/s10764-005-0724-z)
85. Bard, K. A., Gaspar, A. D. & S-J, Vick 2011 Chimpanzee faces ender the magnifying glass: emerging methods reveal cross-species similarities and individuality. In Personality and temperment in nonhuman primates (eds A. Weiss et aL), pp. 193-231. New York, NY: Springer.
86. Gaspar, A. 2006 Universals and individuality in facial behavior-past and future of an evolutionary perspective. Acta Ethol. 9, 1-14. (doi:10.1007/s10211-006-0010-x).
87. Brent, L. J. N., Lehmann, J. & Ramos-Fernandez, G. 2011 Social network analysis in the study of nonhuman primates: a historical perspective. Am. F Primatol. 73, 720-730. (doi:10.1002/ajp.20949)
88. Brent, L. J. N., Lehmann, J. & Ramos-Fernandez, G. 2011 Social network analysis in the study of nonhuman primates: a historical perspective. Am. F Primatol. 73, 720-730. (doi:10.1002/ajp.20949)
89. Raleigh, M. J., McGuire, M. T., Brammer, G. L. & Yuwiler, A. 1984 Social and environmental influences on blood serotonin concentrations in monkeys. Arch. Gen. Psych. 41, 405-410. (doi:10.1001/archpsyc.1984.01790150095013)
90. Raleigh, M. J., Brammer, G. L., McGuire, M. T. & Yuwiler, A. 1985 Dominant social status facilitates the behavioral effects of serotonergic agonists. Brain Res. 348, 274-282. (doi:10.1016/0006-8993(85)90445-7).
91. Shively, C. A., Brammer, G. L., Kaplan, J. R., Raleigh, M. J. & Manuck, S. B. 1991 The complex relationship between behavioral attributes, social status, and whole blood serotonin in male Macaca fascicularis. Am. F. Primatol. 23, 99-112. (doi:10.1002/ajp.1350230204)
92. McCall, R. B. & Aghajanian, G. K. 1979 Serotonergic facilitation of facial motoneuron excitation. Brain Res. 169, 11-27. (doi:10.1016/0006-8993(79)90370-6).