A Neural Circuit Covarying with Social Hierarchy in Macaques

PLoS Biology

Volumn 12, Issue 9, 2014, Pages

  Noonan, MaryAnn P ^a   Sallet, Jerome ^a   Mars, Rogier B ^a,b   Neubert, Franz X ^a   O'Reilly, Jill X ^b   Andersson, Jesper L ^b   Mitchell, Anna S ^a   Bell, Andrew H ^c   Miller, Karla L ^b   Rushworth, Matthew F S ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; CORPUS STRIATUM; DEFORMATION BASED MORPHOMETRIC; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HYPOTHALAMUS; LEFT HEMISPHERE; MACACA; MALE; MORPHOMETRICS; NEURAL CIRCUIT; NEUROANATOMY; NEUROIMAGING; NON INVASIVE MEASUREMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; QUANTITATIVE ANALYSIS; RAPHE NUCLEUS; RETICULAR FORMATION; SOCIAL COGNITION; SOCIAL DOMINANCE; SOCIAL NETWORK; SOCIAL STATUS; STRUCTURAL MAGNETIC RESONANCE IMAGING; SUPERIOR TEMPORAL SULCUS; ANIMAL; BRAIN MAPPING; EMOTION; MIDBRAIN RAPHE NUCLEUS; NERVE CELL NETWORK; PHYSIOLOGY; PSYCHOLOGY; RHESUS MONKEY; TEMPORAL LOBE;

ANIMALIA; MACACA; MAMMALIA; PRIMATES;

AMYGDALA; ANIMALS; BRAIN MAPPING; CORPUS STRIATUM; EMOTIONS; FEMALE; GRAY MATTER; HIERARCHY, SOCIAL; HYPOTHALAMUS; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; MIDBRAIN RAPHE NUCLEI; NERVE NET; PREFRONTAL CORTEX; TEMPORAL LOBE;

EID: 84920475269     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001940     Document Type: Article

References (72)

