The first cortical circuits: Subplate neurons lead the way and shape cortical organization

doi:10.1515/NF-2018-0010

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The first cortical circuits: Subplate neurons lead the way and shape cortical organization

Journal Article•DOI•

The first cortical circuits: Subplate neurons lead the way and shape cortical organization

Patrick O. Kanold¹•Institutions (1)

University of Maryland, College Park¹

07 Feb 2019-Neuroforum (De Gruyter)-Vol. 25, Iss: 1, pp 15-23

TL;DR: The circuitry and functional roles of cortical subplate neurons are reviewed, focusing on their purpose in the development of primary sensory cortices in the developing mammalian brain.

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Abstract: Abstract The cerebral cortex is essential for our sensory experiences and conscious thought. Its neural connections, in particular sensory areas of the cerebral cortex, are shaped and sculpted by our early sensory experiences. Onset of these first sensory experiences of the world mark an important developmental event, enabling our worldy interactions to shape the makeup of our cerebral cortex. These long-lasting effects of early sensory experience are particularly striking in human communication, since early exposure to the mother’s language is required to detect all nuances in the underlying sounds. Early interactions with the world are mediated by a key set of neurons, subplate neurons, which remain part of the developing cerebral cortex until most of them disappear at later stages of development. They play a crucial role in the developing mammalian brain. Here I review the circuitry and functional roles of cortical subplate neurons, focusing on their purpose in the development of primary sensory cortices.

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Journal Article•DOI•

The enigmatic fetal subplate compartment forms an early tangential cortical nexus and provides the framework for construction of cortical connectivity.

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Ivica Kostović¹•Institutions (1)

University of Zagreb¹

11 Jul 2020-Progress in Neurobiology

TL;DR: Evidence on the development and connectivity of the deep, cell-sparse, synapse-containing subplate compartment (SPC) is evaluated and its role in the pathogenesis of neurodevelopmental disorders is discussed.

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58 citations

Cites background from "The first cortical circuits: Subpla..."

...GABA seems to be an excitatory transmitter at this early age, as shown in several studies (Ben-Ari, 2014; Hanganu et al., 2002; Kanold, 2019; Khazipov and Luhmann, 2006; Luhmann and Khazipov, 2018; Moore et al., 2011; Sedmak et al., 2016; Vanhatalo and Kaila, 2006)....
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...…acids as putative transmitters (Antón-Bolaños et al., 2018; Antonini and Shatz, 1990; Hanganu et al., 2002; Hoerder-Suabedissen and Molnár, 2015; Kostović et al., 2019b) and contact other SPN. Glutamatergic terminals may also originate from CP neurons (Hanganu et al., 2002; Kanold, 2019, 2009)....
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...…2018; Friauf et al., 1990; Kanold, 2009; Kanold and Luhmann, 2010; Kilb et al., 2011; Luhmann et al., 2009; Luhmann and Khazipov, 2018) and consequently influence further development of cortical neuronal circuitry (Kanold, 2019; Milh et al., 2007; Molnár et al., 2019; Tolonen et al., 2007)....
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...These “silent” synapses were documented in a comparatively later postnatal period in rats (Kanold, 2019)....
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...…2 were focused on physiological events in local subplate circuitry within a given cortical area (Friauf et al., 1990; Hanganu et al., 2009, 2002; Kanold, 2019; Kanold et al., 2003; Luhmann et al., 2009; Luhmann and Khazipov, 2018) and focal modulation of subplate circuitry from thalamic and CP…...
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Journal Article•DOI•

Quantitative In vivo MRI Assessment of Structural Asymmetries and Sexual Dimorphism of Transient Fetal Compartments in the Human Brain.

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Lana Vasung¹, Caitlin K. Rollins¹, Hyuk Jin Yun¹, Clemente Velasco-Annis¹, Jennings Zhang², Konrad Wagstyl³, Alan C. Evans², Simon K. Warfield¹, Henry A. Feldman¹, P. Ellen Grant¹, Ali Gholipour¹ - Show less +7 more•Institutions (3)

Boston Children's Hospital¹, Montreal Neurological Institute and Hospital², University of Cambridge³

14 Mar 2020-Cerebral Cortex

TL;DR: The hypothesis that structural asymmetries and sexual dimorphism in relative volumes of cortical regions are present during prenatal brain development is supported.

