Postnatal development of the amygdala: A stereological study in macaque monkeys

Journal of Comparative Neurology

Volumn 520, Issue 9, 2012, Pages 1965-1984

  Chareyron, Loïc J ^a   Lavenex, Pamela Banta ^a   Amaral, David G ^b   Lavenex, Pierre ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amygdaloid complex; Anxiety; Astrocytes; Autism; Emotion; Fear; Neurodevelopmental disorders; Neurons; Neuropil; Oligodendrocytes; Schizophrenia; Social behavior

Indexed keywords

ACCESSORY BASAL NUCLEUS; AMYGDALOID NUCLEUS; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BASAL AMYGDALA; BRAIN DEVELOPMENT; BRAIN GROWTH; BRAIN MATURATION; BRAIN SIZE; CELL COUNT; CENTRAL NUCLEUS (AMYGDALA); CONTROLLED STUDY; LATERAL AMYGDALA; MACACA MULATTA; MEDIAL AMYGDALA; NERVE CELL NETWORK; NONHUMAN; OLIGODENDROGLIA; PARALAMINAR NUCLEUS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; STEREOLOGY;

AGE FACTORS; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; FEMALE; MACACA MULATTA; MALE; NEUROGLIA; NEURONS; STEREOTAXIC TECHNIQUES;

EID: 84859517425     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23023     Document Type: Article

References (79)

