DOCSLIB.ORG

Review: Cortical Construction in Autism Spectrum Disorder: Columns, Connectivity and the Subplate

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Review: Cortical Construction in Autism Spectrum Disorder: Columns, Connectivity and the Subplate Neuropathology and Applied Neurobiology (2016), 42, 115–134 doi: 10.1111/nan.12227 Review: Cortical construction in autism spectrum disorder: columns, connectivity and the subplate J. J. Hutsler* and M. F. Casanova† *Department of Psychology, Program in Neuroscience, University of Nevada, Reno, and †Department of Psychiatry and Behavioral Science, University of Louisville School of Medicine, Louisville, USA J. J. Hutsler and M. F. Casanova (2016) Neuropathology and Applied Neurobiology Cortical construction in autism spectrum disorder: columns, connectivity and the subplate The cerebral cortex undergoes protracted maturation terize autism. These alterations to cortical circuitry likely during human development and exemplifies how biology underlie the behavioural phenotype in autism and con- and environment are inextricably intertwined in the con- tribute to the unique pattern of deficits and strengths that struction of complex neural circuits. Autism spectrum characterize cognitive functioning. Recent findings within disorders are characterized by a number of pathological the cortical subplate may indicate that alterations to changes arising from this developmental process. These cortical construction begin prenatally, before activity- include: (i) alterations to columnar structure that have dependent connections are established, and are in need of significant implications for the organization of cortical cir- further study. A better understanding of cortical develop- cuits and connectivity; (ii) alterations to synaptic spines ment in autism spectrum disorders will draw bridges on individual cortical units that may underlie specific between the microanatomical computational circuitry types of connectional changes; and (iii) alterations within and the atypical behaviours that arise when that circuitry the cortical subplate, a region that plays a role in proper is modified. In addition, it will allow us to better exploit the cortical development and in regulating interregional com- constructional plasticity within the brain to design more munication in the mature brain. Although the cerebral targeted interventions that better manage atypical corti- cortex is not the only structure affected in the disorder, it is cal construction and that can be applied very early in post- a fundamental contributor to the behaviours that charac- natal life. Keywords: cerebral cortex, neurodevelopment, neuropathology, prenatal and its delayed maturation is associated with a flexible Introduction neurocomputational architecture that is open to a wide The human cerebral cortex occupies a unique place variety of early environmental influences [6,7]. It is, within the organization of the nervous system. Its posi- perhaps, the structure in the brain that best demonstrates tion, development and evolution provide the base upon how biology and environment are inextricably inter- which complex cognitive functions are established. The twined in the construction of the complex neural circuits organization of this multilayered sheet of tissue reflects that underpin our success and behavioural flexibility as a both its evolutionary and developmental history [1–4]. species [8,9]. Relative to the other components of the central nervous In developmental disorders where cognitive abilities are system, its expansion in human primates is remarkable [5] significantly impaired, the origin of the problem is often readily apparent in the atypical organization of the cer- Correspondence: Jeffrey J. Hutsler, Department of Psychology, ebral cortex [10,11]. In contrast, pervasive developmental Program in Neuroscience, University of Nevada, MS 296, 1664 N. Virginia Ave., Reno, NV 89557-0296, USA. Tel: +1 775 682 8694; disorders, such as autism, often show a remarkably intact Fax: +1 775 784 1126; E-mail: [email protected] cortical organization upon casual microscopic examina- © 2015 British Neuropathological Society 115 116 J. J. Hutsler and M. F. Casanova tion [12–14], although a number of subtle pathological afferent and efferent connections, their distribution of changes have been described [15]. Intensified efforts to neurones and their spatial expression of neuroactive pro- understand the organization of the cortex in autism spec- teins and peptides. Cortical layers can be described based trum disorder (ASD), along with numerous