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Abstract: Structural asymmetries and sexual dimorphism of the human cerebral cortex have been identified in newborns, infants, children, adolescents, and adults. Some of these findings were linked with cognitive and neuropsychiatric disorders, which have roots in altered prenatal brain development. However, little is known about structural asymmetries or sexual dimorphism of transient fetal compartments that arise in utero. Thus, we aimed to identify structural asymmetries and sexual dimorphism in the volume of transient fetal compartments (cortical plate [CP] and subplate [SP]) across 22 regions. For this purpose, we used in vivo structural T2-weighted MRIs of 42 healthy fetuses (16.43-36.86 gestational weeks old, 15 females). We found significant leftward asymmetry in the volume of the CP and SP in the inferior frontal gyrus. The orbitofrontal cortex showed significant rightward asymmetry in the volume of CP merged with SP. Males had significantly larger volumes in regions belonging to limbic, occipital, and frontal lobes, which were driven by a significantly larger SP. Lastly, we did not observe sexual dimorphism in the growth trajectories of the CP or SP. In conclusion, these results support the hypothesis that structural asymmetries and sexual dimorphism in relative volumes of cortical regions are present during prenatal brain development.

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34 citations

Journal Article•DOI•

The Integrative Function of Silent Synapses on Subplate Neurons in Cortical Development and Dysfunction.

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Patrick O. Kanold¹, Rongkang Deng¹, Xiangying Meng¹•Institutions (1)

University of Maryland, College Park¹

16 Apr 2019-Frontiers in Neuroanatomy

TL;DR: Subplate associated circuits are reviewed, their changing functions, and possible roles in development and disease are discussed, to suggest a crucial link between early injuries and later circuit dysfunction.

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Abstract: The thalamocortical circuit is of central importance in relaying information to the cortex. In development, subplate neurons (SPNs) form an integral part of the thalamocortical pathway. These early born cortical neurons are the first neurons to receive thalamic inputs and excite neurons in the cortical plate. This feed-forward circuit topology of SPNs supports the role of SPNs in shaping the formation and plasticity of thalamocortical connections. Recently it has been shown that SPNs also receive inputs from the developing cortical plate and project to the thalamus. The cortical inputs to SPNs in early ages are mediated by N-methyl-D-aspartate (NMDA)-receptor only containing synapses while at later ages α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-receptors are present. Thus, SPNs perform a changing integrative function over development. NMDA-receptor only synapses are crucially influenced by the resting potential and thus insults to the developing brain that causes depolarizations, e.g., hypoxia, can influence the integrative function of SPNs. Since such insults in humans cause symptoms of neurodevelopmental disorders, NMDA-receptor only synapses on SPNs might provide a crucial link between early injuries and later circuit dysfunction. We thus here review subplate associated circuits, their changing functions, and discuss possible roles in development and disease.

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22 citations

Cites result from "The first cortical circuits: Subpla..."

...…the putative role of subplate in setting up protomaps of cortical organization (O’Leary and Borngasser, 2006; O’Leary et al., 2007; Wess et al., 2017; Kanold, 2019) and given that alterations are present in the target layers of SPNs, these observations are consistent with a potential role of early…...
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...Given the putative role of subplate in setting up protomaps of cortical organization (O’Leary and Borngasser, 2006; O’Leary et al., 2007; Wess et al., 2017; Kanold, 2019) and given that alterations are present in the target layers of SPNs, these observations are consistent with a potential role of early SPN dysfunction in the emergence of ASDs....
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Journal Article•DOI•

Sleep Problems in Preschoolers With Autism Spectrum Disorder Are Associated With Sensory Sensitivities and Thalamocortical Overconnectivity.

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Annika C. Linke¹, Bosi Chen², Lindsay Olson², Cynthia Ibarra¹, Chris Fong², Sarah Reynolds¹, Michael Apostol¹, Mikaela Kinnear¹, Ralph-Axel Müller², Inna Fishman² - Show less +6 more•Institutions (2)

San Diego State University¹, University of California, San Diego²

31 Jul 2021-Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

TL;DR: In this paper, the authors investigated the relationship between auditory-thalamic functional connectivity measured during natural sleep functional magnetic resonance imaging, sleep problems, and sound sensitivities in 70 toddlers and preschoolers with ASD compared with a matched group of 46 typically developing children.

