Postnatal development of the hippocampus in the Rhesus macaque (Macaca mulatta): A longitudinal magnetic resonance imaging study

Hippocampus

Volumn 24, Issue 7, 2014, Pages 794-807

  Hunsaker, Michael R ^a,b,c   Scott, Julia A ^a,b   Bauman, Melissa D ^a,b   Schumann, Cynthia M ^a,b   Amaral, David G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

Hippocampus; Longitudinal development; Magnetic resonance imaging; Primate model; Rhesus macaque

Indexed keywords

ARTICLE; BRAIN ASYMMETRY; BRAIN DEVELOPMENT; BRAIN SIZE; FEMALE; FUNCTIONAL NEUROIMAGING; GROUPS BY AGE; GROWTH RATE; HIPPOCAMPUS; LEFT HEMISPHERE; LONGITUDINAL STUDY; MALE; MONKEY MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RHESUS MONKEY; RIGHT HEMISPHERE; SEX DIFFERENCE; ANIMAL; GROWTH, DEVELOPMENT AND AGING; NEUROIMAGING; ORGAN SIZE; SEXUAL DEVELOPMENT;

ANIMALS; FEMALE; HIPPOCAMPUS; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; NEUROIMAGING; ORGAN SIZE; SEX CHARACTERISTICS;

EID: 84902546597     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22271     Document Type: Article

References (70)

