Distinct abnormalities of the primate prefrontal cortex caused by ionizing radiation in early or midgestation

Journal of Comparative Neurology

Volumn 521, Issue 5, 2013, Pages 1040-1053

  Selemon, Lynn D ^a   Ceritoglu, Can ^b   Ratnanather, J Tilak ^b   Wang, Lei ^c   Harms, Michael P ^d   Aldridge, Kristina ^e   Begović, Anita ^a   Csernansky, John G ^c   Miller, Michael I ^b   Rakic, Pasko ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Missouri   (United States)

Author keywords

Magnetic resonance imaging; Neurodevelopment; Schizophrenia; Stereology; Thalamocortical

Indexed keywords

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION CORTEX; BRAIN DEVELOPMENT; BRAIN SIZE; CELL COUNT; CELL DENSITY; CORTICAL THICKNESS (BRAIN); EMBRYO; GRAY MATTER; IONIZING RADIATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRENATAL EXPOSURE; PRIORITY JOURNAL; RADIATION EXPOSURE; RHESUS MONKEY; STEREOMETRY;

AGE FACTORS; ANIMALS; BRAIN MAPPING; CELL COUNT; COHORT STUDIES; DISEASE MODELS, ANIMAL; FEMALE; MACACA MULATTA; MAGNETIC RESONANCE IMAGING; MALE; NEURONS; PREFRONTAL CORTEX; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RADIATION INJURIES; RADIATION, IONIZING;

EID: 84873879826     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23217     Document Type: Article

References (66)