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9 citations

Journal Article•DOI•

Sleep Problems in Preschoolers With Autism Spectrum Disorder Are Associated With Sensory Sensitivities and Thalamocortical Overconnectivity

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01 Jan 2023-Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

TL;DR: In this paper , the authors investigated the relationship between auditory-thalamic functional connectivity measured during natural sleep functional magnetic resonance imaging, sleep problems, and sound sensitivities in 70 toddlers and preschoolers with ASD compared with a matched group of 46 typically developing children.

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8 citations

References

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Journal Article•DOI•

Of human bonding: newborns prefer their mothers' voices

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Anthony J. DeCasper, William P. Fifer¹•Institutions (1)

University of North Carolina at Greensboro¹

06 Jun 1980-Science

TL;DR: The neonate's preference for the maternal voice suggests that the period shortly after birth may be important for initiating infant bonding to the mother.

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Abstract: By sucking on a nonnutritive nipple in different ways, a newborn human could produce either its mother's voice or the voice of another female. Infants learned how to produce the mother's voice and produced it more often than the other voice. The neonate's preference for the maternal voice suggests that the period shortly after birth may be important for initiating infant bonding to the mother.

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1,852 citations

"The first cortical circuits: Subpla..." refers background in this paper

...Since newborns already show a preference for maternal voice (DeCasper and Fifer, 1980; Mehler et al., 1988; Voegtline et al., 2013) the relevant pro- cesses are likely active from early stages in development....
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...Even though auditory experience in a human fetus is attenuated by the womb, the preference for maternal voice in newborns (DeCasper and Fifer, 1980; Mehler et al., 1988; Voegtline et al., 2013) suggests that sounds can activate the human auditory system in utero, and that these sounds are processed…...
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Journal Article•DOI•

A precursor of language acquisition in young infants.

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Jacques Mehler¹, Peter W. Jusczyk¹, Ghislaine Lambertz¹, Nilofar Halsted², Josiane Bertoncini¹, Claudine Amiel-Tison - Show less +2 more•Institutions (2)

School for Advanced Studies in the Social Sciences¹, University of Oregon²

01 Jul 1988-Cognition

TL;DR: Four-day-old French and 2-month-old American infants distinguish utterances in their native languages from those of another language, and two experiments with low-pass-filtered versions of the samples replicated the main findings of discrimination of the native language utterances.

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1,268 citations

Journal Article•DOI•

Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain

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Ivica Kostović¹, Pasko Rakic²•Institutions (2)

University of Zagreb¹, Yale University²

15 Jul 1990-The Journal of Comparative Neurology

TL;DR: The cytological organization and the timetable of emergence and dissolution of the transient subplate zone subjacent to the developing visual and somatosensory cortex were studied in a series of human and monkey fetal brains.

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Abstract: The cytological organization and the timetable of emergence and dissolution of the transient subplate zone subjacent to the developing visual and somatosensory cortex were studied in a series of human and monkey fetal brains. Cerebral walls processed with Nissl, Golgi, electron-microscopic, and histochemical methods show that this zone consists of migratory and postmigratory neurons, growth cones, loosely arranged axons, dendrites, synapses, and glial cells. In both species the subplate zone becomes visible at the beginning of the mid-third of gestation as a cell-poor/fiber-rich layer situated between the intermediate zone and the developing cortical plate. The subplate zone appears earlier in the somatosensory than in the visual area and reaches maximal width at the beginning of the last third of gestation in both regions. At the peak of its size the ratio between the width of the subplate zone and cortical plate in the somatosensory cortex is 2:1 in monkey and 4:1 in man while in the occipital lobe these structures have about equal width in both species. The dissolution of the subplate zone begins during the last third of gestation with degeneration of some subplate neurons and the relocation of fiber terminals into the cortex. The subplate zone disappears faster in the visual than in the somatosensory area. The present results together with our previous findings support the hypothesis that the subplate zone may serve as a “waiting” compartment for transient cellular interactions and a substrate for competition, segregation, and growth of afferents originated sequentially from the brain stem, basal forebrain, thalamus, and from the ipsi- and contralateral cerebral hemisphere. After a variable and partially overlapping time period, these fibers enter the cortical plate while the subplate zone disappears leaving only a vestige of cells scattered throughout the subcortical white matter. A comparison between species indicates that the size and duration of the subplate zone increases during mammalian evolution and culminates in human fetuses concomitantly with an enlargement of cortico-cortical fiber systems. The regional difference in the size, pattern, and resolution of the subplate zone correlates also with the pattern of cerebral convolutions. Our findings indicate that, contrary to prevailing notions, the subplate may not be a vestige of the phylogenetically old network but a transient embryonic structure that expanded during evolution to subserve the increasing number of its connections.