1. Chiao JY, (2010) Neural basis of social status hierarchy across species. Curr Opin Neurobiol 20: 803–809.
2. Schulke O, Bhagavatula J, Vigilant L, Ostner J, (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20: 2207–2210.
3. Azzi JC, Sirigu A, Duhamel JR, (2012) Modulation of value representation by social context in the primate orbitofrontal cortex. Proc Natl Acad Sci U S A 109: 2126–2131.
4. Massen JJ, van den Berg LM, Spruijt BM, Sterck EH, (2010) Generous leaders and selfish underdogs: pro-sociality in despotic macaques. PLoS ONE 5: e9734.
5. Klein JT, Shepherd SV, Platt ML, (2009) Social attention and the brain. Curr Biol 19: R958–R962.
6. Fujii N, Hihara S, Nagasaka Y, Iriki A, (2009) Social state representation in prefrontal cortex. Soc Neurosci 4: 73–84.
7. Klein JT, Deaner RO, Platt ML, (2008) Neural correlates of social target value in macaque parietal cortex. Curr Biol 18: 419–424.
8. Raleigh MJ, McGuire MT, Brammer GL, Pollack DB, Yuwiler A, (1991) Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys. Brain Res 559: 181–190.
9. Kumaran D, Melo HL, Duzel E, (2012) The emergence and representation of knowledge about social and nonsocial hierarchies. Neuron 76: 653–666.
10. Quallo MM, Price CJ, Ueno K, Asamizuya T, Cheng K, et al. (2009) Gray and white matter changes associated with tool-use learning in macaque monkeys. Proc Natl Acad Sci U S A 106: 18379–18384.
11. Ashburner J, Friston KJ, (2000) Voxel-based morphometry—the methods. Neuroimage 11: 805–821.
12. Salmond CH, Ashburner J, Vargha-Khadem F, Gadian DG, Friston KJ, (2000) Detecting bilateral abnormalities with voxel-based morphometry. Hum Brain Mapp 11: 223–232.
13. Watkins KE, Vargha-Khadem F, Ashburner J, Passingham RE, Connelly A, et al. (2002) MRI analysis of an inherited speech and language disorder: structural brain abnormalities. Brain 125: 465–478.
14. Bridge H, Cowey A, Ragge N, Watkins K, (2009) Imaging studies in congenital anophthalmia reveal preservation of brain architecture in ‘visual’ cortex. Brain 132: 3467–3480.
15. Sallet J, Mars RB, Noonan MP, Andersson JL, O'Reilly JX, et al. (2011) Social network size affects neural circuits in macaques. Science 334: 697–700.
16. Zumpe D, Michael RP, (1986) Dominance index: a simple measure of relative dominance status in primates. American Journal of Primatology 10: 291–300.
17. Mietchen D, Gaser C, (2009) Computational morphometry for detecting changes in brain structure due to development, aging, learning, disease and evolution. Front Neuroinform 3: 25.
18. Neubert FX, Mars RB, Buch ER, Olivier E, Rushworth MF, (2010) Cortical and subcortical interactions during action reprogramming and their related white matter pathways. Proc Natl Acad Sci U S A 107: 13240–13245.
19. Buch ER, Mars RB, Boorman ED, Rushworth MF, (2010) A network centered on ventral premotor cortex exerts both facilitatory and inhibitory control over primary motor cortex during action reprogramming. J Neurosci 30: 1395–1401.
20. Buch ER, Johnen VM, Nelissen N, O'Shea J, Rushworth MF, (2011) Noninvasive associative plasticity induction in a corticocortical pathway of the human brain. J Neurosci 31: 17669–17679.
21. Mars RB, Klein MC, Neubert FX, Olivier E, Buch ER, et al. (2009) Short-latency influence of medial frontal cortex on primary motor cortex during action selection under conflict. J Neurosci 29: 6926–6931.
22. Davare M, Rothwell JC, Lemon RN, (2010) Causal connectivity between the human anterior intraparietal area and premotor cortex during grasp. Curr Biol 20: 176–181.
23. Davare M, Montague K, Olivier E, Rothwell JC, Lemon RN, (2009) Ventral premotor to primary motor cortical interactions during object-driven grasp in humans. Cortex 45: 1050–1057.
24. Davare M, Lemon R, Olivier E, (2008) Selective modulation of interactions between ventral premotor cortex and primary motor cortex during precision grasping in humans. J Physiol 586: 2735–2742.
25. Hosokawa T, Watanabe M, (2012) Prefrontal neurons represent winning and losing during competitive video shooting games between monkeys. J Neurosci 32: 7662–7671.
26. Baez-Mendoza R, Schultz W, (2013) The role of the striatum in social behavior. Front Neurosci 7: 233.
27. Santos GS, Nagasaka Y, Fujii N, Nakahara H, (2012) Encoding of social state information by neuronal activities in the macaque caudate nucleus. Soc Neurosci 7: 42–58.
28. Yoshida K, Saito N, Iriki A, Isoda M, (2012) Social error monitoring in macaque frontal cortex. Nat Neurosci 15: 1307–1312.
29. Yoshida K, Saito N, Iriki A, Isoda M, (2011) Representation of others' action by neurons in monkey medial frontal cortex. Curr Biol 21: 249–253.
30. Chang SW, Barter JW, Ebitz RB, Watson KK, Platt ML, (2012) Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta). Proc Natl Acad Sci U S A 109: 959–964.
31. Chang SW, Gariepy JF, Platt ML, (2012) Neuronal reference frames for social decisions in primate frontal cortex. Nat Neurosci 16 (2) 243–250.
32. Gordon TP, Bernstein IS, Rose RM, (1978) Social and seasonal influences on testosterone secretion in the male rhesus monkey. Physiol Behav 21: 623–627.
33. Gesquiere LR, Learn NH, Simao MC, Onyango PO, Alberts SC, et al. (2011) Life at the top: rank and stress in wild male baboons. Science 333: 357–360.
34. Murray EA, Wise SP, Drevets WC, (2011) Localization of dysfunction in major depressive disorder: prefrontal cortex and amygdala. Biol Psychiatry 69: e43–54.
35. Doya K, (2008) Modulators of decision making. Nat Neurosci 11: 410–416.
