Fetal sulcation and gyrification in common marmosets (Callithrix jacchus) obtained by ex vivo magnetic resonance imaging

Neuroscience

Volumn 257, Issue , 2014, Pages 158-174

  Sawada, K ^a   Hikishima, K ^b,c   Murayama, A Y ^b,e   Okano, H J ^d   Sasaki, E ^c   Okano, H ^b,e  

^a TSUKUBA INTERNATIONAL UNIVERSITY   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

^d JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e KEIO UNIVERSITY   (Japan)

Author keywords

Basal radial glia; Common marmoset; Gyrification; Non human primates; Outer subventricular zone

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN CORTEX; BRAIN SIZE; CALCARINE SULCUS; CALLITHRIX; CELL STRUCTURE; CONTROLLED STUDY; CORPUS CALLOSUM; CORRELATION COEFFICIENT; EMBRYO; EX VIVO STUDY; FETAL GYRIFICATION; FETAL SULCATION PATTERN; FETUS; FUNCTIONAL NEUROIMAGING; GESTATIONAL AGE; HEART RATE; IMAGE ANALYSIS; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; MORPHOLOGY; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETO-OCCIPITAL SULCUS; PET-MRI SCANNER; PRIORITY JOURNAL; SEX DIFFERENCE; SUBICULUM; SUBVENTRICULAR ZONE;

BASAL RADIAL GLIA; BRG; CAL; CALCARINE SULCUS; CALLOSAL SULCUS; CAS; CC; CENTRAL SULCUS; CGS; CINGULATE SULCUS; CIRCULAR SULCUS; CIRS; COMMON MARMOSET; CORPUS CALLOSUM; CORTICAL PLATE; CP; CS; E; EMBRYONIC DAY; GESTATIONAL WEEK; GI; GW; GYRIFICATION; GYRIFICATION INDEX; HE; HEMATOXYLIN AND EOSIN; HIPPOCAMPAL FISSURE; HIS; LATERAL FISSURE; LF; MAGNETIC RESONANCE IMAGING; MRI; NON-HUMAN PRIMATES; OCCIPITOTEMPORAL SULCUS; OSVZ; OTS; OUTER SUBVENTRICULAR ZONE; PARIETOOCCIPITAL SULCUS; PBS; PD; PE; PETROUS PORTION OF THE TEMPORAL BONE; PH3; PHOSPHATE-BUFFERED SALINE; PHOSPHOHISTONE H3; POS; POSTNATAL DAY; SI; SP; SUBPLATE; SULCATION INDEX; VENTRICULAR ZONE; VZ;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BRAIN MAPPING; CALLITHRIX; CEREBRAL CORTEX; EMBRYO, MAMMALIAN; EYE PROTEINS; FEMALE; FUNCTIONAL LATERALITY; GESTATIONAL AGE; HOMEODOMAIN PROTEINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; T-BOX DOMAIN PROTEINS; TUBULIN;

EID: 84890063993     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.10.067     Document Type: Article

References (64)