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852 citations

"The first cortical circuits: Subpla..." refers background in this paper

...From these observations, it was hypothesized that SPNs serve as a transient target and waiting compartment (Kostovic and Rakic, 1990; Ghosh and Shatz, 1992b; Hevner, 2000; Kostovic and Judas, 2002)....
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...Therefore, the study of how SPN neurons differ across species might hold clues to the evolution of the human neocortex, because SPNs seem to be overrepresented in species with more complex cortical organization (Kostovic and Rakic, 1990; Kanold and Luhmann, 2010)....
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Journal Article•DOI•

Maternal immune activation: Implications for neuropsychiatric disorders

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Myka L. Estes¹, A. Kimberley McAllister¹•Institutions (1)

University of California, Davis¹

19 Aug 2016-Science

TL;DR: Common principles revealed by maternal immune activation models are described, highlighting recent findings that strengthen their relevance for schizophrenia and autism and are starting to reveal the molecular mechanisms underlying the effects of MIA on offspring.

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Abstract: Epidemiological evidence implicates maternal infection as a risk factor for autism spectrum disorder and schizophrenia. Animal models corroborate this link and demonstrate that maternal immune activation (MIA) alone is sufficient to impart lifelong neuropathology and altered behaviors in offspring. This Review describes common principles revealed by these models, highlighting recent findings that strengthen their relevance for schizophrenia and autism and are starting to reveal the molecular mechanisms underlying the effects of MIA on offspring. The role of MIA as a primer for a much wider range of psychiatric and neurologic disorders is also discussed. Finally, the need for more research in this nascent field and the implications for identifying and developing new treatments for individuals at heightened risk for neuroimmune disorders are considered.

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760 citations

"The first cortical circuits: Subpla..." refers background in this paper

...Similarly, maternal stress or inflammation (Estes and McAllister, 2016) can potentially alter SPN function....
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Journal Article•DOI•

Neuron number and size in prefrontal cortex of children with autism

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Eric Courchesne¹, Peter R. Mouton, Michael E. Calhoun, Katerina Semendeferi, Clelia Ahrens-Barbeau, Melodie J. Hallet, Cynthia Carter Barnes, Karen Pierce - Show less +4 more•Institutions (1)

University of California, San Diego¹

09 Nov 2011-JAMA

TL;DR: Brain overgrowth in males with autism involved an abnormal excess number of neurons in the PFC, and autistic children had both greater total prefrontal neuron counts and brain weight for age than control children.

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Abstract: Results Children with autism had 67% more neurons in the PFC (mean, 1.94 billion; 95% CI, 1.57-2.31) compared with control children (1.16 billion; 95% CI, 0.901.42; P=.002), including 79% more in DL-PFC (1.57 billion; 95% CI, 1.20-1.94 in autism cases vs 0.88 billion; 95% CI, 0.66-1.10 in controls; P=.003 ) and 29% more in M-PFC ( 0.36 billion; 95% CI, 0.33-0.40 in autism cases vs 0.28 billion; 95% CI, 0.23-0.34 in controls; P=.009). Brain weight in the autistic cases differed from normative mean weight for age by a mean of 17.6% (95% CI, 10.2%-25.0%; P=.001), while brains in controls differed by a mean of 0.2% (95% CI, �8.7% to 9.1%; P=.96). Plots of counts by weight showed autistic children had both greater total prefrontal neuron counts and brain weight for age than control children. Conclusion In this small preliminary study, brain overgrowth in males with autism involved an abnormal excess number of neurons in the PFC.

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635 citations

"The first cortical circuits: Subpla..." refers background in this paper

...Histological studies on human postmortem tissue from autism patients shows an altered boundary between L6 and white matter (Avino and Hutsler, 2010) as well altered neural cell number and patchy subplate gene expression changes (Courchesne et al., 2011; Stoner et al., 2014)....
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