1. Algan O, Rakic P. 1997. Radiation-induced, lamina-specific deletions of neurons in the primate visual cortex. J Comp Neurol 38: 355-352.
2. Arndt S, Cohen G, Alliger RJ, Swayze VW 2nd, Andreasen NC. 1991. Problems with ratio and proportion measures of imaged cerebral structures. Psychiatry Res 40: 79-89.
3. Barch DM. 2005. The cognitive neuroscience of schizophrenia. Annu Rev Clin Psychol 1: 321-353.
4. Beg MF, Miller MI, Trouve A, Younes L. 2005. Computing large deformation metric mapping via geodesic flows of diffeomorphisms. Int J Comput Vision 61: 139-157.
5. Breunig JJ, Haydar TF, Rakic P. 2011. Neural stem cells: historical perspective and future prospects. Neuron 70: 614-625.
6. Brown AS, Schaefer CA, Wyatt RJ, Goetz R, Begg MD, Gorman JM, Susser ES. 2000. Maternal exposure to respiratory infections and adult schizophrenia spectrum disorders: a prospective birth cohort study. Schizophr Bull 26: 287-295.
7. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9: 110-122.
8. Carter CS, Perlstein W, Ganguli R, Brar J, Mintun M, Cohen JD. 1998. Functional hypofrontality and working memory dysfunction in schizophrenia. Am J Psychiatry 155: 1285-1287.
9. Caviness VS Jr, Rakic P. 1978. Mechanisms of cortical development: a view from mutations in mice. Annu Rev Neurosci 1: 297-326.
10. Ceritoglu C, Wang L, Selemon LD, Csernansky JG, Miller MI, Ratnanather JT. 2010. Large deformation diffeomorphic metric mapping registration of reconstructed 3D histological section images and in vivo MR images. Front Hum Neurosci 4: 3.
11. Christensen JR, Larsen KB, Lisanby SH, Scalia J, Arango V, Dwork AJ, Pakkenberg B. 2007. Neocortical and hippocampal neuron and glial cell numbers in the rhesus monkey. Anat Rec 290: 330-340.
12. Convit A, Wolf OT, deLeon MJ, Patalinjug M, Kandil E, Caraos C, Scherer A, Saing Louis LA, Cancro R. 2001. Volumetric analysis of the pre-frontal regions: findings in aging and schizophrenia. Psychiatry Res 107: 61-73.
13. Dombrowski SM, Hilgetag CC, Barbas H. 2001. Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb Cortex 11: 975-988.
14. Dorph-Petersen KA, Pierri JN, Wu Q, Sampson AR, Lewis DA. 2007. Primary visual cortex volume and total neuron number are reduced in schizophrenia. J Comp Neurol 501: 290-301.
15. Eidelberg D, Galaburda AM. 1982. Symmetry and asymmetry in the human posterior thalamus. I. Cytoarchitectonic analysis in normal persons. Arch Neurol 39: 325-332.
16. Giguere M, Goldman-Rakic PS. 1988. Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277: 195-213.
17. Goldman-Rakic PS. 1987. Circuitry of the prefrontal cortex and the regulation of behavior by representational knowledge. In: Plum F, Mountcastle V, editors. Handbook of physiology, vol. 5. Bethesda, MD: American Physiological Society. p. 373-417.
18. Goldman-Rakic PS. 1991. Prefrontal cortical dysfunction in schizophrenia: the relevance of working memory. In: Caroll BJ, Barrett JE, editors. Psychopathology and the brain. New York: Raven Press. p 1-23.
19. Goldman-Rakic PS. 1994. Working memory dysfunction in schizophrenia. J Neuropsych Clin Neurosci 4: 348-357.
20. Goldman-Rakic PS, Porrino LJ. 1985. The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242: 535-560.
21. Gundersen HJG. 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: 3-45.
22. Gundersen HJG, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorensen FB, Vesterby A, West MJ. 1988. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96: 379-394.
23. Gundersen HJG, Jensen EBV, Kieu K, Nielsen J. 1999. The efficiency of systematic sampling in stereology - reconsidered. J Microsc 193: 199-211.
24. Gur RE, Cowell PE, Latshaw A, Turetsky BI, Grossman RI, Arnold SE, Bilker WB, Gur RC. 2000. Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. Arch Gen Psychiatry 57: 761-768.
25. Guttlerez-Galve L, Wheeler-Kingshott, CAM, Altmann DR, Price G, Chu EM, Leeson VC, Lobo A, Barker GJ, Barnes TRE, Joyce EM, Ron MA. 2010. Changes in the frontotemporal cortex and cognitive correlates in first episode psychosis. Biol Psychiatry 68: 51-60.