1. Aliashkevich AF, Yilmazer-Hanke D, Van Roost D, Mundhenk B, Schramm J, Blumcke I. 2003. Cellular pathology of amygdala neurons in human temporal lobe epilepsy. Acta Neuropathol 106: 99-106.
2. Amaral DG, Price JL, Pitkänen A, Carmichael ST. 1992. Anatomical organization of the primate amygdaloid complex. In: Aggleton J, editor. The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss. p 1-66.
3. Arisi GM, Foresti ML, Mukherjee S, Shapiro LA. 2011. The role of olfactory stimulus in adult mammalian neurogenesis. Behav Brain Res [Epub ahead of print].
4. Aroniadou-Anderjaska V, Fritsch B, Qashu F, Braga MF. 2008. Pathology and pathophysiology of the amygdala in epileptogenesis and epilepsy. Epilepsy Res 78: 102-116.
5. Baron-Cohen S, Ring HA, Bullmore ET, Wheelwright S, Ashwin C, Williams SC. 2000. The amygdala theory of autism. Neurosci Biobehav Rev 24: 355-364.
6. Berdel B, Morys J, Maciejewska B. 1997a. Neuronal changes in the basolateral complex during development of the amygdala of the rat. Int J Dev Neurosci 15: 755-765.
7. Berdel B, Morys J, Maciejewska B, Dziewiatkowski J. 1997b. Volume and topographical changes of the basolateral complex during the development of the rat's amygdaloid body. Folia Morphol (Warsz) 56: 1-11.
8. Bernier PJ, Parent A. 1998a. The anti-apoptosis bcl-2 proto-oncogene is preferentially expressed in limbic structures of the primate brain. Neuroscience 82: 635-640.
9. Bernier PJ, Parent A. 1998b. Bcl-2 protein as a marker of neuronal immaturity in postnatal primate brain. J Neurosci 18: 2486-2497.
10. 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.
11. 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.
12. Bourgeois JP, Rakic P. 1993. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13: 2801-2820.
13. Bourgeois JP, Goldman-Rakic PS, Rakic P. 1994. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4: 78-96.
14. Bouwmeester H, Smits K, Van Ree JM. 2002a. Neonatal development of projections to the basolateral amygdala from prefrontal and thalamic structures in rat. J Comp Neurol 450: 241-255.
15. Bouwmeester H, Wolterink G, van Ree JM. 2002b. Neonatal development of projections from the basolateral amygdala to prefrontal, striatal, and thalamic structures in the rat. J Comp Neurol 442: 239-249.
16. 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.
17. Cavedo E, Boccardi M, Ganzola R, Canu E, Beltramello A, Caltagirone C, Thompson PM, Frisoni GB. 2011. Local amygdala structural differences with 3T MRI in patients with Alzheimer disease. Neurology 76: 727-733.
18. Chareyron LJ, Banta Lavenex P, Amaral DG, Lavenex P. 2011. Stereological analysis of the rat and monkey amygdala. J Comp Neurol [Epub ahead of print].
19. Courchesne E, Chisum HJ, Townsend J, Cowles A, Covington J, Egaas B, Harwood M, Hinds S, Press GA. 2000. Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. Radiology 216: 672-682.
20. Decampo D, Fudge J. 2012. Where and what is the paralaminar nucleus? A review on a unique and frequently overlooked area of the primate amygdala. Neurosci Biobehav Rev 36: 520-535.
21. Drevets WC. 2003. Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci 985: 420-444.
22. Fitting S, Booze RM, Hasselrot U, Mactutus CF. 2008. Differential long-term neurotoxicity of HIV-1 proteins in the rat hippocampal formation: a design-based stereological study. Hippocampus 18: 135-147.
23. Fowler CD, Liu Y, Ouimet C, Wang Z. 2002. The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51: 115-128.
24. Fudge JL. 2004. Bcl-2 immunoreactive neurons are differentially distributed in subregions of the amygdala and hippocampus of the adult macaque. Neuroscience 127: 539-556.
25. Giedd JN, Vaituzis AC, Hamburger SD, Lange N, Rajapakse JC, Kaysen D, Vauss YC, Rapoport JL. 1996. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol 366: 223-230.
26. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL. 1999. Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2: 861-863.
27. Grady MS, Charleston JS, Maris D, Witgen BM, Lifshitz J. 2003. Neuronal and glial cell number in the hippocampus after experimental traumatic brain injury: analysis by stereological estimation. J Neurotrauma 20: 929-941.
28. Gundersen HJ. 1986. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 143( Pt 1): 3-45.
29. Gundersen HJ. 1988. The nucleator. J Microsc 151( Pt 1): 3-21.