1. Alvarado MC, Bachevalier J. 2005. Selective neurotoxic damage to the hippocampal formation impairs performance of the transverse patterning and location memory tasks in rhesus macaques. Hippocampus 15:118-131.
2. Amaral DG, Bauman MD, Schumann CM. 2003. The amygdala and autism: Implications from non-human primate studies. Genes Brain Behav 2:295-302.
3. Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC. 2011. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54:2033-2044.
4. Avants BB, Yushkevich P, Pluta J, Minkoff D, Korczykowski M, Detre J, Gee JC. 2010. The optimal template effect in hippocampus studies of diseased populations. Neuroimage 49:2457-2466.
5. Bachevalier J, Alvarado MC, Malkova L. 1999. Memory and socioemotional behavior in monkeys after hippocampal damage incurred in infancy or in adulthood. Biol Psychiatry 46:329-339.
6. Bachevalier J, Beauregard M, Alvarado MC. 1999. Long-term effects of neonatal damage to the hippocampal formation and amygdaloid complex on object discrimination and object recognition in rhesus monkeys (Macaca mulatta). Behav Neurosci 113:1127-1151.
7. Bachevalier J, Malkova L. 2006. The amygdala and development of social cognition: Theoretical comment on Bauman, Toscano, Mason, Lavenex, and Amaral (2006). Behav Neurosci 120:989-991.
8. Bauman M, Kemper TL. 1985. Histoanatomic observations of the brain in early infantile autism. Neurology 35:866-874.
9. Bauman MD, Lavenex P, Mason WA, Capitanio JP, Amaral DG. 2004. The development of mother-infant interactions after neonatal amygdala lesions in rhesus monkeys. J Neurosci 24:711-721.
10. Bauman MD, Lavenex P, Mason WA, Capitanio JP, Amaral DG. 2004. The development of social behavior following neonatal amygdala lesions in rhesus monkeys. J Cogn Neurosci 16:1388-1411.
11. Bauman MD, Toscano JE, Babineau BA, Mason WA, Amaral DG. 2008. Emergence of stereotypies in juvenile monkeys (Macaca mulatta) with neonatal amygdala or hippocampus lesions. Behav Neurosci 122:1005-1015.
12. 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.
13. Bauman ML, Kemper TL. 2005. Neuroanatomic observations of the brain in autism: A review and future directions. Int J Dev Neurosci 23:183-187.
14. Casey BJ, Giedd JN, Thomas KM. 2000. Structural and functional brain development and its relation to cognitive development. Biol Psychol 54:241-257.
15. Caviness VSJ, Kennedy DN, Richelme C, Rademacher J, Filipek PA. 1996. The human brain age 7-11 years: A volumetric analysis based on magnetic resonance images. Cereb Cortex 6:726-736.
16. Caviness VSJ, Lange NT, Makris N, Herbert MR, Kennedy DN. 1999. MRI-based brain volumetrics: Emergence of a developmental brain science. Brain Dev 21:289-295.
17. 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.
18. Courchesne E, Karns CM, Davis HR, Ziccardi R, Carper RA, Tigue ZD, Chisum HJ, Moses P, Pierce K, Lord C, Lincoln AJ, Pizzo S, Schreibman L, Haas RH, Akshoomoff NA, Courchesne RY. 2001. Unusual brain growth patterns in early life in patients with autistic disorder: An MRI study. Neurology 57:245-254.
19. Csernansky JG, Joshi S, Wang L, Haller JW, Gado M, Miller JP, Grenander U, Miller MI. 1998. Hippocampal morphometry in schizophrenia by high dimensional brain mapping. Proc Natl Acad Sci USA 95:11406-11411.
20. Deboer T, Wu Z, Lee A, Simon TJ. 2007. Hippocampal volume reduction in children with chromosome 22q11.2 deletion syndrome is associated with cognitive impairment. Behav Brain Funct 3:54.
21. Dierssen M, Vallina IF, Baamonde C, Lumbreras MA, Martinez-Cue C, Calatayud SG, Florez J. 1996. Impaired cyclic AMP production in the hippocampus of a Down syndrome murine model. Brain Res Dev Brain Res 95:122-124.
22. Eckenhoff MF, Rakic P. 1988. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. J Neurosci 8:2729-2747.
23. Eckenhoff MF, Rakic P. 1991. A quantitative analysis of synaptogenesis in the molecular layer of the dentate gyrus in the rhesus monkey. Brain Res Dev Brain Res 64:129-135.
24. Filipek PA, Richelme C, Kennedy DN, Caviness VSJ. 1994. The young adult human brain: An MRI-based morphometric analysis. Cereb Cortex 4:344-360.
25. Franklin MS, Kraemer GW, Shelton SE, Baker E, Kalin NH, Uno H. 2000. Gender differences in brain volume and size of corpus callosum and amygdala of rhesus monkey measured from MRI images. Brain Res 852:263-267.
26. Giedd JN, Castellanos FX, Rajapakse JC, Vaituzis AC, Rapoport JL. 1997. Sexual dimorphism of the developing human brain. Prog Neuropsychopharmacol Biol Psychiatry 21:1185-1201.
27. Giedd JN, Lalonde FM, Celano MJ, White SL, Wallace GL, Lee NR, Lenroot RK. 2009. Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J Am Acad Child Adolesc Psychiatry 48:465-470.
28. Giedd JN, Lenroot RK, Shaw P, Lalonde F, Celano M, White S, Tossell J, Addington A, Gogtay N. 2008. Trajectories of anatomic brain development as a phenotype. Novartis Found Symp 289:101-112; discussion 112.
29. Giedd JN, Raznahan A, Mills KL, Lenroot RK. 2012. Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biol Sex Differ 3:19.
30. Giedd JN, Stockman M, Weddle C, Liverpool M, Alexander-Bloch A, Wallace GL, Lee NR, Lalonde F, Lenroot RK. 2010. Anatomic magnetic resonance imaging of the developing child and adolescent brain and effects of genetic variation. Neuropsychol Rev 20:349-361.
31. 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.
32. Harrison PJ. 1999. The neuropathology of schizophrenia. A critical review of the data and their interpretation. Brain 122:593-624.
33. Hazlett HC, Poe M, Gerig G, Smith RG, Provenzale J, Ross A, Gilmore J, Piven J. 2005. Magnetic resonance imaging and head circumference study of brain size in autism: Birth through age 2 years. Arch Gen Psychiatry 62:1366-1376.
34. Huppi PS, Dubois J. 2006. Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med 11:489-497.
