Top

Published in:

01-09-2009 | Head and Neck Radiology

Region-specific maturation of cerebral cortex in human fetal brain: diffusion tensor imaging and histology

Authors: Richa Trivedi, Rakesh K. Gupta, Nuzhat Husain, Ram K. S. Rathore, Sona Saksena, Savita Srivastava, Gyanendra K. Malik, Vinita Das, Mandakini Pradhan, Manoj K. Sarma, Chandra M. Pandey, Ponnada A. Narayana

Published in: Neuroradiology | Issue 9/2009

Abstract

Introduction

In this study, diffusion tensor imaging (DTI) and glial fibrillary acidic protein (GFAP) immunohistochemical analysis in different cortical regions in fetal brains at different gestational age (GA) were performed.

Methods

DTI was performed on 50 freshly aborted fetal brains with GA ranging from 12 to 42 weeks to compare age-related fractional anisotropy (FA) changes in different cerebral cortical regions that include frontal, parietal, occipital, and temporal lobes at the level of thalami. GFAP immunostaining was performed and the percentage of GFAP-positive areas was quantified.

Results

The cortical FA values in the frontal lobe peaked at around 26 weeks of GA, occipital and temporal lobes at around 20 weeks, and parietal lobe at around 23 weeks. A significant, but modest, positive correlation (r = 0.31, p = 0.02) was observed between cortical FA values and percentage area of GFAP expression in cortical region around the time period during which the migrational events are at its peak, i.e., GA ≤ 28 weeks for frontal cortical region and GA ≤ 22 weeks for rest of the lobes.

Conclusions

The DTI-derived FA quantification with its GFAP immunohistologic correlation in cortical regions of the various lobes of the cerebral hemispheres supports region-specific migrational and maturational events in human fetal brain.

Meyer G, Schaaps JP, Moreau L, Goffinet AM (2000) Embryonic and early fetal development of the human neocortex. J Neurosci 20:1858–1868PubMed

Kostović I (1990) Structural and histochemical reorganization of the human prefrontal cortex during perinatal and postnatal life. Prog Brain Res 85:223–239. doi:10.1016/S0079-6123(08)62682-5 PubMedCrossRef

Kostovic I, Rakic P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297:441–470. doi:10.1002/cne.902970309 PubMedCrossRef

Rakic P (2003) Developmental and evolutionary adaptation of cortical radial glia. Cereb Cortex 13:541–549. doi:10.1093/cercor/13.6.541 PubMedCrossRef

Rakic P, Kornack DR (2001) Neocortical expansion and elaboration during primate evolution: a view from neuroembryology. In: Falk D, Gibson KR (eds) Evolutionary anatomy of the primate cerebral cortex. Cambridge University Press, Cambridge, pp 30–56

Rakic P (1988) Intrinsic and extrinsic determinants of neocortical parcellation: a radial unit model. In: Rakic P, Singer W (eds) Neurobiology of neocortex. Wiley, New York, pp 5–28

Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62:1–35. doi:10.1016/0006-8993(73)90617-3 PubMedCrossRef

Barkovich AJ (1999) Pediatric neuroimaging. Lippincott Williams & Wilkins, Philadelphia

Kostović I, Judas M, Rados M, Hrabac P (2002) Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb Cortex 12:536–544. doi:10.1093/cercor/12.5.536 PubMedCrossRef

10.

Bignami A, Dahl D (1974) Astrocyte-specific protein and neuroglial differentiation. An immunofluorescence study with antibodies to the glial fibrillary acidic protein. J Comp Neurol 153:27–38. doi:10.1002/cne.901530104 PubMedCrossRef

11.

Bignami A, Dahl D, Rueger DC (1980) Glial fibrillary acidic (GFA) protein in normal neural cells and in pathological conditions. Adv Cell Neurobiol 1:285–310

12.

Eng LF, Vanderhaeghen JJ, Bignami A, Gerstl B (1971) An acidic protein isolated from fibrous astrocytes. Brain Res 28:351–354. doi:10.1016/0006-8993(71)90668-8 PubMedCrossRef

13.

Wilkinson M, Hume R, Strange R, Bell JE (1990) Glial and neuronal differentiation in human fetal brain 9–23 weeks of gestation. Neuropathol Appl Neurobiol 16:193–204. doi:10.1111/j.1365-2990.1990.tb01156.x PubMedCrossRef

14.

