Selective reduction of neuron number and volume of the mediodorsal nucleus of the thalamus in macaques following irradiation at early gestational ages

Journal of Comparative Neurology

Volumn 515, Issue 4, 2009, Pages 454-464

  Selemon, Lynn D ^a   Begović, Anita ^a   Rakic, Pasko ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anterior nucleus; Neurodevelopment; Pulvinar nucleus; Schizophrenia; Stereology

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL VOLUME; CONTROLLED STUDY; CYTOARCHITECTURE; FEMALE; GESTATIONAL AGE; GLIA; MACACA; MALE; MATURATION; NERVE CELL; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PULVINAR; RADIATION EXPOSURE; THALAMUS DORSOMEDIAL NUCLEUS; X IRRADIATION;

ANALYSIS OF VARIANCE; ANIMALS; CELL COUNT; FEMALE; MACACA MULATTA; MALE; MEDIODORSAL THALAMIC NUCLEUS; NEUROGLIA; NEURONS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RADIATION; STEREOTAXIC TECHNIQUES;

EID: 67650682770     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22078     Document Type: Article

References (68)

1. Abitz M, Damgaard Nielsen R, Jones EG, Laursen H, Graem N, Pakkenberg B. 2007. Excess of neurons in the human newborn mediodorsal thalamus compared with that of the adult. Cereb Cortex 17:2573-2578.
2. Algan O, Rakic P. 1997. Radiation-induced, lamina-specific deletion of neurons in the primate visual cortex. J Comp Neurol 12:335-352.
3. Altman J, Bayer SA. 1979. Development of the diencephalon in the rat. IV. Quantitative study of the time of origin of neurons and the internuclear chronological gradients in the thalamus. J Comp Neurol 188:455-471.
4. Altman J, Bayer SA. 1988. Development of the rat thalamus: II. Time and site of origin and settling pattern of neurons derived from the anterior lobule of the thalamic neuroepithelium. J Comp Neurol 275:378-405.
5. Andreasen NC, Arndt S, Swayze V II, Cizadlo T, Flaum M, O'Leary D, Ehrhardt JC, Yuh WTC. 1994. Thalamic abnormalities in schizophrenia visualized through magnetic resonance image averaging. Science 266: 294-298.
6. Arciniegas D, Rojas DC, Teale P, Sheeder J, Sandberg E, Reite M. 1999. The thalamus and the schizophrenia phenotype: failure to replicate reduced volume. Biol Psychiatry 45:1329-1335.
7. 3H]thymidine autoradiographic analysis of the time of neuron origin in the rhesus monkey. Neuroscience 4:767-778.
8. 3H]thymidine and electron microscopic study. Neuroscience 5:2125-2138.
9. Brown AS, Schaefer CA, Wyatt RJ, Geotz 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.
10. Buchsbaum MS, Someya T, Teng CY, Abel L, Chin S, Najafi A, Haier RJ, Wu J, Bunney WE Jr. 1996. PET and MRI of the thalamus in never medicated patients with schizophrenia. Am J Psychiatry 153:191-199.
11. Byne W, Buchsbaum MS, Kemether E, Hazlett EA, Schinwari A, Mitropoulou V, Siever LJ. 2001. Magnetic resonance imaging of the thalamic mediodorsal nucleus and pulvinar in schizophrenia and schizotypal personality disorder. Arch Gen Psychiatry 58:133-140.
12. Byne W, Buchsbaum MS, Mattiace LA, Hazlett EA, Kemether E, Elhakem SL, Purohit DP, Haroutunian V, Jones L. 2002. Post-mortem assessment of thalamic nucleuar volumes in subjects with schizophrenia. Am J Psychiatry 159:59-65.
13. Chen B, Schaevitz LR, McConnell SK. 2005a. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci U S A 102:17184-17189.
14. Chen JG, Rasin MR, Kwan KY, Sestan N. 2005b. Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc Natl Acad Sci U S A 102:17792-17797.
15. Cholfin JA, Rubenstein JLR. 2007. Patterning of frontal cortex subdivisions by Fgf17. Proc Natl Acad Sci U S A 104:7652-7657.
16. Csernansky JG, Schindler MK, Splinter NR, Wang L, Gado M, Selemon LD, Rastogi-Cruz D, Posener JA, Thompson PA, Miller MI. 2004. Abnormalities of thalamic volume and shape in schizophrenia. Am J Psychiatry 161:896-902.
17. Cullen TJ, Walker MA, Parkinson N, Craven R, Crow TJ, Esiri MM, Harrison PJ. 2003. A postmortem study of the mediodorsal nucleus of the thalamus in schizophrenia. Schizophr Res 60:157-166.