35. Huppi PS, Warfield S, Kikinis R, Barnes PD, Zientara GP, Jolesz FA, Tsuji MK, Volpe JJ. 1998. Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol 43:224-235.
36. Jabes A, Lavenex PB, Amaral DG, Lavenex P. 2010. Quantitative analysis of postnatal fneurogenesis and neuron number in the macaque monkey dentate gyrus. Eur J Neurosci 31:273-285.
37. Jabes A, Lavenex PB, Amaral DG, Lavenex P. 2011. Postnatal development of the hippocampal formation: A stereological study in macaque monkeys. J Comp Neurol 519:1051-1070.
38. Jack CRJ, Petersen RC, Xu Y, O'Brien PC, Smith GE, Ivnik RJ, Boeve BF, Tangalos EG, Kokmen E. 2000. Rates of hippocampal atrophy correlate with change in clinical status in aging and AD. Neurology 55:484-489.
39. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. 2012. FSL. Neuroimage 62:782-790.
40. Kalin NH. 2004. Studying non-human primates: A gateway to understanding anxiety disorders. Psychopharmacol Bull 38(Suppl 1):8-13.
41. Kalin NH, Shelton SE. 1989. Defensive behaviors in infant rhesus monkeys: Environmental cues and neurochemical regulation. Science 243:1718-1721.
42. Keuker JI, Luiten PG, Fuchs E. 2003. Preservation of hippocampal neuron numbers in aged rhesus monkeys. Neurobiol Aging 24:157-165.
43. 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.
44. Lavenex P, Banta Lavenex P, Amaral DG. 2007. Postnatal development of the primate hippocampal formation. Dev Neurosci 29:179-192.
45. Lavenex PB, Amaral DG, Lavenex P. 2006. Hippocampal lesion prevents spatial relational learning in adult macaque monkeys. J Neurosci 26:4546-4558.
46. Lavenex P, Sugden SG, Davis RR, Gregg JP, Banta Lavenex P. 2011. Developmental regulation of gene expression and astrocytic processes may explain selective hippocampal vulnerability. Hippocampus 21:142-149.
47. Lenroot RK, Giedd JN. 2008. The changing impact of genes and environment on brain development during childhood and adolescence: Initial findings from a neuroimaging study of pediatric twins. Dev Psychopathol 20:1161-1175.
48. Leverenz JB, Raskind MA. 1998. Early amyloid deposition in the medial temporal lobe of young Down syndrome patients: A regional quantitative analysis. Exp Neurol 150:296-304.
49. Lipska BK, Weinberger DR. 2002. A neurodevelopmental model of schizophrenia: Neonatal disconnection of the hippocampus. Neurotox Res 4:469-475.
50. Machado CJ, Bachevalier J. 2003. Non-human primate models of childhood psychopathology: the promise and the limitations. J Child Psychol Psychiatry 44:64-87.
51. Malkova L, Heuer E, Saunders RC. 2006. Longitudinal magnetic resonance imaging study of rhesus monkey brain development. Eur J Neurosci 24:3204-3212.
52. 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.
53. Pfluger T, Weil S, Weis S, Vollmar C, Heiss D, Egger J, Scheck R, Hahn K. 1999. Normative volumetric data of the developing hippocampus in children based on magnetic resonance imaging. Epilepsia 40:414-423.
54. Rawlins RG, Kessler MJ. 1986. Demography of free-ranging Cayo Santiago macaques. In: Rawlins RG, Kessler MJ, editors. The Cayo Santiago Macaques: History, Behavior, and Biology. Albany: State University of New York Press.
55. Rawlins RG, Kessler MJ, Turnquist JE. 1984. Reproductive performance, population dynamics and anthropometrics of the free-ranging Cayo Santiago rhesus macaques. J Med Primatol 13:247-259.
56. Raymond GV, Bauman ML, Kemper TL. 1996. Hippocampus in autism: A Golgi analysis. Acta Neuropathol 91:117-119.
57. Saitoh O, Karns CM, Courchesne E. 2001. Development of the hippocampal formation from 2 to 42 years: MRI evidence of smaller area dentata in autism. Brain 124:1317-1324.
58. Schumann CM, Hamstra J, Goodlin-Jones BL, Kwon H, Reiss AL, Amaral DG. 2007. Hippocampal size positively correlates with verbal IQ in male children. Hippocampus 17:486-493.
59. 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.
60. Seress L. 1992. Morphological variability and developmental aspects of monkey and human granule cells: Differences between the rodent and primate dentate gyrus. Epilepsy Res Suppl 7:3-28.
61. Shamy JL, Buonocore MH, Makaron LM, Amaral DG, Barnes CA, Rapp PR. 2006. Hippocampal volume is preserved and fails to predict recognition memory impairment in aged rhesus monkeys (Macaca mulatta). Neurobiol Aging 27:1405-1415.
62. Sowell ER, Thompson PM, Toga AW. 2004a. Mapping changes in the human cortex throughout the span of life. Neuroscientist 10:372-392.
63. Sowell ER, Thompson PM, Leonard CM, Welcome SE, Kan E, Toga AW. 2004b. Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24:8223-8231.
64. Tanaka C, Matsui M, Uematsu A, Noguchi K, Miyawaki T. 2012. Developmental trajectories of the fronto-temporal lobes from infancy to early adulthood in healthy individuals. Dev Neurosci 34:477-487.
65. Thompson DK, Wood SJ, Doyle LW, Warfield SK, Egan GF, Inder TE. 2009. MR-determined hippocampal asymmetry in full-term and preterm neonates. Hippocampus 19:118-123.
66. Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC. 2010. N4ITK: Improved N3 bias correction. IEEE Trans Med Imaging 29:1310-1320.
67. Uecker A, Obrzut JE. 1993. Hemisphere and gender differences in mental rotation. Brain Cogn 22:42-50.
68. Utsunomiya H, Takano K, Okazaki M, Mitsudome A. 1999. Development of the temporal lobe in infants and children: analysis by MR-based volumetry. AJNR Am J Neuroradiol 20:717-723.
69. Wallace GL, Eric Schmitt J, Lenroot R, Viding E, Ordaz S, Rosenthal MA, Molloy EA, Clasen LS, Kendler KS, Neale MC, Giedd JN. 2006. A pediatric twin study of brain morphometry. J Child Psychol Psychiatry 47:987-993.
70. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G. 2006. User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage 31:1116-1128.