advances in upon their cellular content, their afferent and efferent quantitative microscopy, have revealed a litany of differ- connections, and the timing of maturation during neural ence from neurotypical (NT) subjects. While the cerebral development. Much like other neuronal structures, these cortex is not the only structure within the brain to be layers are not independent of one another, but are bound impacted by autism, its protracted development leaves it together and brought into functional registration by vulnerable to the shaping influences of earlier develop- columns of cells that traverse the layers [27,28]. mental events. Indeed, the very behaviours that are Single columns of cells share similarities in their required for a diagnosis of autism are largely dependent response properties [28,29] and are visually distinguish- on cortical functioning. able in many areas of cortex as vertical clusters of neu- The behavioural phenotype in ASD is not solely charac- rones separated from neighbouring minicolumns by a cell terized by deficits in cognitive functions. Rather, individu- sparse neuropil space. The sharing of response character- als with ASD often show better performance on many istics between spatially adjacent columns arises naturally types of cognitive tasks. These include embedded figures from the types of inputs that a cortical region receives, tasks, block design tasks and visual search [16–18]. In along with the fundamental rules that guide activity- addition to these simple tasks, 5% to 10% of the ASD dependent strengthening and weakening of connections population present with islands of ability that are remark- between neural units [6,7,30,31]. Neurones within a able in quality [19]. In the context of the present discus- minicolumn share a developmental history [32,33] and sion, these findings suggest that the cortex in autism may be the basis upon which evolutionary selection cannot be simply portrayed as abnormal or atypical. has acted to modify the computational architecture Rather, the organization of the cerebral cortex, and its [2,3,34,35]. More recently, the minicolumn as a distinct resulting computational and functional properties, repre- functional unit has been reaffirmed in primate prefrontal sents a kind of state that may reliably differ from the popu- cortex (PFC) by studying emergent higher cognitive func- lation as a whole. Certain features of this organization tions from encoded interlaminar communication within a may well be adaptive in specific environmental contexts. column [36]. Indeed, forms of this organization may exist in the general Although we have yet to fully characterize the connec- population in a fashion that is subclinical and even ben- tional and physiological organization within a single eficial at the individual level [20]. More extreme forms of column, models of internal columnar organization with this organization are clearly not adaptive. They interfere varying levels of microanatomical detail have been sug- with the day-to-day social and communicative activities gested [37–43]. One popular framework for understand- that have been so critical to our survival and success as a ing the column, and how minicolumns are assembled species. into the overall cortical sheet, is by framing its organiza- Although several reviews of changes within the brain tion during development. Prior to the embryonic estab- of ASD subjects are available [21–26], here we will focus lishment of the cortical plate (the aggregation of cells on three topics that are specifically related to the organi- that will become the cerebral cortex), there exists a layer zation of cerebral cortex: (i) the atypical organization of of cells and fibres at the surface of the neural tube: the cortical structure; (ii) alterations to connectional organi- preplate [32,44–46]. Many future cortical neurones are zation; and (iii) the potentially critical role the subplate generated at the inner wall of the developing neural plays in forming these structural and connectional tube by a group of precursor cells aggregated within the changes. ventricular and subventricular zones. Precursor cells undergo several rounds of symmetrical division in which more precursor cells are generated. This symmetrical NT cortical organization division gives way to several rounds of asymmetrical The organization of the human cerebral cortex is cur- division where each dividing precursor cell produces rently understood at multiple levels of analysis. Cortical another precursor cell and a neuroblast. The number of regions differ based upon their functional activity, their rounds of symmetrical cell division plays an important © 2015 British Neuropathological Society NAN 2016; 42: 115–134 Cortical construction in autism 117 role in determining the number of cortical columns that Structural changes to cortical organization will eventually populate the cortical sheet, while the in ASD asymmetrical cell divisions that follow partially deter- mine the final number of cells within a cortical column. Quantitative studies of post mortem cortical tissue have Such a model provides a window into how modifications revealed a number of important differences between ASD of cortical size,