36. Baez-Mendoza R, Harris CJ, Schultz W, (2013) Activity of striatal neurons reflects social action and own reward. Proc Natl Acad Sci U S A 110: 16634–16639.
37. Murray EA, Wise SP, (2010) Interactions between orbital prefrontal cortex and amygdala: advanced cognition, learned responses and instinctive behaviors. Curr Opin Neurobiol 20: 212–220.
38. Izquierdo A, Suda RK, Murray EA, (2005) Comparison of the effects of bilateral orbital prefrontal cortex lesions and amygdala lesions on emotional responses in rhesus monkeys. J Neurosci 25: 8534–8542.
39. Raleigh MJ, Brammer GL, Yuwiler A, Flannery JW, McGuire MT, et al. (1980) Serotonergic influences on the social behavior of vervet monkeys (Cercopithecus aethiops sabaeus). Exp Neurol 68: 322–334.
40. Kerman IA, Enquist LW, Watson SJ, Yates BJ, (2003) Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants. J Neurosci 23: 4657–4666.
41. Izquierdo A, Newman TK, Higley JD, Murray EA, (2007) Genetic modulation of cognitive flexibility and socioemotional behavior in rhesus monkeys. Proc Natl Acad Sci U S A 104: 14128–14133.
42. Dolen G, Darvishzadeh A, Huang KW, Malenka RC, (2013) Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501: 179–184.
43. Saleem K, Logothetis N (2007) A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates. San Diego, CA: Elsevier/Academic Press.
44. Paxinos G, Huang X-F, Petrides M, Toga A (2008) The rhesus monkey brain in stereotaxic coordinates. San Diego, CA: Elsevier/Academic Press.
45. Bauman MD, Toscano JE, Mason WA, Lavenex P, Amaral DG, (2006) The expression of social dominance following neonatal lesions of the amygdala or hippocampus in rhesus monkeys (Macaca mulatta). Behav Neurosci 120: 749–760.
46. Teicher MH, Anderson CM, Polcari A, (2012) Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci U S A 109: E563–E572.
47. Uno H, Tarara R, Else JG, Suleman MA, Sapolsky RM, (1989) Hippocampal damage associated with prolonged and fatal stress in primates. J Neurosci 9: 1705–1711.
48. Sapolsky RM, (1992) Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology 17: 701–709.
49. Mars RB, Neubert FX, Noonan MP, Sallet J, Toni I, et al. (2012) On the relationship between the “default mode network” and the “social brain”. Front Hum Neurosci 6: 189.
50. Silk J, Cheney D, Seyfarth R, (2013) A practical guide to the study of social relationships. Evol Anthropol 22: 213–225.
51. Sallet J, Mars RB, Noonan MP, Neubert FX, Jbabdi S, et al. (2013) The organization of dorsal frontal cortex in humans and macaques. J Neurosci 33: 12255–12274.
52. Mars RB, Sallet J, Neubert FX, Rushworth MF, (2013) Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex. Proc Natl Acad Sci U S A 110: 10806–10811.
53. Rushworth MF, Mars RB, Sallet J, (2013) Are there specialized circuits for social cognition and are they unique to humans? Curr Opin Neurobiol 23 (3) 436–442.
54. Mars RB, Sallet J, Schuffelgen U, Jbabdi S, Toni I, et al. (2011) Connectivity-based subdivisions of the human right “temporoparietal junction area”: evidence for different areas participating in different cortical networks. Cereb Cortex 22 (8) 1894–1903.
55. Behrens TE, Hunt LT, Rushworth MF, (2009) The computation of social behavior. Science 324: 1160–1164.
56. Frith CD, Frith U, (2007) Social cognition in humans. Curr Biol 17: R724–R732.
57. Kumaran D, Maguire EA, (2005) The human hippocampus: cognitive maps or relational memory? J Neurosci 25: 7254–7259.
58. Seo H, Lee D, (2008) Cortical mechanisms for reinforcement learning in competitive games. Philos Trans R Soc Lond B Biol Sci 363: 3845–3857.
59. Seo H, Barraclough DJ, Lee D, (2007) Dynamic signals related to choices and outcomes in the dorsolateral prefrontal cortex. Cereb Cortex 17 Suppl 1: i110–i117.
60. Seyfarth RM, Silk JB, Cheney DL, (2012) Variation in personality and fitness in wild female baboons. Proc Natl Acad Sci U S A 109: 16980–16985.
61. Wilkinson RG, (1999) Health, hierarchy, and social anxiety. Ann N Y Acad Sci 896: 48–63.
62. Fedigan LM (1992) Primates paradigms: sex roles and social bonds. Chicago: University of Chicago Press.
63. Mars RB, Jbabdi S, Sallet J, O'Reilly JX, Croxson PL, et al. (2011) Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J Neurosci 31: 4087–4100.
64. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, et al. (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1: S208–S219.
65. Frey S, Pandya DN, Chakravarty MM, Bailey L, Petrides M, et al. (2011) An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space). Neuroimage 55: 1435–1442.
66. Chakravarty MM, Frey S, Collins DL (2008) Digital atlas of the monkey brain in stereotactic co-ordinates. In: Paxinos G, Huang XF, Petrides M, Toga AW, editors. The rhesus monkey brain in stereotactic coordinates. Amsterdam: Elsevier.
67. Jenkinson M, Bannister P, Brady M, Smith S, (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17: 825–841.
68. Jenkinson M, Smith S, (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5: 143–156.
69. Andersson JLR, Jenkinson M, Smith S (2007) Non-linear optimisation. FMRIB Technical Report TR07JA1 TR07JA1.
70. Andersson JLR, Jenkinson M, Smith S (2007) Non-linear registration, aka Spatial normalisation. FMRIB Technical Report. TR07JA2 TR07JA2.
71. Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, et al. (1999) Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 18: 712–721.
72. Smith SM, Nichols TE, (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44: 83–98.