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Kanold the Subplate and Early Cortical Circuits NE33CH02-Kanold ARI 14 May 2010 15:44 The Subplate and Early Cortical Circuits Patrick O. Kanold1 and Heiko J. Luhmann2 1Department of Biology, University of Maryland, College Park, Maryland 20742; email: [email protected] 2Institute of Physiology and Pathophysiology, University Medical Center of the Johannes Gutenberg University, D-55128 Mainz, Germany; email: [email protected] Annu. Rev. Neurosci. 2010. 33:23–48 Key Words First published online as a Review in Advance on cerebral cortex, development, plasticity, cortical column, neuronal March 4, 2010 network, connectivity, cell death, neuropeptides, MAP2, The Annual Review of Neuroscience is online at neurotransmitters neuro.annualreviews.org This article’s doi: Abstract 10.1146/annurev-neuro-060909-153244 The developing mammalian cerebral cortex contains a distinct class of Copyright c 2010 by Annual Reviews. cells, subplate neurons (SPns), that play an important role during early All rights reserved development. SPns are the first neurons to be generated in the cerebral 0147-006X/10/0721-0023$20.00 cortex, they reside in the cortical white matter, and they are the first to mature physiologically. SPns receive thalamic and neuromodulatory Annu. Rev. Neurosci. 2010.33:23-48. Downloaded from www.annualreviews.org by Universitat Zurich- Hauptbibliothek Irchel on 12/03/11. For personal use only. inputs and project into the developing cortical plate, mostly to layer 4. Thus SPns form one of the first functional cortical circuits and are required to relay early oscillatory activity into the developing cortical plate. Pathophysiological impairment or removal of SPns profoundly affects functional cortical development. SPn removal in visual cortex prevents the maturation of thalamocortical synapses, the maturation of inhibition in layer 4, the development of orientation selective responses and the formation of ocular dominance columns. SPn removal also alters ocular dominance plasticity during the critical period. Therefore, SPns are a key regulator of cortical development and plasticity. SPns are vul- nerable to injury during prenatal stages and might provide a crucial link between brain injury in development and later cognitive malfunction. 23 NE33CH02-Kanold ARI 14 May 2010 15:44 INTRODUCTION Contents The subplate represents a transient layer in the INTRODUCTION.................. 24 developing cerebral cortex, which is located di- DEVELOPMENTAL ORIGINS rectly under the cortical plate and which con- OF SUBPLATE NEURONS . 24 sists of a heterogeneous neuronal population MORPHOLOGICAL AND according to morphology and neurotransmitter ELECTROPHYSIOLOGICAL identity (Kostovic & Rakic 1980, 1990; Luskin PROPERTIES OF SUBPLATE & Shatz 1985). The subplate plays an important NEURONS....................... 25 role in the pathfinding of corticopetal and cor- THALAMIC INNERVATION, ticofugal axonal projections (Ghosh et al. 1990, CORTICAL MICROCIRCUITRY, McConnell et al. 1989), in the development of AND NEUROMODULATION the cortical columnar architecture (Ghosh & OF SUBPLATE NEURONS . 27 Shatz 1992a, 1994; Kanold 2004; Kanold et al. Subplate Projections ............... 34 2003), in developmental plasticity, and in the THE SUBPLATE: AN ACTIVE maturation of cortical inhibition (Kanold 2009, HUBSTATION.................. 35 Kanold & Shatz 2006). SPns (subplate neurons) ROLE OF THE SUBPLATE IN possess a number of structural and functional REGULATING MATURATION properties, which put them in an ideal position OF CORTICAL INHIBITION to be critically involved in all these develop- (AND EXCITATION) . 36 mental processes, i.e., they show relatively ma- Role of Subplate Neurons in ture electrophysiological properties and they Maturation of Thalamocortical are well interconnected in the developing cor- Synapses....................... 36 tical network (Friauf et al. 1990, Hanganu et al. Role of Subplate Neurons in 2002). Maturation of Cortical In 1994, Allendoerfer and Shatz published Inhibition . 36 a review in Annual Review of Neuroscience ROLE OF THE SUBPLATE IN (Allendoerfer & Shatz 1994) summarizing the SCULPTURING role of the subplate in the development of con- NEOCORTICAL nections between the thalamus and neocortex. ARCHITECTURE Over the past 15 years, we have learned a lot (COLUMNS)..................... 37 more about the function and diverse roles of Role of the Subplate in Area Identity SPns in neocortical development. The present and Radial Unit Formation . 37 review aims to provide a summary of our cur- Role of Subplate Neurons rent knowledge on the development, connec- tivity, function, and plasticity of SPns in the Annu. Rev. Neurosci. 2010.33:23-48. Downloaded from www.annualreviews.org by Universitat Zurich- Hauptbibliothek Irchel on 12/03/11. For personal use only. in Establishing the Functional CorticalArchitecture............ 