30. Gundersen HJ, Jensen EB. 1987. The efficiency of systematic sampling in stereology and its prediction. J Microsc 147( Pt 3): 229-263.
31. Hamidi M, Drevets WC, Price JL. 2004. Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry 55: 563-569.
32. Humphrey T. 1968. The development of the human amygdala during early embryonic life. J Comp Neurol 132: 135-165.
33. Ichinohe N, Hayashi M, Wakabayashi K, Rockland KS. 2009. Distribution and progression of amyloid-beta deposits in the amygdala of the aged macaque monkey, and parallels with zinc distribution. Neuroscience 159: 1374-1383.
34. Jabès A, Banta Lavenex P, Amaral DG, Lavenex P. 2010. Quantitative analysis of postnatal neurogenesis and neuron number in the macaque monkey dentate gyrus. Eur J Neurosci 31: 273-285.
35. Jabès A, Banta Lavenex P, Amaral DG, Lavenex P. 2011. Postnatal development of the hippocampal formation: a stereological study in macaque monkeys. J Comp Neurol 519: 1051-1070.
36. Jagalska-Majewska H, Wojcik S, Dziewiatkowski J, Luczynska A, Kurlapska R, Morys J. 2003. Postnatal development of the basolateral complex of rabbit amygdala: a stereological and histochemical study. J Anat 203: 513-521.
37. Kalin NH, Shelton SE, Davidson RJ. 2004. The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J Neurosci 24: 5506-5515.
38. Kalmar JH, Wang F, Chepenik LG, Womer FY, Jones MM, Pittman B, Shah MP, Martin A, Constable RT, Blumberg HP. 2009. Relation between amygdala structure and function in adolescents with bipolar disorder. J Am Acad Child Adolesc Psychiatry 48: 636-642.
39. Kim MJ, Loucks RA, Palmer AL, Brown AC, Solomon KM, Marchante AN, Whalen PJ. 2011. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res 223: 403-410.
40. Knickmeyer RC, Gouttard S, Kang C, Evans D, Wilber K, Smith JK, Hamer RM, Lin W, Gerig G, Gilmore JH. 2008. A structural MRI study of human brain development from birth to 2 years. J Neurosci 28: 12176-12182.
41. Kordower JH, Piecinski P, Rakic P. 1992. Neurogenesis of the amygdaloid nuclear complex in the rhesus monkey. Brain Res Dev Brain Res 68: 9-15.
42. Kreczmanski P, Heinsen H, Mantua V, Woltersdorf F, Masson T, Ulfig N, Schmidt-Kastner R, Korr H, Steinbusch HW, Hof PR, Schmitz C. 2007. Volume, neuron density and total neuron number in five subcortical regions in schizophrenia. Brain 130( Pt 3): 678-692.
43. Lavenex P, Steele MA, Jacobs LF. 2000a. The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. Eur J Neurosci 12: 643-648.
44. Lavenex P, Steele MA, Jacobs LF. 2000b. Sex differences, but no seasonal variations in the hippocampus of food-caching squirrels: a stereological study. J Comp Neurol 425: 152-166.
45. Lavenex P, Banta Lavenex P, Bennet JL, Amaral DG. 2009. Postmortem changes in the neuroanatomical characteristics of the primate brain: hippocampal formation. J Comp Neurol 512: 27-51.
46. Lawrie SM, Whalley HC, Job DE, Johnstone EC. 2003. Structural and functional abnormalities of the amygdala in schizophrenia. Ann N Y Acad Sci 985: 445-460.
47. Luzzati F, Peretto P, Aimar P, Ponti G, Fasolo A, Bonfanti L. 2003. Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci U S A 100: 13036-13041.
48. Luzzati F, Bonfanti L, Fasolo A, Peretto P. 2009. DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex 19: 1028-1041.
49. Malkova L, Heuer E, Saunders RC. 2006. Longitudinal magnetic resonance imaging study of rhesus monkey brain development. Eur J Neurosci 24: 3204-3212.
50. Marlatt MW, Philippens I, Manders E, Czeh B, Joels M, Krugers H, Lucassen PJ. 2011. Distinct structural plasticity in the hippocampus and amygdala of the middle-aged common marmoset (Callithrix jacchus). Exp Neurol 230: 291-301.
51. Mizukami S, Nishizuka M, Arai Y. 1983. Sexual difference in nuclear volume and its ontogeny in the rat amygdala. Exp Neurol 79: 569-575.
52. Morris JA, Jordan CL, Breedlove SM. 2008. Sexual dimorphism in neuronal number of the posterodorsal medial amygdala is independent of circulating androgens and regional volume in adult rats. J Comp Neurol 506: 851-859.
53. Mosconi MW, Cody-Hazlett H, Poe MD, Gerig G, Gimpel-Smith R, Piven J. 2009. Longitudinal study of amygdala volume and joint attention in 2- to 4-year-old children with autism. Arch Gen Psychiatry 66: 509-516.
54. Nave KA. 2010. Myelination and support of axonal integrity by glia. Nature 468: 244-252.