Load more

Recommended publications
  • Subplate Neurons: Crucial Regulators of Cortical Development and Plasticity
    REVIEW ARTICLE published: 20 August 2009 NEUROANATOMY doi: 10.3389/neuro.05.016.2009 Subplate neurons: crucial regulators of cortical development and plasticity Patrick O. Kanold* Department of Biology, Institute for Systems Research, and Program in Neuroscience and Cognitive Science, University of Maryland, College Park, MD, USA Edited by: The developing cerebral cortex contains a distinct class of cells, subplate neurons, which Kathleen S. Rockland, RIKEN Brain form one of the fi rst functional cortical circuits. Subplate neurons reside in the cortical white Science Institute, Japan matter, receive thalamic inputs and project into the developing cortical plate, mostly to layer Reviewed by: Heiko J. Luhmann, Institut für 4. Subplate neurons are present at key time points during development. Removal of subplate Physiologie und Pathophysiologie, neurons profoundly affects cortical development. Subplate removal in visual cortex prevents the Germany maturation of thalamocortical synapse, the maturation of inhibition in layer 4, the development Sampsa Vanhatalo, of orientation selective responses in individual cortical neurons, and the formation of ocular University of Helsinky, Finland dominance columns. In addition, monocular deprivation during development reveals that ocular *Correspondence: Patrick O. Kanold, Department of dominance plasticity is paradoxical in the absence of subplate neurons. Because subplate neurons Biology, University of Maryland, 1116 projecting to layer 4 are glutamatergic, these diverse defi cits following subplate removal were Biosciences Research Building, hypothesized to be due to lack of feed-forward thalamic driven cortical excitation. A computational College Park, MD 20742, USA. model of the developing thalamocortical pathway incorporating feed-forward excitatory subplate e-mail: [email protected] projections replicates both normal development and plasticity of ocular dominance as well as the effects of subplate removal.
    [Show full text]
  • Regional Scattering of Primate Subplate Zolt ´Anmoln ´Ara,1 and Anna Hoerder-Suabedissena
    COMMENTARY COMMENTARY Regional scattering of primate subplate Zolt ´anMoln ´ara,1 and Anna Hoerder-Suabedissena The subplate layer is a highly dynamic zone of the generation of the macaque cortical neuronal cohorts developing cerebral cortex that reaches huge propor- that we still use today (7). Since then we gained a tions in human and nonhuman primates and has been much better understanding of the subplate and its associated with various brain developmental abnor- dynamic interactions with incoming afferents and malities. It contains some of the earliest-born neurons forming cortical circuits in a variety of species (4, 8– of the cortex. Surprisingly, the timing of subplate neuron 11). Additionally, the subplate has been the subject birth, migration, distribution, and degree of programmed of imaging studies and transcriptomic analyses be- cell death has only been analyzed in detail in rodents and cause of increasing evidence for its association with carnivores, but not in primates. The study by Duque et al. various cognitive developmental disorders (7, 12–14). (1) is the first that specifically examines the distribution of The majority of recent work on the subplate was subplate cells labeled with the DNA replication marker conducted on rodents and carnivores, sometimes with tritiated thymidine ([3H]dT) across different brain regions clear interspecies differences (15–18), emphasizing the in valuable archived macaque brain material. They show importance of nonhuman primate and human studies that macaque subplate neurons, after having completed such as the one in PNAS (1). Combined birth dating and their migration, become secondarily displaced inward by marker expression studies in the mouse suggest that the arrival of subcortical and cortical axons.
