|
|
|
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 117, Issue 3 1031-1047, Copyright © 1993 by Company of Biologists
JOURNAL ARTICLES |
A Ghosh and CJ Shatz
Department of Neurobiology, Stanford University School of Medicine, CA 94305.
During cerebral cortical development, ingrowing axons from different thalamic nuclei select and invade their cortical targets. The selection of an appropriate target is first evident even before thalamic axons grow into the cortical plate: initially axons accumulate and wait below their cortical target area in a zone called the subplate. This zone also contains the first postmitotic neurons of the cerebral cortex, the subplate neurons. Here we have investigated whether subplate neurons are involved in the process of target selection by thalamic axons by ablating them from specific cortical regions at the onset of the waiting period and examining the subsequent thalamocortical axon projection patterns. Subplate neurons were ablated at the onset of the waiting period by intracortical injections of kainic acid. The effect of the ablation on the thalamocortical projection from visual thalamus was examined by DiI-labeling of the LGN days to weeks following the lesion. At two to four weeks post-lesion, times when LGN axons would have normally invaded the cortical plate, the axons remained below the cortical plate and grew past their appropriate cortical target in an anomalous pathway. Moreover, examination of LGN axons at one week post-lesion, a time when they would normally be waiting and branching within the visual subplate, indicated that the axons had already grown past their correct destination. These observations suggest that visual subplate neurons are involved in the process by which LGN axons select and subsequently grow into visual cortex. In contrast, subplate neurons do not appear to play a major role in the initial morphological development of the LGN itself. Subplate ablations did not alter dendritic growth or shapes of LGN projection neurons during the period under study, nor did it prevent the segregation of retinal ganglion cell axons into eye-specific layers. However, the overall size of the LGN was reduced, suggesting that there may be increased cell death of LGN neurons in the absence of subplate neurons. To examine whether subplate neurons beneath other neocortical areas play a similar role in the formation of thalamocortical connections, subplate neurons were deleted beneath auditory cortex at the onset of the waiting period for auditory thalamic axons. Subsequent DiI labeling revealed that in these animals the majority of MGN axons had grown past auditory cortex instead of innervating it. Taken together these observations underscore a general requirement for subplate neurons throughout neocortex in the process of cortical target selection and ingrowth by thalamic axons.(ABSTRACT TRUNCATED AT 400 WORDS)
This article has been cited by other articles:
|
|
 |
|
  W. Kilb, I. L. Hanganu, A. Okabe, B. A. Sava, C. Shimizu-Okabe, A. Fukuda, and H. J. Luhmann Glycine Receptors Mediate Excitation of Subplate Neurons in Neonatal Rat Cerebral Cortex J Neurophysiol, August 1, 2008; 100(2): 698 - 707. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. K. Wagner Progesterone Receptors and Neural Development: A Gap between Bench and Bedside? Endocrinology, June 1, 2008; 149(6): 2743 - 2749. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. G. Wright, G. P. Demyanenko, A. Powell, M. Schachner, L. Enriquez-Barreto, T. S. Tran, F. Polleux, and P. F. Maness Close Homolog of L1 and Neuropilin 1 Mediate Guidance of Thalamocortical Axons at the Ventral Telencephalon J. Neurosci., December 12, 2007; 27(50): 13667 - 13679. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Amiel-Tison, J. Gosselin, and A. Kurjak Three-dimensional/Four-dimensional Ultrasonography to Detect Fetal Brain Damage NeoReviews, October 1, 2007; 8(10): e425 - e434. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Torres-Reveron and M. J. Friedlander Properties of Persistent Postnatal Cortical Subplate Neurons J. Neurosci., September 12, 2007; 27(37): 9962 - 9974. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. Bai, M. Ishida, M. Okabe, and Y. Arimatsu Role of the Protomap and Target-derived Signals in the Development of Intrahemispheric Connections Cereb Cortex, January 1, 2006; 16(1): 124 - 135. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Shimogori and E. A. Grove Fibroblast Growth Factor 8 Regulates Neocortical Guidance of Area-Specific Thalamic Innervation J. Neurosci., July 13, 2005; 25(28): 6550 - 6560. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. J. Volpe Encephalopathy of Prematurity Includes Neuronal Abnormalities Pediatrics, July 1, 2005; 116(1): 221 - 225. [Full Text] [PDF]
|
|
|
|
|
|
A. Madan and W. V. Good Preterm Birth and the Visual System NeoReviews, March 1, 2005; 6(3): e153 - e159. [Full Text] [PDF]
|
|
|
|
|
|
T. E. Inder, S. K. Warfield, H. Wang, P. S. Huppi, and J. J. Volpe Abnormal Cerebral Structure Is Present at Term in Premature Infants Pediatrics, February 1, 2005; 115(2): 286 - 294. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Zhao, E. Forster, X. Chai, and M. Frotscher Different Signals Control Laminar Specificity of Commissural and Entorhinal Fibers to the Dentate Gyrus J. Neurosci., August 13, 2003; 23(19): 7351 - 7357. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Grossberg and A. Seitz Laminar Development of Receptive Fields, Maps and Columns in Visual Cortex: The Coordinating Role of the Subplate Cereb Cortex, August 1, 2003; 13(8): 852 - 863. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Shu, Y. Li, A. Keller, and L. J. Richards The glial sling is a migratory population of developing neurons Development, July 1, 2003; 130(13): 2929 - 2937. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Leingartner, L. J. Richards, R. H. Dyck, C. Akazawa, and D. D.M. O'Leary Cloning and Cortical Expression of Rat Emx2 and Adenovirus-mediated Overexpression to Assess its Regulation of Area-specific Targeting of Thalamocortical Axons Cereb Cortex, June 1, 2003; 13(6): 648 - 660. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Garel, K. Yun, R. Grosschedl, and J. L. R. Rubenstein The early topography of thalamocortical projections is shifted in Ebf1 and Dlx1/2 mutant mice Development, March 14, 2003; 129(24): 5621 - 5634. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Xie, E. Skinner, C. Landry, V. Handley, V. Schonmann, E. Jacobs, R. Fisher, and A. Campagnoni Influence of the Embryonic Preplate on the Organization of the Cerebral Cortex: A Targeted Ablation Model J. Neurosci., October 15, 2002; 22(20): 8981 - 8991. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. F. DeFreitas, P. S. McQuillen, and C. J. Shatz A Novel p75NTR Signaling Pathway Promotes Survival, Not Death, of Immunopurified Neocortical Subplate Neurons J. Neurosci., July 15, 2001; 21(14): 5121 - 5129. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. James Barkovich and R. I. Kuzniecky Gray matter heterotopia Neurology, December 12, 2000; 55(11): 1603 - 1608. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Del Rio, A. Martinez, C. Auladell, and E. Soriano Developmental History of the Subplate and Developing White Matter in the Murine Neocortex. Neuronal Organization and Relationship with the Main Afferent Systems at Embryonic and Perinatal Stages Cereb Cortex, August 1, 2000; 10(8): 784 - 801. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Wickman, C. Karschin, A. Karschin, M. R. Picciotto, and D. E. Clapham Brain Localization and Behavioral Impact of the G-Protein-Gated K+ Channel Subunit GIRK4 J. Neurosci., August 1, 2000; 20(15): 5608 - 5615. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Soria and A. Fairen Cellular Mosaics in the Rat Marginal Zone Define an Early Neocortical Territorialization Cereb Cortex, April 1, 2000; 10(4): 400 - 412. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J. Barkovich, R. Hevner, and R. Guerrini Syndromes of Bilateral Symmetrical Polymicrogyria AJNR Am. J. Neuroradiol., November 1, 1999; 20(10): 1814 - 1821. [Abstract] [Full Text]
|
|
|
|
|
|