1. Armstrong E., Curtis M., Buxhoeveden D.P., Fregoe C., Zilles K., Casanova M.F., McCarthy W.F. Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. Cereb Cortex 1991, 1:426-432.
2. Armstrong E., Schleicher A., Omran H., Curtis M., Zilles K. The ontogeny of human gyrification. Cereb Cortex 1995, 5:56-63.
3. Bonnici H.M., William T., Moorhead J., Stanfield A.C., Harris J.M., Owens D.G., Johnstone E.C., Lawrie S.M. Pre-frontal lobe gyrification index in schizophrenia, mental retardation and comorbid groups: an automated study. Neuroimage 2007, 35:648-654.
4. Caviness V.S., Goto T., Tarui T., Takahashi T., Bhide P.G., Nowakowski R.S. Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb Cortex 2003, 13:592-598.
5. Cheung A.F., Kondo S., Abdel-Mannan O., Chodroff R.A., Sirey T.M., Bluy L.E., Webber N., DeProto J., Karlen S.J., Krubitzer L., Stolp H.B., Saunders N.R., Molnár Z. The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb Cortex 2010, 20:1071-1081.
6. Chi J.G., Dooling E.C., Gilles F.H. Gyral development of the human brain. Ann Neurol 1977, 1:86-93.
7. Dubois J., Benders M., Cachia A., Lazeyras F., Leuchter R.H.V., Sizonenko S.V., Borradori-Tolsa C., Mangin J.F., Hüppi P.S. Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex 2008, 18:1444-1454.
8. Epple G. Comparative studies on vocalization in marmoset monkeys (Hapalidae). Folia Primatol (Basel) 1968, 8:1-40.
9. Fietz S.A., Kelava I., Vogt J., Wilsch-Bräuninger M., Stenzel D., Fish J.L., Corbeil D., Riehn A., Distler W., Nitsch R., Huttner W.B. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 2010, 13:690-699.
10. Fujiyoshi K., Yamada M., Nakamura M., Yamane J., Katoh H., Kitamura K., Kawai K., Okada S., Momoshima S., Toyama Y., Okano H. In vivo tracing of neural tracts in the intact and injured spinal cord of marmosets by diffusion tensor tractography. J Neurosci 2007, 27:11991-11998.
11. Fukunishi K., Sawada K., Kashima M., Sakata-Haga H., Fukuzaki K., Fukui Y. Development of cerebral sulci and gyri in fetuses of cynomolgus monkeys (Macaca fascicularis). Anat Embryol (Berl) 2006, 211:757-764.
12. Fukunishi K., Sawada K., Kashima M., Saito S., Sakata-Haga H., Sukamoto T., Aoki I., Fukui Y. Correlation between formation of the calcarine sulcus and morphological maturation of the lateral ventricle in cynomolgus monkey fetuses. Acta Neurobiol Exp (Wars) 2011, 71:381-386.
13. Hansen D.V., Lui J.H., Parker P.R.L., Kriegstein A.R. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 2010, 464:554-561.
14. Hearn J.P., Abbott D.H., Chambers P.C., Hodges J.K., Lunn S.F. Use of the common marmoset, Callithrix jacchus, in reproductive research. Primates Med 1978, 10:40-49.
15. Herculano-Houzel S., Mota B., Wong P., Kaas J.H. Connectivity-driven white matter scaling and folding in primate cerebral cortex. Proc Natl Acad Sci U S A 2010, 107:19008-19013.
16. Hevner R.F., Haydar T.F. The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis. Cereb Cortex 2012, 22:465-468.
17. Hikishima K., Sawada K., Murayama A., Komaki Y., Kawai K., Sato N., Inoue T., Itoh T., Momoshima S., Iriki A., Okano H.J., Sasaki E., Okano H. Atlas of the developing brain of the marmoset monkey using magnetic resonance histology. Neuroscience 2013, 230:102-113.
18. Hilgetag C.C., Barbas A.H. Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2006, 2:e22.
19. Huang H., Xue R., Zhang J., Ren T., Richards L.J., Yarowsky P., Miller M.I., Mori S. Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J Neurosci 2009, 29:4263-4273.
20. Imai N., Sawada K., Fukunishi K., Sakata-Haga H., Fukui Y. Sexual dimorphism of sulcal length asymmetry in cerebrum of adult cynomolgus monkeys (Macaca fascicularis). Congenit Anom (Kyoto) 2011, 51:161-166.
21. Iwanami A., Yamane J., Katoh H., Nakamura M., Momoshima S., Ishii H., Tanioka Y., Tamaoki N., Nomura T., Toyama Y., Okano H. Establishment of graded spinal cord injury model in a non-human primate: the common marmoset. J Neurosci Res 2005, 80:172-181.
22. Iwanami A., Kaneko S., Nakamura M., Kanemura Y., Mori H., Kobayashi S., Yamasaki M., Momoshima S., Ishii H., Ando K., Tanioka Y., Tamaoki N., Nomura T., Toyama Y., Okano H. Transplantation of human neural stem cells for spinal cord injury in primates. J Neurosci Res 2005, 80:182-190.