Choi BH, Lapham LW (1978) Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopy study. Brain Res 148:295–311. doi:10.1016/0006-8993(78)90721-7 PubMedCrossRef

15.

Roessmann U, Gambetti P (1986) Astrocytes in the developing human brain. An immunohistochemical study. Acta Neuropathol 70:308–313. doi:10.1007/BF00686089 PubMedCrossRef

16.

Brisse H, Fallet C, Sebag G, Nessmann C, Blot P, Hassan M (1997) Supratentorial parenchyma in the developing fetal brain: in vitro MR study with histologic comparison. AJNR Am J Neuroradiol 18:1491–1497PubMed

17.

Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson 111:209–219. doi:10.1006/jmrb.1996.0086 CrossRef

18.

Mukherjee P, McKinstry RC (2006) Diffusion tensor imaging and tractography of human brain development. Neuroimaging Clin N Am 16:19–43. doi:10.1016/j.nic.2005.11.004 PubMedCrossRef

19.

Deipolyi AR, Mukherjee P, Gill K, Henry RG, Partridge SC, Veeraraghavan S, Jin H, Lu Y, Miller SP, Ferriero DM, Vigneron DB, Barkovich AJ (2005) Comparing microstructural and macrostructural development of the cerebral cortex in premature newborns: diffusion tensor imaging versus cortical gyration. Neuroimage 27:579–586. doi:10.1016/j.neuroimage.2005.04.027 PubMedCrossRef

20.

Gupta RK, Hasan KM, Trivedi R, Pradhan M, Das V, Parikh NA, Narayana PA (2005) Diffusion tensor imaging of the developing human cerebrum. J Neurosci Res 81:172–178. doi:10.1002/jnr.20547 PubMedCrossRef

21.

Maas LC, Mukherjee P, Carballido-Gamio J, Veeraraghavan S, Miller SP, Partridge SC, Henry RG, Barkovich AJ, Vigneron DB (2004) Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 22:1134–1140. doi:10.1016/j.neuroimage.2004.02.035 PubMedCrossRef

22.

McKinstry RC, Mathur A, Miller JH, Ozcan A, Snyder AZ, Schefft GL, Almli CR, Shiran SI, Conturo TE, Neil JJ (2002) Radial organization of the developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. Cereb Cortex 12:1237–1243. doi:10.1093/cercor/12.12.1237 PubMedCrossRef

23.

Miller SP, Vigneron DB, Henry RG, Bohland MA, Ceppi-Cozzio C, Hoffman C, Newton N, Partridge JC, Ferriero DM, Barkovich AJ (2002) Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imaging 16:621–632. doi:10.1002/jmri.10205 PubMedCrossRef

24.

Hüppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44:584–590. doi:10.1203/00006450-199810000-00019 PubMedCrossRef

25.

Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR, Akbudak E, Aronovitz JA, Miller JP, Lee BC, Conturo TE (1998) Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209:57–66PubMed

26.

Hasan KM, Narayana PA (2003) Computation of the mean diffusivity, and fractional anisotropy maps without tensor decoding and diagonalization: theoretical analysis and experimental validation. Magn Reson Med 50:589–598. doi:10.1002/mrm.10552 PubMedCrossRef

27.

Saksena S, Rai V, Saraswat VA, Rathore RS, Purwar A, Kumar M, Thomas MA, Gupta RK (2008) Cerebral diffusion tensor imaging and in vivo proton magnetic resonance spectroscopy in patients with fulminant hepatic failure. J Gastroenterol Hepatol 23:e111–e119. doi:10.1111/j.1440-1746.2007.05158.x PubMedCrossRef

28.

Bayer SA, Altman J (2004) Atlas of human central nervous system development (vol 2): the human brain during the third trimester. CRC, New York

29.

Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722. doi:10.1093/brain/120.4.701 PubMedCrossRef

30.

Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time and origin and eventual disposition. Science 183:425–427. doi:10.1126/science.183.4123.425 PubMedCrossRef

31.

Rakic P (1972) Mode of migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61–84. doi:10.1002/cne.901450105 PubMedCrossRef

32.

Levitt P, Rakic P (1980) Immunoperoxidase localization of glial fibrillary acid protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol 193:815–840. doi:10.1002/cne.901930316 PubMedCrossRef

33.

Takahashi T, Misson JP, Caviness VS Jr (1990) Glial process elongation and branching in the developing murine neocortex: a qualitative and quantitative immunohistochemical analysis. J Comp Neurol 302:15–28. doi:10.1002/cne.903020103 PubMedCrossRef

34.