F. Aboitiz Feature Article: Evolution of Isocortical Organization. A Tentative Scenario Including Roles of Reelin, p35/cdk5 and the Subplate Zone Cereb Cortex, October 1, 1999; 9(7): 655 - 661. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Mackarehtschian, C. K. Lau, I. Caras, and S. K. McConnell Regional Differences in the Developing Cerebral Cortex Revealed by Ephrin-A5 Expression Cereb Cortex, September 1, 1999; 9(6): 601 - 610. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. C. Noctor, S. L. Palmer, T. Hasling, and S. L. Juliano Interference with the Development of Early Generated Neocortex Results in Disruption of Radial Glia and Abnormal Formation of Neocortical Layers Cereb Cortex, March 1, 1999; 9(2): 121 - 136. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Abbadie, K. Skinner, I. Mitrovic, and A. I. Basbaum Neurons in the dorsal column white matter of the spinal cord: Complex neuropil in an unexpected location PNAS, January 5, 1999; 96(1): 260 - 265. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. S. Lee, J. L. Collins, M. J. Anzivino, E. A. Frankel, and F. Schottler Heterotopic Neurogenesis in a Rat with Cortical Heterotopia J. Neurosci., November 15, 1998; 18(22): 9365 - 9375. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Mann, V. Zhukareva, A. Pimenta, P. Levitt, and J. Bolz Membrane-Associated Molecules Guide Limbic and Nonlimbic Thalamocortical Projections J. Neurosci., November 15, 1998; 18(22): 9409 - 9419. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Sato, T. Hirata, M. Ogawa, and H. Fujisawa Requirement for Early-Generated Neurons Recognized by Monoclonal Antibody Lot1 in the Formation of Lateral Olfactory Tract J. Neurosci., October 1, 1998; 18(19): 7800 - 7810. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. C. Gilmore, T. Ohshima, A. M. Goffinet, A. B. Kulkarni, and K. Herrup Cyclin-Dependent Kinase 5-Deficient Mice Demonstrate Novel Developmental Arrest in Cerebral Cortex J. Neurosci., August 15, 1998; 18(16): 6370 - 6377. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Molnar, R. Adams, A. M. Goffinet, and C. Blakemore The Role of the First Postmitotic Cortical Cells in the Development of Thalamocortical Innervation in the Reeler Mouse J. Neurosci., August 1, 1998; 18(15): 5746 - 5765. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. M. Catalano and C. J. Shatz Activity-Dependent Cortical Target Selection by Thalamic Axons Science, July 24, 1998; 281(5376): 559 - 562. [Abstract] [Full Text]
|
|
|
|
|
|
P.-P. Gao, Y. Yue, J.-H. Zhang, D. P. Cerretti, P. Levitt, and R. Zhou Regulation of thalamic neurite outgrowth by the Eph ligand ephrin-A5: Implications in the development of thalamocortical projections PNAS, April 28, 1998; 95(9): 5329 - 5334. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. A. Compagnone and S. H. Mellon Dehydroepiandrosterone: A potential signalling molecule for neocortical organization during development PNAS, April 14, 1998; 95(8): 4678 - 4683. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Sretavan, E Pure, M. Siegel, and L. Reichardt Disruption of retinal axon ingrowth by ablation of embryonic mouse optic chiasm neurons Science, July 7, 1995; 269(5220): 98 - 101. [Abstract] [PDF]
|
|
|
|
|
|
C De Felipe, R. Pinnock, and S. Hunt Modulation of chemotropism in the developing spinal cord by substance P Science, February 10, 1995; 267(5199): 899 - 902. [Abstract] [PDF]
|
|
|
|
 |
|
 I Fernaud-Espinosa, M Nieto-Sampedro, and P Bovolenta Differential effects of glycosaminoglycans on neurite outgrowth from hippocampal and thalamic neurones J. Cell Sci., January 6, 1994; 107(6): 1437 - 1448. [Abstract] [PDF]
|
|
|
|
|
|
K Sharma, Z Korade, and E Frank Development of specific muscle and cutaneous sensory projections in cultured segments of spinal cord Development, January 5, 1994; 120(5): 1315 - 1323. [Abstract] [PDF]
|
|
|
|
|
|
A. Cahana, T. Escamez, R. S. Nowakowski, N. L. Hayes, M. Giacobini, A. von Holst, O. Shmueli, T. Sapir, S. K. McConnell, W. Wurst, et al. Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization PNAS, May 22, 2001; 98(11): 6429 - 6434. [Abstract] [Full Text] [PDF]
|
|