26. Harms MP, Wang L, Campanella C, Aldridge K, Moffitt AJ, Kuelper J, Ratnanather JT, Miller MI, Barch DM, Csernansky JG. 2010. Structural abnormalities in gyri of the prefrontal cortex in individuals with schizophrenia and their unaffected siblings. Br J Psychiatry 196: 50-157.
27. Hollister JM, Laing P, Mednick SA. 1996. Rhesus incompatibility as a risk factor for schizophrenia in male adults. Arch Gen Psychiatry 53: 19-24.
28. Insel BJ, Schaefer CA, McKeague IW, Susser ES, Brown AS. 2008. Maternal iron deficiency and the risk of schizophrenia in offspring. Arch Gen Psychiatry 65: 1136-1144.
29. Jones EG. 1986. Connectivity of the primate sensory-motor cortex. In: Jones EG, Peters A, editors. Cerebral cortex, vol. 5. Sensory-motor areas and aspects of cortical connectivity. New York: Plenum Press. p. 113-183.
30. Joshi SC, Miller MI. 2000 Landmark matching via large deformation diffeomorphisms. IEEE Trans Image Process 9: 1357-1370.
31. Joyner AH, Roddey JC, Bloss CS, Bakken TE, Rimol LM, Melle I, Agartz I, Djurovic S, Topol EJ, Schork NJ, Andreassen OA, Dale AM. 2009. A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations. Proc Natl Acad Sci U S A 106: 15483-15488.
32. Lotfipour S, Ferguson E, Leonard G, Perron M, Pike B, Richer L, Seguin JR, Toro R, Veillette S, Pausova Z, Paus T. 2009. Orbitofrontal cortex and drug use during adolescence. Role of prenatal exposure to maternal smoking and BDNF genotype. Arch Gen Psychiatry 66: 1244-1252.
33. Lopez-Garcia P, Aizenstein HJ, Snitz BE, Walter RP, Carter CS. 2006. Automated ROI-based brain parcellation analysis of frontal and temporal brain volumes in schizophrenia. Psychiatry Res 147: 153-156.
34. Mao Y, Ge X, Frank CL, Madison JM, Koehler AN, Doud MK, Tassa C, Berry EM, Soda T, Singh KK, Biechele T, Petryshen TL, Moon RT, Haggarty SJ, Tsai LH. 2009. DISC1 regulated neural progenitor proliferation via modulation of GSK3β/β-catenin signaling. Cell 136: 1017-1031.
35. Mathalon DH, Sullivan EV, Rawles JM, Pfefferbaum A. 1993. Correction for head size in brain-imaging measurements. Psychiatry Res 50: 121-139.
36. McConnell SK. 1988. Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J Neurosci 8: 945-974.
37. Miller MI, Massie AB, Ratnanather JT, Botteron KN, Csernansky JG. 2000. Bayesian construction of geometrically based cortical thickness metrics. Neuroimage 12: 676-687.
38. Miller MI, Hosakere M, Barker AR, Priebe CE, Lee N, Ratnanather JT, Wang L, Gado M, Morris JC, Csernansky JG. 2003. Labeled cortical mantle distance maps of the cingulate quantify differences between dementia of the Alzheimer type and healthy aging. Proc Natl Acad Sci U S A 100: 15172-15177.
39. Pakkenberg B. 1993. Total nerve cell number in neocortex in chronic schizophrenic and controls estimated using optical disectors Biol Psychiatry 34: 768-772.
40. Pannizzon MS, Fennema-Notestine C, Eyler LT, Jernigan TL, Prom-Wormley E, Neale M, Jacobson K, Lyons MJ, Grant MD, Franz CE, Xian H, Tsuang M, Fischl B, Seidman L, Dale A, Kremen WS. 2009. Distinct genetic influences on cortical surface area and cortical thickness. Cereb Cortex 19: 2728-2735.
41. Rajkowska G, Goldman-Rakic PS. 1995. Cytoarchitectonic definition of prefrontal areas in the normal human cortex. II. Variability in locations of areas 9 and 46 and relationship to the Talairach Coordinate System. Cereb Cortex 5: 323-337.
42. Rakic P. 1988a. Specification of cerebral cortical areas. Science 241: 170-176.
43. Rakic P. 1988b. Defects of neuronal migration and the pathogensis of cortical malformations. Prog Brain Res 73: 15-37.
44. Rakic P. 1995. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18: 383-388.
45. Rakic P, Suner I, Williams RW. 1991. A novel cytoarchitectonic area induced experimentally within primate visual cortex. Proc Natl Acad Sci U S A 88: 2083-2087.
46. Rakic P, Ayoub AE, Breunig JJ, Dominguez MH. 2009. Decision by division: making cortical maps. Trend Neurosci 32: 291-301.
