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Published in: Brain Structure and Function 6/2006

01-11-2006 | Original Article

Development of cerebral sulci and gyri in fetuses of cynomolgus monkeys (Macaca fascicularis)

Authors: K. Fukunishi, K. Sawada, M. Kashima, H. Sakata-Haga, K. Fukuzaki, Y. Fukui

Published in: Brain Structure and Function | Issue 6/2006

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Abstract

This study aimed to clarify the development of sulci and gyri on the external surface of the cerebrum of cynomolgus monkeys. Sulcus formation began with the appearance of the lateral fissure on embryonic day (ED) 70, followed by delineations of four cerebral lobes by the emergence of the parietooccipital sulcus, central sulcus, and preoccipital notch on EDs 80–90. The following primary sulci were then visible until ED 120: the superior temporal sulcus on ED 90; the intraparietal sulcus, lunate sulcus, inferior occipital sulcus, and arcuate sulcus on ED 100; and the principle sulcus on ED 110; the occipitotemporal sulcus, anterior middle temporal sulcus, and superior postcentral dimple on ED 120. These sulci demarcated the superior temporal gyrus on ED 90, the precentral gyrus, supramarginal gyrus, and angular gyrus on ED 100, and the inferior and middle temporal gyri, postocentral gyrus, superior parietal lobule, superior, middle and inferior frontal gyri, and inferior occipital gyrus on ED 120. Except for the intermediate and lateral orbitofrontal sulci, the sulci that appeared on ED 130 and thereafter were not related to the gyrus demarcations. Intriguingly, the brain markedly gained weight on EDs 100 and 120, corresponding to the embryonic ages when almost all gyri were visible. The results suggest that a rapid growth of the cerebrum involves convolutions of the gyri by a regular sequence of the sulcus formation in cynomolgus monkeys. This study further provides a standard of reference for normal development in the cerebral cortical morphology of cynomolgus monkeys.
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Literature
go back to reference Armstrong E, Curtis M, Buxhoeveden DP, Fregoe C, Zilles K, Casanova MF, McCarthy WF (1991) Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. Cereb Cortex 1:426–432PubMedCrossRef Armstrong E, Curtis M, Buxhoeveden DP, Fregoe C, Zilles K, Casanova MF, McCarthy WF (1991) Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. Cereb Cortex 1:426–432PubMedCrossRef
go back to reference Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63PubMedCrossRef Armstrong E, Schleicher A, Omran H, Curtis M, Zilles K (1995) The ontogeny of human gyrification. Cereb Cortex 5:56–63PubMedCrossRef
go back to reference Chiavaras MM, Petrides M (2000) Orbitofrontal sulci of the human and macaque monkey brain. J Comp Neurol 422:35–54PubMedCrossRef Chiavaras MM, Petrides M (2000) Orbitofrontal sulci of the human and macaque monkey brain. J Comp Neurol 422:35–54PubMedCrossRef
go back to reference Dorovini-Zis K, Dolman CL (1977) Gestational development of brain. Arch Pathol Lab Med 101:192–195PubMed Dorovini-Zis K, Dolman CL (1977) Gestational development of brain. Arch Pathol Lab Med 101:192–195PubMed
go back to reference Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury JF, Sebag G, Hassan M (2001) Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. AJNR Am J Neuroradiol 22:184–189PubMed Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury JF, Sebag G, Hassan M (2001) Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. AJNR Am J Neuroradiol 22:184–189PubMed
go back to reference Gilles FH, Gomez IG (2005) Developmental neuropathology of the second half of gestation. Early Hum Dev 81:245–253PubMedCrossRef Gilles FH, Gomez IG (2005) Developmental neuropathology of the second half of gestation. Early Hum Dev 81:245–253PubMedCrossRef
go back to reference Grefkes C, Fink GR (2005) The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3–17PubMedCrossRef Grefkes C, Fink GR (2005) The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3–17PubMedCrossRef
go back to reference Huang CC (1991) Sonographic cerebral sulcal development in premature newborns. Brain Dev 13:27–31PubMed Huang CC (1991) Sonographic cerebral sulcal development in premature newborns. Brain Dev 13:27–31PubMed
go back to reference van der Knaap MS, van Wezel-Meijler G, Barth PG, Barkhof F, Ader HJ, Valk J (1996) Normal gyration and sulcation in preterm and term neonates: appearance on MR images. Radiology 200:389–396PubMed van der Knaap MS, van Wezel-Meijler G, Barth PG, Barkhof F, Ader HJ, Valk J (1996) Normal gyration and sulcation in preterm and term neonates: appearance on MR images. Radiology 200:389–396PubMed
go back to reference Koyama M, Hasegawa I, Osada T, Adachi Y, Nakahara K, Miyashita Y (2004) Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41:795–807PubMedCrossRef Koyama M, Hasegawa I, Osada T, Adachi Y, Nakahara K, Miyashita Y (2004) Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 41:795–807PubMedCrossRef
