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

Patrick O. Kanold 1
  • 1 Department of Biology, 1116 Biosciences Res. Bldg., Maryland, USA
Patrick O. Kanold
  • Corresponding author
  • Department of Biology, University of Maryland, 1116 Biosciences Res. Bldg., College Park, MD 20742 USA, Phone: +1 (301) 405.5741, Maryland, USA
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  • Patrick Kanold is a Professor at the University of Maryland, College Park. He obtained his Dipl.-Ing. in Electrical Engineering at the Technische Universität Berlin 1994; his Ph.D. in Biomedical Engineering from the Johns Hopkins University in Baltimore, USA. From 2000–2006 he was a postdoctoral fellow and Instructor at the Department of Neurobiology at Harvard Medical School in Boston, USA. Since 2007 he is at the University of Maryland College Park, USA.
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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.

  • Akerman CJ, Smyth D, Thompson ID (2002) Visual experience before eye-opening and the development of the retinogeniculate pathway. Neuron 36:869–879.

  • Akerman CJ, Grubb MS, Thompson ID (2004) Spatial and temporal properties of visual responses in the thalamus of the developing ferret. J Neurosci 24:170–182.

  • Antonini A, Shatz CJ (1990) Relation Between Putative Transmitter Phenotypes and Connectivity of Subplate Neurons During Cerebral Cortical Development. The European journal of neuroscience 2:744–761.

  • Avino TA, Hutsler JJ (2010) Abnormal cell patterning at the cortical gray-white matter boundary in autism spectrum disorders. Brain research 1360:138–146.

  • Bakken TE et al. (2016) A comprehensive transcriptional map of primate brain development. Nature 535:367–375.

  • Barkat TR, Polley DB, Hensch TK (2011) A critical period for auditory thalamocortical connectivity. Nat Neurosci 14:1189–1194.

  • Bayer L, Serafin M, Eggermann E, Saint-Mleux B, Machard D, Jones BE, Muhlethaler M (2004) Exclusive postsynaptic action of hypocretin-orexin on sublayer 6b cortical neurons. J Neurosci 24:6760–6764.

  • Belgard TG, Marques AC, Oliver PL, Abaan HO, Sirey TM, Hoerder-Suabedissen A, Garcia-Moreno F, Molnar Z, Margulies EH, Ponting CP (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71:605–616.

  • Birnholz JC, Benacerraf BR (1983) The development of human fetal hearing. Science 222:516–518.

  • Blum T, Saling E, Bauer R (1985) First magnetoencephalographic recordings of the brain activity of a human fetus. Br J Obstet Gynaecol 92:1224–1229.

  • Butts DA, Kanold PO (2010) The applicability of spike time dependent plasticity to development. Front Synaptic Neurosci 2:30.

  • Case L, Broberger C (2017) Neurotensin Broadly Recruits Inhibition via White Matter Neurons in the Mouse Cerebral Cortex: Synaptic Mechanisms for Decorrelation. Cereb Cortex:1–14.

  • Case L, Lyons DJ, Broberger C (2017) Desynchronization of the Rat Cortical Network and Excitation of White Matter Neurons by Neurotensin. Cereb Cortex 27:2671–2685.

  • Chen M, Weng S, Deng Q, Xu Z, He S (2009) Physiological properties of direction-selective ganglion cells in early postnatal and adult mouse retina. The Journal of physiology 587:819–828.

  • Chun JJ, Shatz CJ (1989) The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J Neurosci 9:1648–1667.

  • Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ, Barnes CC, Pierce K (2011) Neuron number and size in prefrontal cortex of children with autism. JAMA 306:2001–2010.

  • DeCasper AJ, Fifer WP (1980) Of human bonding: newborns prefer their mothers’ voices. Science 208:1174–1176.

  • Deng R, Kao JPY, Kanold PO (2017) Distinct Translaminar Glutamatergic Circuits to GABAergic Interneurons in the Neonatal Auditory Cortex. Cell Rep 19:1141–1150.

  • Draganova R, Eswaran H, Murphy P, Huotilainen M, Lowery C, Preissl H (2005) Sound frequency change detection in fetuses and newborns, a magnetoencephalographic study. Neuroimage 28:354–361.

  • Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ (2006) Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 439:79–83.

  • Erzurumlu RS, Gaspar P (2012) Development and critical period plasticity of the barrel cortex. The European journal of neuroscience 35:1540–1553.

  • Espinosa JS, Stryker MP (2012) Development and plasticity of the primary visual cortex. Neuron 75:230–249.

  • Estes ML, McAllister AK (2016) Maternal immune activation: Implications for neuropsychiatric disorders. Science 353:772–777.

