Neuronal populations in the basolateral nuclei of the amygdala are differentially increased in humans compared with apes: A stereological study

Journal of Comparative Neurology

Volumn 520, Issue 13, 2012, Pages 3035-3054

  Barger, Nicole ^a   Stefanacci, Lisa ^a   Schumann, Cynthia M ^b   Sherwood, Chet C ^c   Annese, Jacopo ^a   Allman, John M ^d   Buckwalter, Joseph A ^e   Hof, Patrick R ^f,g   Semendeferi, Katerina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^g NEW YORK CONSORTIUM IN EVOLUTIONARY PRIMATOLOGY   (United States)

Author keywords

Amygdala; Ape; Comparative neuroanatomy; Human evolution; Lateral nucleus; Stereology

Indexed keywords

ACCESSORY BASAL AMYGDALA; ADOLESCENT; ADULT; AGED; AMYGDALOID NUCLEUS; ARTICLE; BASAL AMYGDALA; BASOLATERAL AMYGDALA; BRAIN NERVE CELL; CELL COUNT; CELL POPULATION; CENTRAL NUCLEUS (AMYGDALA); CHILD; CHIMPANZEE; COMPARATIVE ANATOMY; CONTROLLED STUDY; FEMALE; GORILLA; HUMAN; HYLOBATIDAE; LATERAL AMYGDALA; MACACA; MALE; NONHUMAN; ORANG UTAN; PRIORITY JOURNAL; SCHOOL CHILD; SPECIES COMPARISON; STEREOMETRY;

ADOLESCENT; ADULT; AGED; AMYGDALA; ANIMALS; BIOLOGICAL EVOLUTION; CELL COUNT; CHILD; FEMALE; HOMINIDAE; HUMANS; MALE; NEURONS; YOUNG ADULT;

EID: 84863583349     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23118     Document Type: Article

References (90)