go back to reference Louw GJ (1989) The development of the sulci and gyri of the bovine cerebral hemispheres. Anat Histol Embryol 18:246–264PubMedCrossRef Louw GJ (1989) The development of the sulci and gyri of the bovine cerebral hemispheres. Anat Histol Embryol 18:246–264PubMedCrossRef
go back to reference Martin RF, Bowden DM (2000) Primate brain maps: structure of the macaque brain. Elsevier, Amsterdam Martin RF, Bowden DM (2000) Primate brain maps: structure of the macaque brain. Elsevier, Amsterdam
go back to reference Martin E, Kikinis R, Zuerrer M, Boesch C, Briner J, Kewitz G, Kaelin P (1988) Developmental stages of human brain: an MR study. J Comput Assist Tomogr 12:917–922PubMedCrossRef Martin E, Kikinis R, Zuerrer M, Boesch C, Briner J, Kewitz G, Kaelin P (1988) Developmental stages of human brain: an MR study. J Comput Assist Tomogr 12:917–922PubMedCrossRef
go back to reference Maudgil DD, Free SL, Sisodiya SM, Lemieux L, Woermann FG, Fish DR, Shorvon SD (1998) Identifying homologous anatomical landmarks on reconstructed magnetic resonance images of the human cerebral cortical surface. J Anat 193:559–571PubMedCrossRef Maudgil DD, Free SL, Sisodiya SM, Lemieux L, Woermann FG, Fish DR, Shorvon SD (1998) Identifying homologous anatomical landmarks on reconstructed magnetic resonance images of the human cerebral cortical surface. J Anat 193:559–571PubMedCrossRef
go back to reference Murphy NP, Rennie J, Cooke RW (1989) Cranial ultrasound assessment of gestational age in low birthweight infants. Arch Dis Child 64:569–572PubMedCrossRef Murphy NP, Rennie J, Cooke RW (1989) Cranial ultrasound assessment of gestational age in low birthweight infants. Arch Dis Child 64:569–572PubMedCrossRef
go back to reference Naidich TP, Yousefzadeh DK, Gusnard DA (1986) Sonography of the normal neonatal head. Supratentorial structures: state-of-the-art imaging. Neuroradiology 28:408–427PubMedCrossRef Naidich TP, Yousefzadeh DK, Gusnard DA (1986) Sonography of the normal neonatal head. Supratentorial structures: state-of-the-art imaging. Neuroradiology 28:408–427PubMedCrossRef
go back to reference Naidich TP, Grant JL, Altman N, Zimmerman RA, Birchansky SB, Braffman B, Daniel JL (1994) The developing cerebral surface. Preliminary report on the patterns of sulcal and gyral maturation—anatomy, ultrasound, and magnetic resonance imaging. Neuroimaging Clin N Am 4:201–240PubMed Naidich TP, Grant JL, Altman N, Zimmerman RA, Birchansky SB, Braffman B, Daniel JL (1994) The developing cerebral surface. Preliminary report on the patterns of sulcal and gyral maturation—anatomy, ultrasound, and magnetic resonance imaging. Neuroimaging Clin N Am 4:201–240PubMed
go back to reference Paxinos G, Huang XF, Toga AW (2000) The Rhesus monkey brain—in stereotaxic coordinates. Academic, San Diego Paxinos G, Huang XF, Toga AW (2000) The Rhesus monkey brain—in stereotaxic coordinates. Academic, San Diego
go back to reference Smart IH, McSherry GM (1986) Gyrus formation in the cerebral cortex in the ferret I Description of the external changes. J Anat 146:141–152PubMed Smart IH, McSherry GM (1986) Gyrus formation in the cerebral cortex in the ferret I Description of the external changes. J Anat 146:141–152PubMed
go back to reference Thompson PM, Schwartz C, Lin RT, Khan AA, Toga AW (1996) Three-dimensional statistical analysis of sulcal variability in the human brain. J Neurosci 16:4261–4274PubMed Thompson PM, Schwartz C, Lin RT, Khan AA, Toga AW (1996) Three-dimensional statistical analysis of sulcal variability in the human brain. J Neurosci 16:4261–4274PubMed
go back to reference Turner OA (1948) Growth and development of the cerebral cortical pattern in man. Arch Neurol Psychiatry 59:1–12PubMed Turner OA (1948) Growth and development of the cerebral cortical pattern in man. Arch Neurol Psychiatry 59:1–12PubMed
go back to reference Weiss K, Aldridge K (2003) What stamps the wrinkle on the brow. Evol Anthropol 12:205–210CrossRef Weiss K, Aldridge K (2003) What stamps the wrinkle on the brow. Evol Anthropol 12:205–210CrossRef
go back to reference Worthen NJ, Gilbertson V, Lau C (1986) Cortical sulcal development seen on sonography: relationship to gestational parameters. J Ultrasound Med 5:153–156PubMed Worthen NJ, Gilbertson V, Lau C (1986) Cortical sulcal development seen on sonography: relationship to gestational parameters. J Ultrasound Med 5:153–156PubMed
go back to reference Zilles K, Armstrong E, Schleicher A, Kretschmann HJ (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol (Berl) 179:173–179CrossRef Zilles K, Armstrong E, Schleicher A, Kretschmann HJ (1988) The human pattern of gyrification in the cerebral cortex. Anat Embryol (Berl) 179:173–179CrossRef
Metadata
Title
Development of cerebral sulci and gyri in fetuses of cynomolgus monkeys (Macaca fascicularis)
Authors
K. Fukunishi
K. Sawada
M. Kashima
H. Sakata-Haga
K. Fukuzaki
Y. Fukui
Publication date
01-11-2006
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 6/2006
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-006-0136-7

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