47. Schindler MK, Wang L, Selemon LD, Goldman-Rakic PS, Csernansky JG. 2002. Abnormalities of thalamic volume and shape detected in fetally irradiated rhesus monkeys with high dimensional brain mapping. Biol Psychiatry 51: 827-837.
48. Selemon LD, Rajkowska G, Goldman-Rakic PS. 1995. Abnormally high neuronal density in the schizophrenic cortex: a morphometric analysis of prefrontal area 9 and occipital area 17. Arch Gen Psychiatry 52: 805-818.
49. Selemon LD, Rajkowska G, Goldman-Rakic PS. 1998. Elevated neuronal density in prefrontal area 46 in brains from schizophrenic patients: application of a 3-dimensional, stereologic counting method. J Comp Neurol 392: 402-412.
50. Selemon LD, Mrzljak J, Kleinman JE, Herman MM, Goldman-Rakic PS. 2003. Regional specificity in the neuropathologic substrates of schizophrenia: a morphometric analysis of Broca's area 44 and area 9. Arch Gen Psychiatry 60: 69-77.
51. Selemon LD, Wang L, Nebel MB, Csernansky JG, Goldman-Rakic PS, Rakic P. 2005. Direct and indirect effects of fetal irradiation on cortical gray and white matter volume in the macaque. Biol Psychiatry 57: 83-90.
52. Selemon LD, Begović' A, Rakic P. 2009. Selective reduction of neuronal number and volume of the mediodorsal nucleus of the thalamus in macaques following irradiation at early gestational ages. J Comp Neurol 515: 454-464.
53. Sidman RL, Rakic P. 1973. Neuronal migration, with special reference to developing human brain: a review. Brain Res 62: 1-35.
54. Sinclair WK, Morton RA. 1966. X-ray sensitivity during the cell generation cycle of cultured Chinese hamster cells. Radiat Res 29: 450-474.
55. Stolp HB, Turnquist C, Dziegielewska KM, Saunders NR, Anthony DC, Molnar Z. 2011. Reduced ventricular proliferation in the foetal cortex following maternal inflammation in the mouse. Brain 134: 3236-3248.
56. Stolp H, Neuhaus A, Sundramoorthi R, Monar Z. 2012. The long and short of it: gene and environmental interactions during early cortical development and consequences for long term neurological disease. Front Psychiatry 3: 50.
57. Sullivan EV, Lim KO, Mathalon D, Marsh L, Beal DM, Harris D, Hoff AL, Faustman WO, Pfefferbaum A. 1998. A profile of cortical gray matter volume deficits characteristic of schizophrenia. Cereb Cortex 8: 117-124.
58. Sun D, Stuart GW, Jenkinson M, Wood SJ, McGorry PD, Velakoulis D, van Ert TGM, Thompson PM, Toga AW, Smith DJ, Cannon TD, Pantelis C. 2009. Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Mol Psychiatry 14: 976-986.
59. Suner I, Rakic P. 1996. Numerical relationship between neurons in the lateral geniculate nucleus and primary visual cortex in macaque monkeys. Vis Neurosci 13: 585-590.
60. Susser ES, Lin SP. 1992. Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944-1945. Arch Gen Psychiatry 49: 983-988.
61. Toro R, Leonard G, Lerner JV, Lerner RM, Perron M, Pike GB, Richer L, Veilette S, Pausova Z, Paus T. 2008. Prenatal exposure to maternal cigarette smoking and the adolescent cerebral cortex. Neuropsychopharmacology 33: 1019-1027.
62. Walhovd KB, Moe V, Slinning K, Due-Tonnessen P, Bjornerud A, Dale AM, van der Kouwe A, Quinn BT, Kosofsky B, Greve D, Fischl B. 2007. Volumetric cerebral characteristics of children exposed to opiates and other substances in utero. Neuroimage 36: 1331-1344.
63. Walker AE. 1940. A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73: 59-86.
64. Weinberger DR, Berman KF, Illowsky BP. 1986. Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia: I. Regional cerebral blood flow (rCFB) evidence. Arch Gen Psychiatry 43: 114-124.
65. Zhang Y, Wu Y, Zhu M, Wang C, Wang J, Zhang Y, Yu C, Jiang T. 2011. Reduced cortical thickness in mental retardation. PLoS ONE 6: 329673.
66. Zhou D, Level C, Lepage C, Rasmussen C, Evans A, Wyper K, Pei J, Andrew G, Massey A, Massey D, Beaulieu C. 2011. Developmental cortical thinning in fetal alcohol spectrum disorders. Neuroiamge 58: 16-25.