    [Show full text]
  • Development, Evolution and Pathology of Neocortical Subplate Neurons
    REVIEWS Development, evolution and pathology of neocortical subplate neurons Anna Hoerder-Suabedissen and Zoltán Molnár Abstract | Subplate neurons have an essential role in cortical circuit formation. They are among the earliest formed neurons of the cerebral cortex, are located at the junction of white and grey matter, and are necessary for correct thalamocortical axon ingrowth. Recent transcriptomic studies have provided opportunities for monitoring and modulating selected subpopulations of these cells. Analyses of mouse lines expressing reporter genes have demonstrated novel, extracortical subplate neurogenesis and have shown how subplate cells are integrated under the influence of sensory activity into cortical and extracortical circuits. Recent studies have revealed that the subplate is involved in neurosecretion and modification of the extracellular milieu. The subplate zone is a transient cortical structure that subplate zone, their molecular identity and their sites of forms during mammalian brain development. Its early generation. Finally, we touch on how perinatal brain inju- maturity, and location at the interface between the devel- ries in the subplate in animal models and in humans can oping cortex and the ingrowing afferent fibres (FIGS 1,2), lead to subtle cytoarchitectonic and circuit abnormalities allows the subplate to have fundamental roles in the that are relevant to autism or schizophrenia. establishment of intracortical and extracortical circuit- ries, and to contribute to the guidance and areal targeting Subplate zone versus subplate cells of thalamocortical axons1. The subplate zone is generally identified based on cyto- Subplate neurons are a heterogeneous population of architectonic distinctions (FIGS 1,2), although not all neurons that are among the earliest generated in the cer- mammalian species have a distinct subplate zone dur- ebral cortex1–5.
    [Show full text]
  • Subplate Neurons: Their Biopsychosocial Role in Cognitive and Neurodevelopmental Disorders, Nociception and Stress
    Journal of Neurology & Stroke Review Article Open Access Subplate neurons: their biopsychosocial role in cognitive and neurodevelopmental disorders, nociception and stress Abstract Volume 10 Issue 5 - 2020 A systematic review was carried out of the literature especially in humans reporting Rosana Maria Tristão, Andressa Carvalho the origin, functions and neural changes of the subplate zone and the relationships with neurodevelopmental disorders and stress or nociceptive reaction in neonates. Thirty-two Oliveira, Nágelin Ferreira Barreto, Carlos articles with established criteria were identified. Academic Google, SciElo, PubMed, Nogueira Aucélio, Geraldo Magela Scopus, Cochraine Library and Web of Science databases were searched until January Fernandes, Karina Nascimento Costa, José 2020 for scientific papers written in any language. Subplate neurons are present during Alfredo Lacerda de Jesus embryogenesis of the nervous system and shortly after birth. Through them, the brain University of Brasilia, Medicine of Child and Adolescent Area, forms the first connections between the thalamus and the cortex originating sensory and Brazil cognitive capacities. Because of this, disorders involving migration and apoptosis failures or tissue injury can lead to psychiatric disorders, such as autism and schizophrenia, and to Correspondence: Rosana Maria Tristão, Child and Adolescent morphological alterations that may alter cognitive functions, modify the perception of pain Area, Faculty of Medicine, University of Brasília, Darcy Ribeiro Campus, 70910-900, Phone +5561999689359, Brasília DF, Brazil, in fetuses and neonates and have repercussions in adult life. Accumulative evidences reveal Email the importance of subplate neurons for neurodevelopment, previously ignored because they are transient cells. The elucidation of some morphological aspects of the cerebral cortex Received: May 28, 2020 | Published: September 08, 2020 may explain mental disorders, the beginning of the perception of nociceptive stimuli and their implication in the long term.