38 cerebral cortex. ROLE OF THE SUBPLATE IN DEVELOPMENTAL PLASTICITY..................... 39 DEVELOPMENTAL ORIGINS CONSEQUENCES OF EARLY OF SUBPLATE NEURONS HYPOXIA, ISCHEMIA, ETC., Cortical neurons are generated in the ven- ON SUBPLATE tricular zone (VZ). The first postmitotic neu- (DYS-)FUNCTION............... 40 rons are the preplate cells (Bystron et al. 2008) SUMMARY AND PERSPECTIVES . 40 (Table 1). The subsequent rounds of cell divi- sions give rise to neurons forming cortical layers 2–6. Via radial migration, these neurons split 24 Kanold · Luhmann NE33CH02-Kanold ARI 14 May 2010 15:44 Table 1 Subplate neurons across species Species Mouse Rat Cat Primate Human Gestation 19.5 21 65 167 40GW Birth E11–13 E12–15 E24–E30 E38–E43 GW5–6 (visual, somato, (Al-Ghoul & (visual) (somato) (Bayer et al. 1993, auditory) (Del Rio Miller 1989, (Allendoerfer (Kostovic & Rakic Kostovic & Rakic et al. 2000, Price et al. Bayer & Altman et al. 1990, 1980) 1990) 1997, Wood et al. 1990) Luskin & Shatz E43–E45 (Visual) 1992, Zeng et al. 1985) (Kostovic & Rakic 2009) 1980) Waiting E14–P0 (Del Rio et al. E16–17, none E36–E50 E78–E124 GW20–26 2000, Deng & (Catalano et al. (Ghosh & Shatz (Kostovic & Rakic (Hevner 2000, Elberger 2003) 1991, Erzurumlu 1992b) 1984) Kostovic et al. & Jhaveri 1992, 2002, Kostovic & Kageyama & Judas 2002, Robertson 1993) Kostovic & Rakic 1984) Death E18–P21 E20–P30 P0–P28 E104–P7 GW34–41 (0–80%) (McQuillen et al. (Al-Ghoul & (Chun & Shatz (visual) (Kostovic (Kostovic & Rakic 2002, Price et al. Miller 1989, 1989a) & Rakic 1990) 1990, Samuelsen 1997, Torres-Reveron Ferrer et al. 1990, E120–P7 (Somato) et al. 2003) & Friedlander 2007, Robertson et al. (Kostovic & Rakic 2 years (PFC) Wood et al. 1992) 2000) 1990) (Delalle et al. 1997) Birth.%GP 56%–66% 57% 36%–46% 22%–27% 13%–15% Waiting%GP 71%–100% 76%–80% 55%–76 45%–85 50%–65% Death%GP 200% 200% 150% 110% 100%–240% the preplate into two regions, the marginal zone MORPHOLOGICAL AND (containing Cajal-Retzius cells) and the sub- ELECTROPHYSIOLOGICAL plate zone (Figure 1a).Therelativesizeofthe PROPERTIES OF SUBPLATE subplate in comparison to the overlying cortical NEURONS plate varies among species (Aboitiz & Montiel In all mammalian species studied so far, 2007). The subplate is largest in monkeys and SPns are characterized by their relatively ma- humans (Molnar´ et al. 2006), suggesting that ture structural and functional properties. In SPns are not a vestige of earlier neuronal struc- newborn rodents and fetal cats, subplate neu- Annu. Rev. Neurosci. 2010.33:23-48. Downloaded from www.annualreviews.org by Universitat Zurich- Hauptbibliothek Irchel on 12/03/11. For personal use only. tures but rather a key structure enabling radial rons show an extensive axonal and dendritic organization and higher intercortical connec- arborization pattern (Figure 1b) (Friauf et al. tivity (Aboitiz 1999, Aboitiz et al. 2005). SPns 1990; Hanganu et al. 2001, 2002). SPns are have been identified in placental mammals such capable of integrating synaptic inputs over their as rodents, cats, ferrets, primates, and humans large dendritic tree, which in rodents can span (Molnar´ et al. 2006). The existence of a sub- in horizontal and vertical directions over a few plate in marsupials is controversial (Harman hundred micrometers (Figure 1c–e). In hu- et al. 1995, Marotte & Sheng 2000, Reep 2000, man prenatal cortex, the dendrites of SPns Reynolds et al. 1985). Since all experiments may extend up to 1 mm and significantly ex- discussed in this review have been performed ceed the size of the basal dendrites of pyra- on placental animals, we focus on placental midal neurons (Mrzljak et al. 1988, 1992). mammals. Short dendritic spines can be observed on the www.annualreviews.org • The Subplate and Early Cortical Circuits 25 NE33CH02-Kanold ARI 14 May 2010 15:44 dendrites of a subpopulation of SPns (Mrzljak markers (Table 2) (Hoerder-Suabedissen et al. et al. 1988), indicating an excitatory function. 2009, Osheroff & Hatten 2009), but also SPns are characterized not only by their large by their variability in morphological appear- diversity in the expression pattern of molecular ance (Figure 1c–e). On the basis of their a gw 14 gw 18 MZ MZ CP CP E 55 MZ SP CP SP E 45 SP IZ PP IZ IZ E 31/32 SVZ E 30 SVZ PP SVZ SVZ VZ VZ VZ VZ VZ VZ b1b1 b2b2 MZ II/III IV V Annu. Rev. Neurosci. 2010.33:23-48. Downloaded from www.annualreviews.org by Universitat Zurich- Hauptbibliothek Irchel on 12/03/11. For personal use only. VI 100 µm 20 µm SP cdec d e 50 µm 26 Kanold · Luhmann NE33CH02-Kanold ARI 14 May 2010 15:44 somato-dendritic morphology (i.e., the form in the dorso-ventral direction, thereby form- of the soma and the orientation of the den- ing a columnar
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