1. Adolphs R. 2003. Cognitive neuroscience of human social behaviour. Nat Rev Neurosci 4: 165-178.
2. Adolphs R. 2010. What does the amygdala contribute to social cognition? Ann N Y Acad Sci 1191: 42-61.
3. Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, Erwin JM, Park S, Goubert V, Hof PR. 2010. The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct 14: 1-23.
4. Amaral D, Insausti R, Cowan WM. 1987. The entorhinal cortex of the monkey: I. Cytoarchitectonic organization. J Comp Neurol 264: 326-355.
5. Amaral DG, Capitanio JP, Jourdain M, Mason WA, Mendoza SP, Prather M. 2003. The amygdala: is it an essential component of the neural network for social cognition? Neuropsychologia 41: 235-240.
6. Andersen BB, Gundersen HJ. 1999. Pronounced loss of cell nuclei and anisotropic deformation of thick sections. J Microsc 196: 69-73.
7. Barger N, Stefanacci L, Semendeferi K. 2007. A comparative volumetric analysis of the amygdaloid complex and basolateral division in the human and ape brain. Am J Phys Anthropol 134: 392-403.
8. Barton RA, Aggleton JP. 2000. Primate evolution and the amygdala. In: Aggleton JP, editor. The amygdala: a functional analysis, 2nd ed. New York: Oxford University Press. p 480-508.
9. Barton R, Aggleton JP, Grenyer R. 2003. Evolutionary coherence of the mammalian amygdala. Proc Biol Sci 270: 539-543.
10. Bechara A, Damasio H, Damasio AR. 2003. Role of the amygdala in decision-making. Ann N Y Acad Sci 985: 356-369.
11. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A. 2002. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci U S A 99: 11464-11469.
12. Berretta S, Pantazopoulos H, Lange N. 2007. Neuron numbers and volume of the amygdala in subjects diagnosed with bipolar disorder or schizophrenia. Biol Psychiatry 62: 884-893.
13. Bickart KC, Wright CI, Dautoff RJ, Dickerson BC, Barrett LF. 2010. Amygdala volume and social network size in humans. Nat Neurosci 14: 163-164.
14. Brothers L. 1990. The social brain: a project for integrating primate behavior and neurophysiology in a new domain. Concepts Neurosci 1: 27-51.
15. Buckwalter JA, Parvizi J, Morecraft RJ, van Hoesen GW. 2008. Thalamic projections to the posteromedial cortex in the macaque. J Comp Neurol 507: 1709-1733.
16. Byrne RW. 1996. Machiavellian intelligence. Evol Anthropol 5: 172-180.
17. Carlo CN, Stevens CF. 2011. Analysis of differential shrinkage in frozen brain sections and its implications for the use of guard zones in stereology. J Comp Neurol 519: 2803-2810.
18. Carlo CN, Stefanacci L, Semendeferi K, Stevens CF. 2010. Comparative analyses of the neuron numbers and volumes of the amygdaloid complex in Old and New World primates. J Comp Neurol 518: 1176-1198.
19. Delgado RA Jr, Van Schaik CP. 2000. The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): a tale of two islands. Evol Anthropol 9: 201-218.
20. de Olmos JS. 2004. The amygdala. In: Paxinos G, Mai JK, editors. The human nervous system. New York: Elsevier. p 739-868.
21. Dorph-Petersen K-A, Nyengaard JR, Gundersen HJ. 2001. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204: 232-246.
22. Dunbar RIM. 1993. Coevolution of neocortical size, group size and language in humans. Behav Brain Sci 16: 681-693.
23. Dunbar RIM. 1995. Neocortex size and group size in primates: a test of the hypothesis. J Hum Evol 28: 287-296.
24. Freese JL, Amaral DG. 2009. Neuroanatomy of the primate amygdala. In: Whalen PJ, Phelps EA, editors. The human amygdala. New York: The Guilford Press. p 3-42.
25. Galaburda AM, Bellugi U. 2000. V. Multi-level analysis of cortical neuroanatomy in Williams syndrome. J Cogn Neurosci 12( suppl 1): 74-88.
26. Gardella D, Hatton W, Rind H, Rosen G. 2003. Differential tissue shrinkage and compression in the z-axis: implications for optical disector counting in vibratome-, plastic- and cryosections. J Neurosci Methods 124: 45-59.
27. Garland T, Harvey PH, Ives AR. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41: 18-32.
28. Ghashghaei HT, Barbas H. 2002. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115: 1261-1279.
29. Grieve SM, Clark CR, Williams LM, Peduto AJ, Gordon E. 2005. Preservation of limbic and paralimbic structures in aging. Hum Brain Mapp 25: 391-401.
30. Gundersen HJ, Jensen EB, Kiêu K, Nielsen J. 1999. The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193: 199-211.
31. Heimer L, Van Hoesen GW. 2006. The limbic lobe and its output channels: implications for emotional functions and adaptive behavior. Neurosci Biobehav Rev 30: 126-147.