23. Kashima M., Sawada K., Fukunishi K., Sakata-Haga H., Tokado H., Fukui Y. Development of cerebral sulci and gyri in fetuses of cynomolgus monkeys (Macaca fascicularis). II. Gross observation of the medial surface. Brain Struct Funct 2008, 212:513-520.
24. Kelava I., Reillo I., Murayama A.Y., Kalinka A.T., Stenzel D., Tomancak P., Matsuzaki F., Lebrand C., Sasaki E., Schwamborn J.C., Okano H., Huttner W.B., Borrell V. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb Cortex 2012, 22:469-481.
25. Kobayashi Y., Okada Y., Itakura G., Iwai H., Nishimura S., Nori S., Hikishima K., Konomi T., Fujiyoshi K., Tsuji O., Toyama Y., Yamanaka S., Nakamura M., Okano H. Human iPSC-derived neural stem cells promote functional recovery after spinal cord injury in common marmosets without tumorigenicity. PLoS ONE 2012, 7:e52787.
26. Kochounov P., Glahn D.C., Fox P., Lancaster J.L., Saleem K., Shelledy W., Zilles K., Thompson P.M., Coulon O., Mangin J.F., Blangero J., Rogers J. Genetics of primary cerebral gyrification: heritability of length, depth and area of primary sulci in an extended pedigree of baboons. Neuroimage 2010, 53:1126-1134.
27. Kriegstein A., Noctor S., Martínez-Cerdeño V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 2006, 7:883-890.
28. Kulynych J.J., Luevano L.F., Jones D.W., Weinberger D.R. Cortical abnormality in schizophrenia: an in vivo application of the gyrification index. Biol Psychiatry 1997, 41:995-999.
29. Levitt J.G., Blanton R.E., Smalley S., Thompson P.M., Guthrie D., McCracken J.T., Sadoun T., Heinichen L., Toga A.W. Cortical sulcal maps in autism. Cereb Cortex 2003, 13:728-735.
30. Lui J.H., Hansen D.V., Kriegstein A.R. Development and evolution of the human neocortex. Cell 2011, 146:18-36.
31. Martínez-Cerdeño V., Cunningham C.L., Camacho J., Antczak J.L., Prakash A.N., Cziep M.E., Walker A.I., Noctor S.C. Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS One 2012, 7:e30178.
32. Naidich T.P., Grant J.L., Altman N., Zimmerman R.A., Birchansky S.B., Braffman B., Daniel J.L. The developing cerebral surface. Preliminary report on the patterns of sulcal and gyral maturation-anatomy, ultrasound, and magnetic resonance imaging. Neuroimaging Clin North Am 1994, 4:201-240.
33. Newman J.D., Kenkel W.M., Aronoff E.C., Bock N.A., Zametkin M.R., Silva A.C. A combined histological and MRI brain atlas of the common marmoset monkey, Callithrix jacchus. Brain Res Rev 2009, 62:1-18.
34. Nonaka-Kinoshita M., Reillo I., Artegiani B., Martínez-Martínez M.Á., Nelson M., Borrell V., Calegari F. Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J 2013, 32:1817-1828.
35. Power R.A., Power M.L., Layne D.G., Jaquish C.E., Oftedal O.T., Tardif S.D. Relations among measures of body composition, age, and sex in the common marmoset monkey (Callithrix jacchus). Comp Med 2001, 51:218-223.
36. Prayer D., Kasprian G., Krampl E., Ulm B., Witzani L., Prayer L., Brugger P.C. MRI of normal fetal brain development. Eur J Radiol 2006, 57:199-216.
37. Rakic P. Neuroscience. Genetic control of cortical convolutions. Science 2004, 303:1983-1984.
38. Reillo I., Borrell V. Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. Cereb Cortex 2012, 22:2039-2054.
39. Richman D.P., Stewart R.M., Hutchinson J.W., Caviness V.S. Mechanical model of brain convolutional development. Science 1975, 189:18-21.
40. Sawada K., Watanabe M. Development of cerebral sulci and gyri in ferrets (Mustela putorius). Congenit Anom (Kyoto) 2012, 52:168-175.
41. Sawada K., Sun X.Z., Fukunishi K., Kashima M., Sakata-Haga H., Tokado H., Aoki I., Fukui Y. Developments of sulcal pattern and subcortical structures of the forebrain in cynomolgus monkey fetuses: 7-tesla magnetic resonance imaging provides high reproducibility of gross structural changes. Brain Struct Funct 2009, 213:469-480.
42. Sawada K., Sun X.-Z., Fukunishi K., Kashima M., Satio S., Sakata-Haga H., Sukamoto T., Aoki I., Fukui Y. Ontogenetic pattern of gyrification in fetuses of cynomolgus monkeys. Neuroscience 2010, 167:735-740.