    [Show full text]
  • Subplate Pioneers and the Formation of Descending Connections from Cerebral Cortex
    The Journal of Neuroscience, April 1994, 14(4): 1892-l 907 Subplate Pioneers and the Formation of Descending Connections from Cerebral Cortex Susan K. McConnell,1 Anirvan Ghosh,2-a and Carla J. Shatz3 ‘Department of Biological Sciences and *Department of Neurobiology, School of Medicine, Stanford University, Stanford, California 94305, and 3Division of Neurobiology, Department of Molecular and Cell Biology, University of California, Berkeley, California 94720 The adult cerebral cortex extends axons to a variety of sub- pioneer neurons are required for the formation of normal adult cortical targets, including the thalamus and superior collic- connections in some systems:cell ablation studies in both ver- ulus. These descending projections are pioneered during tebrates(Kuwada, 1986)and invertebrates (Bastiani et al., 1985; development by the axons of a transient population of sub- Klose and Bentley, 1989) have demonstratedthat many axons plate neurons (McConnell et al., 1989). We show here that fail to develop normally in the absenceof pioneers. the descending axons of cortical plate neurons appear to In the mammalian telencephalon,a transient classof pioneer be delayed significantly in their outgrowth, compared with neurons lays down the initial axonal pathways between the ce- those of subplate neurons. To assess the possible role of rebral cortex and the thalamus (McConnell et al., 1989).These subplate neurons in the formation of these pathways, sub- subplate neurons are among the earliest-generatedneurons of plate neurons were ablated during the embryonic period. In the neocortex, but the majority of thesecells disappearin early all cases, an axon pathway formed from visual cortex through postnatal periods in a wave of cell death (Valverde and Facal- the internal capsule and into the thalamus.
    [Show full text]
  • Hypothesis on the Dual Origin of the Mammalian Subplate
    REVIEW ARTICLE published: 07 April 2011 NEUROANATOMY doi: 10.3389/fnana.2011.00025 Hypothesis on the dual origin of the mammalian subplate Juan F. Montiel1,2*, Wei Zhi Wang1, Franziska M. Oeschger1, Anna Hoerder-Suabedissen1, Wan Ling Tung1, Fernando García-Moreno1, Ida Elizabeth Holm3, Aldo Villalón2 and Zoltán Molnár1* 1 Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, UK 2 Center for Biomedical Research, Faculty of Medicine, Diego Portales University, Santiago, Chile 3 Department of Pathology, Randers Hospital, Randers and Clinical Institute, University of Aarhus, Aarhus, Denmark Edited by: The development of the mammalian neocortex relies heavily on subplate. The proportion of Luis Puelles, Universidad de Murcia, this cell population varies considerably in different mammalian species. Subplate is almost Spain undetectable in marsupials, forms a thin, but distinct layer in mouse and rat, a larger layer in Reviewed by: carnivores and big-brained mammals as pig, and a highly developed embryonic structure in Heiko J. Luhmann, Institut für Physiologie und Pathophysiologie, human and non-human primates. The evolutionary origin of subplate neurons is the subject of Germany current debate. Some hypothesize that subplate represents the ancestral cortex of sauropsids, Patrick O. Kanold, University of while others consider it to be an increasingly complex phylogenetic novelty of the mammalian Maryland, USA neocortex. Here we review recent work on expression of several genes that were originally *Correspondence: identified in rodent as highly and differentially expressed in subplate. We relate these observations Juan F. Montiel, Faculty of Medicine, Diego Portales University, Av. Ejército to cellular morphology, birthdating, and hodology in the dorsal cortex/dorsal pallium of several 141, Santiago, Chile.
    [Show full text]
  • Subplate Neuron Ablation Alters Neurotrophin Expression and Ocular Dominance Column Formation
    Subplate neuron ablation alters neurotrophin expression and ocular dominance column formation E. S. Lein*†, E. M. Finney*†‡, P. S. McQuillen*, and C. J. Shatz*§ *Howard Hughes Medical Institute͞Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720 Contributed by Carla J. Shatz, September 13, 1999 Ocular dominance column formation in visual cortex depends on a ratio of 9:1 kainic acid͞microspheres) were coinjected for both the presence of subplate neurons and the endogenous visualization of the injection sites and to limit spread of the expression of neurotrophins. Here we show that deletion of kainic acid (14, 15). Each animal received two injections, spaced subplate neurons, which supply glutamatergic inputs to visual approximately 1 mm apart anteroposteriorly, producing a zone cortex, leads to a paradoxical increase in brain-derived neurotro- of ablation up to several millimeters in extent (see refs. 14, 15 for phic factor mRNA in the same region of visual cortex in which complete details). Control animals were either identically in- ocular dominance columns are absent. Subplate neuron ablation jected with saline plus microspheres (9:1; n ϭ three animals) into also increases glutamic acid decarboxylase-67 levels, indicating an the visual subplate or were unmanipulated (n ϭ 2). In three alteration in cortical inhibition. These observations imply a role for additional control animals, 0.5-␮l injections of kainic acid plus this special class of neurons in modulating activity-dependent microspheres were injected into layer 4 of visual cortex rather competition by regulating levels of neurotrophins and excitability than into the subplate. within a developing cortical circuit.