Voigt T (1989) Development of glial cells in the cerebral wall of ferrets: direct tracing of their transformation from radial glia into astrocytes. J Comp Neurol 289:74–88. doi:10.1002/cne.902890106 PubMedCrossRef

35.

Schmechel DE, Rakic P (1979) A Golgi study of radial glial cells in the developing monkey telencephalon: morphogenesis and transformation into astrocytes. Anat Embryol (Berl) 156:115–152. doi:10.1007/BF00300010 CrossRef

36.

Huttenlocher PR, Decourten C (1987) The development of synapses in striate cortex of man. Hum Neurobiol 6:1–9PubMed

37.

Houde O, Tzourio-Mazoyer N (2003) Neural foundations of logical and mathematical cognition. Nat Rev Neurosci 4:507–514. doi:10.1038/nrn1117 PubMedCrossRef

38.

Bourgeois JP, Goldman-Rakic PS, Rakic P (1994) Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4:78–96. doi:10.1093/cercor/4.1.78 PubMedCrossRef

39.

Koenderink MJ, Uylings HB, Mrzljak L (1994) Postnatal maturation of the layer III pyramidal neurons in the human prefrontal cortex: a quantitative Golgi analysis. Brain Res 653:173–182. doi:10.1016/0006-8993(94)90387-5 PubMedCrossRef

40.

Mrzljak L, Uylings HB, Kostovic I, van Eden CG (1992) Prenatal development of neurons in the human prefrontal cortex: II. A quantitative Golgi study. J Comp Neurol 316:485–496. doi:10.1002/cne.903160408 PubMedCrossRef

41.

Huttenlocher PR (1979) Synaptic density in human frontal cortex developmental changes and effects of aging. Brain Res 163:195–205. doi:10.1016/0006-8993(79)90349-4 PubMedCrossRef

42.

Goldman PS, Alexander GE (1977) Maturation of prefrontal cortex in the monkey revealed by local reversible cryogenic depression. Nature 267:613–615. doi:10.1038/267613a0 PubMedCrossRef

43.

Sowell ER, Thompson PM, Tessner KD, Toga AW (2001) Mapping continued brain growth and gray matter density reduction in dorsal frontal cortex: inverse relationships during postadolescent brain maturation. J Neurosci 21:8819–8829PubMed

44.

Chugani HT (1998) Biological basis of emotions: brain systems and brain development. Pediatrics 102:1225–1229PubMed

45.

Jiang S, Xue H, Counsell S, Anjari M, Allsop J, Rutherford M, Rueckert D, Hajnal JV (2007) In-utero three dimension high resolution fetal brain diffusion tensor imaging. Med Image Comput Comput Assist Interv Int Conf Med Image Comput Comput Assist Interv 10:18–26PubMed

46.

Kim DH, Chung S, Vigneron DB, Barkovich AJ, Glenn OA (2008) Diffusion-weighted imaging of the fetal brain in vivo. Magn Reson Med 59:216–220. doi:10.1002/mrm.21459 PubMedCrossRef

Title: Region-specific maturation of cerebral cortex in human fetal brain: diffusion tensor imaging and histology
Authors: Richa Trivedi
Rakesh K. Gupta
Nuzhat Husain
Ram K. S. Rathore
Sona Saksena
Savita Srivastava
Gyanendra K. Malik
Vinita Das
Mandakini Pradhan
Manoj K. Sarma
Chandra M. Pandey
Ponnada A. Narayana
Publication date: 01-09-2009
Publisher: Springer-Verlag
Published in: Neuroradiology / Issue 9/2009
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI: https://doi.org/10.1007/s00234-009-0533-8

At a glance: The STEP trials

Springer Medicine

Region-specific maturation of cerebral cortex in human fetal brain: diffusion tensor imaging and histology

Abstract

Introduction

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 9/2009

Assessment of arcuate fasciculus with diffusion-tensor tractography may predict the prognosis of aphasia in patients with left middle cerebral artery infarcts

Lower fractional anisotropy at the anterior body of the normal-appearing corpus callosum in multiple sclerosis versus symptomatic carotid occlusion

38th Annual Meeting of The Japanese Society of Neuroradiology, 4-5-6 February 2009, Mito, Japan

Percutaneous radio-frequency thermocoagulation of the Gasserian ganglion guided by high-speed real-time CT fluoroscopy

Letter to the editor

European Society of Neuroradiology (ESNR)