43. Sawada K., Sun X.-Z., Fukunishi K., Kashima M., Satio S., Aoki I., Sakata-Haga H., Fukui Y. Development of corticocortical long associative fibers in cynomolgus monkey fetal cerebrum analyzed using DTI: its relation to sulcal formation. Adv Studies Biol 2011, 3:133-150.
44. Sawada K., Fukunishi K., Kashima M., Saito S., Aoki I., Fukui Y. Fetal gyrification in cynomolgus monkeys: a concept of developmental stages of gyrification. Anat Rec (Hoboken) 2012, 295:1065-1074.
45. Sawada K., Fukunishi K., Kashima M., Imai N., Saito S., Sakata-Haga H., Aoki I., Fukui Y. Neuroanatomic and MRI references for normal development of cerebral sulci of laboratory primate, cynomolgus monkeys (Macaca fascicularis). Congenit Anom (Kyoto) 2012, 52:16-27.
46. Shitamukai A., Konno D., Matsuzaki F. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 2011, 31:3683-3695.
47. Stahl R., Walcher T., De Juan Romero C., Pilz G.A., Cappello S., Irmler M., Sanz-Aquela J.M., Beckers J., Blum R., Borrell V., Götz M. Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 2013, 153:535-549.
48. Stevenson M.F. Birth and perinatal behaviour in family groups of the common marmoset (Callithrix jacchus jacchus), compared to other primates. J Hum Evol 1976, 5:365-381.
49. Takahashi T., Goto T., Miyama S., Nowakowski R.S., Caviness V.S. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 1999, 19:10357-10371.
50. Tarui T., Takahashi T., Nowakowski R.S., Hayes N.L., Bhide P.G., Caviness V.S. Overexpression of p27 Kip 1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb Cortex 2005, 15:1343-1355.
51. Toro R., Burnod Y. A morphogenetic model for the development of cortical convolutions. Cereb Cortex 2005, 15:1900-1913.
52. Tuoc T.C., Boretius S., Sansom S.N., Pitulescu M.E., Frahm J., Livesey F.J., Stoykova A. Chromatin regulation by BAF170 controls cerebral cortical size and thickness. Dev Cell 2013, 25:256-269.
53. van Essen D.C. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997, 385:313-318.
54. Wang X., Tsai J.W., LaMonica B., Kriegstein A.R. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 2011, 14:555-561.
55. Weiss K., Aldridge K. What stamps the wrinkle on the brow. Evol Anthropol 2003, 12:205-210.
56. Welker W (1990) Why does cerebral cortex fissure and fold? A review of determinations of gyri and sulci. In: Jones EG, Petere A. (Eds.), Comparative structure and evolution of cerebral cortex, Part II, Vol. 8B, pp 3-136. Plenum, New York.
57. Yamada M., Momoshima S., Masutani Y., Fujiyoshi K., Abe O., Nakamura M., Aoki S., Tamaoki N., Okano H. Diffusion-tensor neuronal fiber tractography and manganese-enhanced MR imaging of primate visual pathway in the common marmoset: preliminary results. Radiology 2008, 249:855-864.
58. Yamazaki Y., Echigo C., Saiki M., Inada M., Watanabe S., Iriki A. Tool-use learning by common marmosets (Callithrix jacchus). Exp Brain Res 2011, 213:63-71.
59. Yamazaki Y., Iriki A., Watanabe S. Modulation of physical understanding by common marmosets (Callithrix jacchus). Anim Cogn 2011, 14:175-186.
60. Yuasa S, Nakamura K, Kohsaka S (2010) Stereotaxic atlas of the marmoset brain, Vol. 1. Nissl-stained sections and their diagrams. Japan: National Institute of Neuroscience, National Center of Neurology and Psychiatry.
61. Zhang J., Richards L.J., Yarowsky P., Huang H., van Zijl P.C., Mori S. Three-dimensional anatomical characterization of the developing mouse brain by diffusion tensor microimaging. Neuroimage 2003, 20:1639-1648.
62. Zilles K., Armstrong E., Schleicher A., Kretschmann H.J. The human pattern of gyrification in the cerebral cortex. Anat Embryol (Berl) 1988, 179:173-179.
63. Zilles K., Armstrong E., Moser K.H., Schleicher A., Stephan H. Gyrification in the cerebral cortex of primates. Brain Behav Evol 1989, 34:143-150.
64. Zilles K., Schleicher A., Langemann C., Amunts K., Morosan P., Palomero-Gallagher N., Schormann T., Mohlberg H., Bürgel U., Steinmetz H., Schlaug G., Roland P.E. Quantitative analysis of sulci in the human cerebral cortex: development, regional heterogeneity, gender difference, asymmetry, intersubject variability and cortical architecture. Hum Brain Mapp 1997, 5:218-221.