    [Show full text]
  • Segregation of Geniculocortical a Role for Subplate Neurons
    The Journal of Neuroscience, June 1994, 14(6): 38623880 Segregation of Geniculocortical Afferents during the Critical Period: A Role for Subplate Neurons Anirvan Ghosh and Carla J. ShatP Department of Neurobiology, Stanford University School of Medicine, Stanford, California 94305 To investigate the cellular interactions within the mammalian Visual experience can have a profound influence on the devel- visual cortex that are important in ocular dominance column opment of connections in the mammalian visual system. This formation, we have examined the role of subplate neurons phenomenonhas been most thoroughly investigated with regard in this process. LGN axons segregate in layer 4 of the cat’s to the system of ocular dominance columns in primary visual visual cortex between the third and sixth postnatal weeks cortex of cat and monkey (Hubel and Wiesel, 1977; LeVay et to give rise to the adult pattern of ocular dominance columns. al., 1980). Axon terminals from neurons of the lateral geniculate Subplate neurons are a transient population of neurons that nucleus (LGN), whose pattern of innervation of cortex gives sit in the white matter but have extensive projections into rise to ocular dominance columns, are initially intermixed with the overlying cortex, particularly layer 4, during neonatal life. regard to eye preference within layer 4 of visual cortex (Rakic, Many subplate neurons are present at birth, but most are 1976; LeVay et al., 1978). Events mediated by neuronal activity gone by the end of the period of LGN axon segregation. To and visual experience are known to be important in the for- examine whether these neurons are required for the seg- mation of ocular dominance columns in layer 4, since the final regation of LGN axons, we deleted them by intracortical in- pattern of ocular dominance is susceptibleto abnormal visual jections of kainic acid either just after LGN axons had grown experience during postnatal development.
    [Show full text]
  • Subplate Zone of the Human Brain: Historical Perspective and New Concepts
    Coll. Antropol. 32 (2008) Suppl. 1: 3–8 Review Subplate Zone of the Human Brain: Historical Perspective and New Concepts Ivica Kostovi}1 and Nata{a Jovanov-Milo{evi}1,2 1 Department of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Zagreb, Croatia 2 Department of Biology, School of Medicine, University of Zagreb, Zagreb, Croatia ABSTRACT Subplate zone (SP) is prominent, transient laminar compartment of the human fetal cerebral wall. The SP develops around 13 and gradually disappears after 32–34 postovulatory weeks. The SP neurons can be found as late as nine postnatal months, while remnants of the SP neurons can be traced until adult age in the form of interstitial neurons of the gyral white matter. SP is composed of postmigratory and migratory neurons, growth cones, loosely arranged axons, dendrites, glial cell and synapses. The remarkable feature of the SP is the presence of large amount of extracellular ma- trix. This feature can be used for delineation of SP in magnetic resonance images (MRI) of both, in vivo and post mortem brains. The importance of SP as the main synaptic zone of the human fetal cortex is based on the rich input of »waiting« afferents from thalamus and cortex, during the crucial phase of cortical target area selection. SP increases during mam- malian evolution and culminates in human brain concomitantly with increase in number and diversity of cortico-corti- cal fibers. The recent neurobiological evidence shows that SP is important site of spontaneous endogeneous activity, building a framework for development of cortical columnar organization.