18. Danos P, Baumann B, Bernstein H-G, Stauch R, Krell D, Falkai P, Bogerts B. 2002. The ventral lateral posterior nucleus of the thalamus in schizophrenia: a post-mortem study. Psychiatry Res Neuroimag 114:1-9.
19. Danos P, Baumann B, Karamer A, Bernstein H-G, Stauch R, Krell D, Falkai P, Bogerts B. 2003. Volumes of association thalamic nuclei in schizophrenia: a post-mortem study. Schizophr Res 60:141-155.
20. Danos P, Schmidt A, Baumann B, Bernstein HG, Northoff G, Stauch R, Krell D, Bogerts B. 2005. Volume and neuron number of the mediodorsal thalamic nucleus in schizophrenia: a replication study. Psychiatry Res 140:281-289.
21. Dominguez MH, Rakic P. 2008. Neuroanatomy of the FGF system. J Comp Neurol 509:141-143.
22. Dorph-Petersen KA, Nyengaard JR, Gundersen HJG. 2001. Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204:232-246.
23. Dorph-Petersen KA, Pierri JN, Sun Z, Sampson AR, Lewis DA. 2004. Stereological analysis of the mediodorsal thalamic nucleus in schizophrenia: volume, neuron number, and cell types. J Comp Neurol 472: 449-462.
24. Gilbert AR, Rosenberg DR, Harenski K, Spencer S, Sweeney JA, Keshavan MS. 2001. Thalamic volume in patients with first-episode schizophrenia. Am J Psychiatry 158:618-624.
25. 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.
26. 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.
27. Gundersen HJG, Jensen EBV, Kieǔ K, Nielsen J. 1999. The efficiency of systematic sampling in stereology - reconsidered. J Microsc 193:199-211.
28. Gur RE, Maany V, Mozley PD, Swanson C, Bilker W, Gur RC. 1998. Subcortical MRI volumes in neuroleptic-naïve and treated patients with schizophrenia. Am J Psychiatry 155:1711-1717.
29. Hazlett EA, Buchsbaum MS, Byne W, Wei T-C, Speigel-Cohen J, Geneve C, Kinderlehrer R, Haznedar MM, Shihabuddin L, Siever LJ. 1999. Three-dimensional analysis with MRI and PET of the size, shape, and function of the thalamus in the schizophrenia spectrum. Am J Psychiatry 156:1190-1199.
30. Hollister JM, Laing P, Mednick SA. 1996. Rhesus incompatibility as a risk factor for schizophrenia in male adults. Arch Gen Psychiatry 53:19-24.
31. Innocenti GM, Price DJ. 2005. Exuberance in the development of cortical networks. Nat Rev Neurosci 6:955-965.
32. Kemether EM, Buchsbaum MS, Byne W, Hazlett EA, Haznedar M, Brickman AM, Platholi J, Bloom R. 2003. Magnetic resonance imaging of mediodorsal, pulvinar, and centromedian nuclei of the thalamus in patiens with schizophrenia. Arch Gen Psychiatry 60:983-991.
33. Kordower JH, Rakic P. 1990. Neurogenesis of the magnocellular basal forebrain nuclei in the rhesus monkey. J Comp Neurol 291:637-653.
34. 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 130:678-692.
35. Levitt P, Rakic P. 1982. The time of genesis, embryonic origin and differentiation of the brain stem monoamine neurons in the rhesus monkey. Brain Res Dev Brain Res 4:35-57.
36. Loganovskaja TK, Loganovsky KN. 1999. EEG, cognitive and psychopathological abnormalities in children irradiated in utero. Int J Psychophysiol 34:213-224.
37. Loganovsky KN, Loganovskaja TK. 2000. Schizophrenia spectrum disorders in persons exposed to ionizing radiation as a result of the Chernobyl accident. Schizophr Bull 26:751-773.
38. Loganovsky KN, Loganovskaja TK, Nechayev SY, Antipchuk YY, Bomko MA. 2008. Disrupted development of the dominant hemisphere following prenatal irradiation. J Neuropsychiatry Clin Neurosci 20:274-291.
39. Lotto RB, Asavaritikra P, Vali L, Price DJ. 2001. Target-derived neurotrophic factors regulate the death of developing forebrain neurons after a change in their trophic requirements. J Neurosci 21:3904-3910.
40. Mednick SA, Machon RA, Huttunen MO, Bonnett D. 1988. Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 45:189-192.
41. Miller M, Christensen GE, Amit Y, Grenander U. 1993. Mathematical textbook of deformable neuroanatomies. Proc Natl Acad Sci U S A 90: 11944-11948.
42. Miller M, Banerjee A, Christensen G, Joshi S, Khaneja N, Gernander U, Matejic L. 1997. Statistical methods in computational anatomy. Stat Methods Med Res 6:267-299.
43. Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD. 2005. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47:817-831.
44. Nielsen RE, Abitz M, Pakkenberg B. 2008. Neuron and glial cell numbers in the mediodorsal thalamic nucleus in brains of schizophrenic subjects. Image Anal Stereol 27:133-141.
45. 3H-thymidine autoradiographic and morphometric analyses. Anat Embryol 162:1-20.
46. O'Leary DDM, Borngasser D. 2006. Cortical ventricular zone progenitors and their progeny maintain spatial relationships and radial patterning during preplate development indicating an early protomap. Cereb Cortex Suppl 1:i46-i56.
47. Oppenheim RW. 1991. Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
48. Otake M, Schull WJ, Yoshimaru H. 1991. A review of forty-five years of study of Hiroshima and Nagasaki atomic bomb survivors. Brain damage among the prenatally exposed. J Radiat Res 32(Suppl):249-264.
49. Pakkenberg B. 1990. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry 47:1023-1028
50. Popken GJ, Bunney WE Jr, Potkin SG, Jones EG. 2000. Subnucleus-specific loss of neurons in medial thalamus of schizophrenics Proc Natl Acad Sci U S A 97:9276-9280.
51. Portas CM, Goldstein JM, Shenton ME, Hokama H, Wible CG, Fischer I, Kikinis R, Donnino R, Jolesz FA, McCarley RW. 1998. Volumetric evaluation of the thalamus in schizophrenic male patients using magnetic resonance imaging. Biol Psychiatry 43:649-659.
52. Preuss UW, Zetzsche T, Jager M, Groll C, Frodl T, Bottlender R, Leinsinger G, Hegerl U, Hahn K, Moller HJ, Meisenzahl EM. 2005. Thalamic volume in first-episode and chronic schizophrenic subjects: a volumetric MRI study. Schizophr Res 73:91-101.
53. Rakic P. 1974. Neurons in the monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425-427.
54. Rakic P. 1977a. Genesis of the dorsal lateral geniculate nucleus in the rhesus monkey: site and time of origin, kinetics of proliferation, routes of migration and pattern of distribution of neurons. J Comp Neurol 176:23-52.
55. Rakic P. 1977b. Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond B Biol Sci 278:245-260.
56. Rakic P. 1988. Specification of cerebral cortical areas. Science 241:170-176.
57. Rakic P. 2002. Pre and post-developmental neurogenesis in primates. Clin Neurosci Res 2:29-39.
58. Rakic P, Riley KP. 1983. Regulation of axon numbers in the primate optic nerve by prenatal binocular competition. Nature 305:135-137.
59. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS. 1986. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232:232-235.
60. Schindler M, Wang L, Selemon LD, Goldman-Rakic PS, Rakic P, 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.
61. Selemon LD, Lidow MS, Goldman-Rakic PS. 1999. Increased volume and glial density in primate prefrontal cortex associated with chronic antipsychotic drug exposure. Biol Psychiatry 46:161-172.
62. Selemon LD, Wang L, Nebel MB, Csernansky JG, Goldman-Rakic PS, Rakic P. 2005. Direct and indirect effects of fetal irradiaton on cortical gray and white matter volume in the macaque. Biol Psychiatry 57:83-90.
63. Susser ES, Lin SP. 1992. Schizophrenia after prenatal exposure to the Dutch Hunger Winter of 1944-1945. Arch Gen Psychiatry 49:983-988.
64. Susser ES, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, Gorman JM. 1996. Schizoprenia after prenatal famine. Further evidence. Arch Gen Psychiatry 53:25-31.
65. Tigges J, Gordon TP, McLure HM, Hall EC, Peters A. 1988. Survival rate and life span of rhesus monkeys at the Yerkes Regional Primate Research Center. Am J Primatol 15:263-273.
66. Williams RW, Rakic P. 1988. Elimination of neurons from the rhesus monkey's lateral geniculate nucleus during development. J Comp Neurol 15:424-436.
67. Young KA, Manaye KF, Liang C-L, Hicks PB, German DC. 2000. Reduced number of mediodorsal and anterior thalamic neurons in schizophrenia. Biol Psychiatry 47:900-953.
68. Young KA, Holcomb LA, Yazdani U, Hicks PB, German DC. 2004. Elevated neuron number in the limbic thalamus in major depression. Am J Psychiatry 161:1270-1277.