32. Heimer L, de Olmos JS, Alheid GF, Pearson J, Sakamoto N, Shinoda K, Marksteiner J, Switzer RC III. 1999. The human basal forebrain. Part II. In: Bloom FE, Björklund A, Hökfelt T, editors. The primate nervous system, Part III. Vol. 15. Amsterdam: Elsevier. p 57-226.
33. Herrmann E, Call J, Hernàndez-Lloreda MV, Hare B, Tomasello M. 2007. Humans have evolved specialized skills of social cognition: the cultural intelligence hypothesis. Science 317: 1360-1366.
34. Hill KR, Walker RS, Bozicević M, Eder J, Headland T, Hewlett B, Hurtado AM, Marlowe F, Wiessner P, Wood B. 2011. Co-residence patterns in hunter-gatherer societies show unique human social structure. Science 331: 1286-1289.
35. Hill RA, Dunbar RIM. 2003. Social network size in humans. Hum Nat 14: 53-72.
36. Holloway R. 1968. The evolution of the primate brain: some aspects of quantitative relations. Brain Res 7: 121-172.
37. Humphrey NK. 1976. The social function of intellect. In: growing points in ethology. Cambridge: Cambridge University Press. p 303-317.
38. Ichinohe N, Rockland KS. 2005. Distribution of synaptic zinc in the macaque monkey amygdala. J Comp Neurol 489: 135-147.
39. Insausti R, Tunon T, Sobreviela T, Insausti A, Gonzalo L. 1995. The human entorhinal cortex: a cytoarchitectonic analysis. J Comp Neurol 355: 171-198.
40. Jolly A. 1966. Lemur social behavior and primate intelligence. Science 153: 501-506.
41. Kanai R, Bahrami B, Roylance R, Rees G. 2011. Online social network size is reflected in human brain structure. Proc R Soc Lond B Biol Sci 278: 1498-1497.
42. Kano T. 1992. The last ape: pygmy chimpanzee behavior and ecology. Stanford, CA: Stanford University Press.
43. LeDoux J. 2007. The amygdala. Curr Biol 17: R868-R874.
44. Lewis KP, Barton RA. 2006. Amygdala size and hypothalamus size predict social play frequency in nonhuman primates: a comparative analysis using independent contrasts. J Comp Psychol 120: 31-37.
45. MacLean PD. 1949. Psychosomatic disease and the visceral brain: recent developments bearing on the Papez theory of emotion. Psychosom Med 11: 338-353.
46. Maddison WP, Maddison DR. 2010. Mesquite: a modular system for evolutionary analysis. Version 2.73. http://mesquiteproject.org.
47. Malone N, Fuentes A. 2009. The ecology and evolution of hylobatid communities: causal and contextual factors underlying inter-and intraspecific variation. In: Whittaker D, Lappan S, editors. The gibbons. New York: Springer. p 241-264.
48. McNeill D. 1996. Hand and mind: what gestures reveal about thought. Chicago: University of Chicago Press.
49. Merker B. 1983. Silver staining of cell bodies by means of physical development. J Neurosci Methods 9: 235-241.
50. Midford P, Garland T, Jr, Maddison W. 2003. PDAP package of Mesquite.
51. Mitani JC, Amsler SJ. 2003. Social and spatial aspects of male subgrouping in a community of wild chimpanzees. Behaviour 140: 869-884.
52. Morrison SE, Salzman CD. 2010. Re-valuing the amygdala. Curr Opin Neurobiol 20: 221-230.
53. Parr LA, Waller BM, Fugate J. 2005. Emotional communication in primates: implications for neurobiology. Curr Opin Neurobiol 15: 716-720.
54. Pika S. 2008. Gestures of apes and pre-linguistic human children: similar or different? First Lang 28: 116-140.
55. Pika S, Liebal K, Call J, Tomasello M. 2005. Gestural communication of apes. Gesture 5: 41-56.
56. Pitkänen A, Amaral DG. 1998. Organization of the intrinsic connections of the monkey amygdaloid complex: projections originating in the lateral nucleus. J Comp Neurol 398: 431-58.
57. Pitkänen A, Kemppainen S. 2002. Comparison of the distribution of calcium-binding proteins and intrinsic connectivity in the lateral nucleus of the rat, monkey, and human amygdala. Pharmacol Biochem Behav 71: 369-77.
58. Poizner H, Klima ES, Bellugi U. 1990. What the hands reveal about the brain. Cambridge, MA: The MIT Press.
59. Pollick AS, de Waal FBM. 2007. Ape gestures and language evolution. Proc Natl Acad Sci U S A 104: 8184-8189.
60. Price JL, Russchen F, Amaral DG. 1987. The limbic region: II. The amygdaloid complex. In: Björklund A, Hökfelt T, Swanson L, editors. Handbook of chemical neuroanatomy: Vol 5. Integrated systems of the CNS. Amsterdam: Elsevier. p 279-388.
61. Purvis A. 1995. A composite estimate of primate phylogeny. Philos Trans R Soc Lond B Biol Sci 348: 405-421.
62. Rilling JK, Insel TR. 1999. The primate neocortex in comparative perspective using magnetic resonance imaging. J Hum Evol 37: 191-223.