55. O'Kusky J, Colonnier M. 1982. Postnatal changes in the number of astrocytes, oligodendrocytes, and microglia in the visual cortex (area 17) of the macaque monkey: a stereological analysis in normal and monocularly deprived animals. J Comp Neurol 210: 307-315.
56. Okuda H, Tatsumi K, Makinodan M, Yamauchi T, Kishimoto T, Wanaka A. 2009. Environmental enrichment stimulates progenitor cell proliferation in the amygdala. J Neurosci Res 87: 3546-3553.
57. Ostby Y, Tamnes CK, Fjell AM, Westlye LT, Due-Tonnessen P, Walhovd KB. 2009. Heterogeneity in subcortical brain development: a structural magnetic resonance imaging study of brain maturation from 8 to 30 years. J Neurosci 29: 11772-11782.
58. Palackal T, Neuringer M, Sturman J. 1993. Laminar analysis of the number of neurons, astrocytes, oligodendrocytes and microglia in the visual cortex (area 17) of 6- and 12-month-old rhesus monkeys fed a human infant soy-protein formula with or without taurine supplementation from birth. Dev Neurosci 15: 54-67.
59. Payne C, Machado CJ, Bliwise NG, Bachevalier J. 2010. Maturation of the hippocampal formation and amygdala in Macaca mulatta: a volumetric magnetic resonance imaging study. Hippocampus 20: 922-935.
60. Pfefferbaum A, Mathalon DH, Sullivan EV, Rawles JM, Zipursky RB, Lim KO. 1994. A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. Arch Neurol 51: 874-887.
61. 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: 431-458.
62. Price JL, Russchen FT, Amaral DG. 1987. The limbic region. II: The amygdaloid complex. In: Björklund A, Hökfelt T, Swanson LW, editors. Handbook of chemical neuroanatomy. Vol. 5. Integrated systems of the CNS. Part I. Amsterdam: Elsevier. p 279-388.
63. 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.
64. Schumann CM, Amaral DG. 2006. Stereological analysis of amygdala neuron number in autism. J Neurosci 26: 7674-7679.
65. Schumann CM, Hamstra J, Goodlin-Jones BL, Lotspeich LJ, Kwon H, Buonocore MH, Lammers CR, Reiss AL, Amaral DG. 2004. The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci 24: 6392-6401.
66. Schumann CM, Barnes CC, Lord C, Courchesne E. 2009. Amygdala enlargement in toddlers with autism related to severity of social and communication impairments. Biol Psychiatry 66: 942-949.
67. Shapiro LA, Ng K, Zhou QY, Ribak CE. 2009. Subventricular zone-derived, newly generated neurons populate several olfactory and limbic forebrain regions. Epilepsy Behav 14 Suppl 1: 74-80.
68. Tottenham N, Sheridan MA. 2009. A review of adversity, the amygdala and the hippocampus: a consideration of developmental timing. Front Hum Neurosci 3: 68.
69. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, Thompson KR, Gradinaru V, Ramakrishnan C, Deisseroth K. 2011. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471: 358-362.
70. Ulfig N, Setzer M, Bohl J. 2003. Ontogeny of the human amygdala. Ann N Y Acad Sci 985: 22-33.
71. Usher J, Leucht S, Falkai P, Scherk H. 2010. Correlation between amygdala volume and age in bipolar disorder - a systematic review and meta-analysis of structural MRI studies. Psychiatry Res 182: 1-8.
72. Vereecken TH, Vogels OJ, Nieuwenhuys R. 1994. Neuron loss and shrinkage in the amygdala in Alzheimer's disease. Neurobiol Aging 15: 45-54.
73. Wakefield CL, Levine MS. 1985. Early postnatal development of basolateral amygdala in kitten: a Golgi morphometric analysis. Brain Res Bull 14: 159-167.
74. West MJ, Gundersen HJ. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296: 1-22.
75. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231: 482-497.
76. Yachnis AT, Roper SN, Love A, Fancey JT, Muir D. 2000. Bcl-2 immunoreactive cells with immature neuronal phenotype exist in the nonepileptic adult human brain. J Neuropathol Exp Neurol 59: 113-119.
77. Yang TT, Simmons AN, Matthews SC, Tapert SF, Frank GK, Max JE, Bischoff-Grethe A, Lansing AE, Brown G, Strigo IA, Wu J, Paulus MP. 2010. Adolescents with major depression demonstrate increased amygdala activation. J Am Acad Child Adolesc Psychiatry 49: 42-51.
78. Zehr JL, Todd BJ, Schulz KM, McCarthy MM, Sisk CL. 2006. Dendritic pruning of the medial amygdala during pubertal development of the male Syrian hamster. J Neurobiol 66: 578-590.
79. Zhang XM, Cai Y, Chu Y, Chen EY, Feng JC, Luo XG, Xiong K, Struble RG, Clough RW, Patrylo PR, Kordower JH, Yan XX. 2009. Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat 3: 17.