    [Show full text]
  • Growth and Targeting of Subplate Axons and Establishment of Major Cortical Pathways
    The Journal of Neuroscience, April 1992, 12(4): 1194-1211 Growth and Targeting of Subplate Axons and Establishment of Major Cortical Pathways Juan A. De Carlos and Dennis D. M. O’Leary Molecular Neurobiology Laboratory, The Salk Institute for Biological Studies, La Jolla, California 92037 In the developing mammalian neocortex, the first postmitotic tion at the junction of the hindbrain and spinal cord, at times neurons form the “preplate” superficial to the neuroepi- shortly after the passing of cortical axons. In every case, thelium. The preplate is later split into a marginal zone (layer the labeled neurons are confined to layer 5; subplate neurons 1) and subplate by cortical plate neurons that form layers are not labeled. Injections that involve thalamus label a sub- 2-6. Cortical efferent axons from layers 5 and 6 and cortical stantial number of layer 6 and subplate cells. Thus, the sub- afferent axons from thalamus pass between cortex and sub- cortical distribution of subplate axons is limited to the in- cortical structures through the internal capsule. Here, we ternal capsule and thalamus. identify in rats the axonal populations that establish the in- We conclude the following. In rats, preplate neurons send ternal capsule, and characterize the potential role of sub- the first cortical axons into the internal capsule, a finding plate axons in the development of cortical efferent and af- comparable to that of McConnell et al. (1969) in cats and ferent projections. ferrets. Thalamic axons coestablish the internal capsule with The early growth of cortical efferent and afferent axons preplate axons, inferring that the initial outgrowth and tar- was studied using l-1 -dioctodecyl-3,3,3’,3’-tetramethylin- geting of thalamocortical axons is independent of the influ- docarbocyanine perchlorate (Dil) as an anterograde and ret- ence of cortical efferents.
    [Show full text]
  • 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.
    [Show full text]
  • Associated with the Subplate Neurons of the Mammalian Cerebral Cortex (Trophic Factors/Neural Development/Cell Death/Brain/Transient Neurons) KAREN L
    Proc. Natl. Acad. Sci. USA Vol. 87, pp. 187-190, January 1990 Neurobiology Nerve growth factor receptor immunoreactivity is transiently associated with the subplate neurons of the mammalian cerebral cortex (trophic factors/neural development/cell death/brain/transient neurons) KAREN L. ALLENDOERFER*, DAVID L. SHELTONt, ERIC M. SHOOTER, AND CARLA J. SHATZ Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305 Communicated by Gunther S. Stent, October 13, 1989 ABSTRACT Nerve growth factor and its receptor (NGFR) do (5, 6). Furthermore, they receive functional synaptic are known to be present in diverse embryonic and neonatal inputs (refs. 5 and 7; E. Friauf, S. K. McConnell, and C.J.S., central nervous system tissues, including the cerebral cortex. unpublished data) and pioneer elaborate projections to cor- However, the identity of the cortical cells expressing NGFR tical and subcortical targets (5, 8). Subplate neurons are also immunoreactivity has not been established. We have used thought to interact with the many ingrowing axonal systems immunolabeling coupled with [3HJthymidine autoradiography from the thalamus and cortex that are known to wait in the to identify such cells in ferret and cat brain. Polyclonal subplate zone (2, 9, 10) before finally invading the cortical antibodies raised against a synthetic peptide corresponding to plate, at -1 week before birth (11). After the waiting period a conserved amino acid sequence of the NGFR were used for ends, subplate neurons begin a programmed cell death, which this purpose. Western (immunologic) blot analyses show that eliminates over 90% of the population, until finally only these antibodies specifically recognize NGFR and precursor 1%o remain by 3 months of age (12, 13).
    [Show full text]