63. Rilling JK, Seligman RA. 2002. A quantitative morphometric comparative analysis of the primate temporal lobe. J Hum Evol 42: 505-533.
64. Rilling JK, Scholz J, Preuss TM, Glasser MF, Errangi BK, Behrens TE. 2011. Differences between chimpanzees and bonobos in neural systems supporting social cognition. Soc Cogn Affect Neurosci 7: 369-379.
65. Rubinow MJ, Juraska JM. 2009. Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: a stereological study. J Comp Neurol 512: 717-725.
66. Sallet J, Mars RB, Noonan MP, Andersson JL, O'Reilly JX, Jbabdi S, Croxson PL, Jenkinson M, Miller KL, Rushworth MFS. 2011. Social network size affects neural circuits in macaques. Science 334: 697-700.
67. Sander D, Grandjean D, Pourtois G, Schwartz S, Seghier ML, Scherer KR, Vuilleumier P. 2005. Emotion and attention interactions in social cognition: brain regions involved in processing anger prosody. Neuroimage 28: 848-58.
68. Schenker NM, Desgouttes A-M, Semendeferi K. 2005. Neural connectivity and cortical substrates of cognition in hominoids. J Hum Evol 49: 547-569.
69. Schumann CM, Amaral DG. 2005. Stereological estimation of the number of neurons in the human amygdaloid complex. J Comp Neurol 491: 320-329.
70. Schumann CM, Amaral DG. 2006. Stereological analysis of amygdala neuron number in autism. J Neurosci 26: 7674-7679.
71. Schumann CM, Bauman MD, Amaral DG. 2011. Abnormal structure or function of the amygdala is a common component of neurodevelopmental disorders. Neuropsychologia 49: 745-759.
72. Semendeferi K, Damasio H. 2000. The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging. J Hum Evol 38: 317-332.
73. Semendeferi K, Damasio H, Frank R, Van Hoesen GW. 1997. The evolution of the frontal lobes: a volumetric analysis based on three-dimensional reconstructions of magnetic resonance scans of human and ape brains. J Hum Evol 32: 375-388.
74. Semendeferi K, Armstrong E, Schleicher A, Zilles K, Van Hoesen GW. 1998. Limbic frontal cortex in hominoids: a comparative study of area 13. Am J Phys Anthropol 106: 129-55.
75. Semendeferi K, Lu A, Schenker N, Damasio H. 2002. Humans and great apes share a large frontal cortex. Nat Neurosci 5: 272-276.
76. Semendeferi K, Barger N, Schenker N. 2010. Brain reorganization in humans and apes. In: Broadfield D, Schick KD, Toth N, Yuan M, editors. The human brain evolving: paleoneurological studies in honor of Ralph L. Holloway. Gosport, IN: Stone Age Institute Press. p 119-156.
77. Sherwood CC, Bauernfeind AL, Bianchi S, Raghanti MA, Hof PR. 2012. Human brain evolution writ large and small. Prog Brain Res 195: 237-254.
78. Shultz S, Dunbar RIM. 2007. The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proc Biol Sci 274: 2429-2436.
79. Sorvari H, Soininen H, Paljärvi L, Karkola K, Pitkänen A. 1995. Distribution of parvalbumin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 360: 185-212.
80. Stefanacci L, Amaral DG. 2002. Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study. J Comp Neurol 451: 301-23.
81. Stephan H, Andy O. 1969. Quantitative comparative neuroanatomy of primates: an attempt at a phylogenetic interpretation. Ann N Y Acad Sci 167: 370-387.
82. Stephan H, Andy O. 1977. Quantitative comparison of the amygdala in insectivores and primates. Acta Anat (Basel) 98: 130-153.
83. Stephan H, Frahm H, Baron G. 1987. Comparison of brain structure volumes in Insectivora and Primates. VII. Amygdaloid components. J Hirnforsch 28: 571.
84. Sugiura M, Kawashima R, Nakamura K, Sato N, Nakamura A, Kato T, Hatano K, Schormann T, Zilles K, Sato K, et al. 2001. Activation reduction in anterior temporal cortices during repeated recognition of faces of personal acquaintances. NeuroImage 13: 877-890.
85. von Bohlen und Halbach O, Unsicker K. 2002. Morphological alterations in the amygdala and hippocampus of mice during ageing. Eur J Neurosci 16: 2434-2440.
86. Ward TS, Rosen GD, von Bartheld CS. 2008. Optical disector counting in cryosections and vibratome sections underestimates particle numbers: effects of tissue quality. Microsc Res Tech 71: 60-68.
87. West MJ. 1993. New stereological methods for counting neurons. Neurobiol Aging 14: 275-285.
88. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
89. Yang TT, Menon V, Eliez S, Blasey C, White CD, Reid AJ, Gotlib IH, Reiss AL. 2002. Amygdalar activation associated with positive and negative facial expressions. Neuroreport 13: 1737-1741.
90. Zhou W-X, Sornette D, Hill RA, Dunbar RIM. 2005. Discrete hierarchical organization of social group sizes. Proc Biol Sci 272: 439-444.