  • Eswaran H, Lowery CL, Robinson SE, Wilson JD, Cheyne D, McKenzie D (2000) Challenges of recording human fetal auditory-evoked response using magnetoencephalography. J Matern Fetal Med 9:303–307.

  • Eswaran H, Preissl H, Wilson JD, Murphy P, Robinson SE, Rose D, Vrba J, Lowery CL (2002) Short-term serial magnetoencephalography recordings offetal auditory evoked responses. Neuroscience letters 331:128–132.

  • Friauf E, Shatz CJ (1991) Changing patterns of synaptic input to subplate and cortical plate during development of visual cortex. Journal of neurophysiology 66:2059–2071.

  • Friauf E, McConnell SK, Shatz CJ (1990) Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci 10:2601–2613.

  • Ghosh A, Shatz CJ (1992a) Involvement of subplate neurons in the formation of ocular dominance columns. Science 255:1441–1443.

  • Ghosh A, Shatz CJ (1992b) Pathfinding and target selection by developing geniculocortical axons. J Neurosci 12:39–55.

  • Ghosh A, Shatz CJ (1993) A role for subplate neurons in the patterning of connections from thalamus to neocortex. Development 117:1031–1047.

  • Ghosh A, Shatz CJ (1994) Segregation of geniculocortical afferents during the critical period: a role for subplate neurons. J Neurosci 14:3862–3880.

  • Ghosh A, Antonini A, McConnell SK, Shatz CJ (1990) Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347:179–181.

  • Hanganu IL, Luhmann HJ (2004) Functional nicotinic acetylcholine receptors on subplate neurons in neonatal rat somatosensory cortex. Journal of neurophysiology 92:189–198.

  • Hanganu IL, Kilb W, Luhmann HJ (2002) Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci 22:7165–7176.

  • Hanganu IL, Okabe A, Lessmann V, Luhmann HJ (2009) Cellular mechanisms of subplate-driven and cholinergic input-dependent network activity in the neonatal rat somatosensory cortex. Cereb Cortex 19:89–105.

  • Hevner RF (2000) Development of connections in the human visual system during fetal mid-gestation: a DiI-tracing study. J Neuropathol Exp Neurol 59:385–392.

  • Higashi S, Molnar Z, Kurotani T, Toyama K (2002) Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording. Neuroscience 115:1231–1246.

  • Hoerder-Suabedissen A, Molnar Z (2013) Molecular diversity of early-born subplate neurons. Cereb Cortex 23:1473–1483.

  • Hoerder-Suabedissen A, Wang WZ, Lee S, Davies KE, Goffinet AM, Rakic S, Parnavelas J, Reim K, Nicolic M, Paulsen O, Molnar Z (2009) Novel markers reveal subpopulations of subplate neurons in the murine cerebral cortex. Cereb Cortex 19:1738–1750.

  • Hoerder-Suabedissen A, Hayashi S, Upton L, Nolan Z, Casas-Torremocha D, Grant E, Viswanathan S, Kanold PO, Clasca F, Kim Y, Molnar Z (2018) Subset of Cortical Layer 6b Neurons Selectively Innervates Higher Order Thalamic Nuclei in Mice. Cereb Cortex.

  • Kanold PO (2009) Subplate neurons: crucial regulators of cortical development and plasticity. Front Neuroanat 3:16.

  • Kanold PO, Shatz CJ (2006) Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 51:627–638.

  • Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48.

  • Kanold PO, Kara P, Reid RC, Shatz CJ (2003) Role of subplate neurons in functional maturation of visual cortical columns. Science 301:521–525.

  • Kostovic I, Rakic P (1980) Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol 9:219–242.

  • 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.

  • Kostovic I, Judas M (2002) Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants. Anat Rec 267:1–6.

  • Kostovic I, Lukinovic N, Judas M, Bogdanovic N, Mrzljak L, Zecevic N, Kubat M (1989) Structural basis of the developmental plasticity in the human cerebral cortex: the role of the transient subplate zone. Metab Brain Dis 4:17–23.

  • Krmpotic-Nemanic J, Kostovic I, Nemanic D, Kelovic Z (1979) The laminar organization of the prospective auditory cortex in the human fetus (11--13.5 weeks of gestation). Acta Otolaryngol 87:241–246.

  • Krug K, Akerman CJ, Thompson ID (2001) Responses of neurons in neonatal cortex and thalamus to patterned visual stimulation through the naturally closed lids. Journal of neurophysiology 85:1436–1443.

  • Lein ES, Finney EM, McQuillen PS, Shatz CJ (1999) Subplate neuron ablation alters neurotrophin expression and ocular dominance column formation. Proceedings of the National Academy of Sciences of the United States of America 96:13491–13495.

  • Lein ES, Belgard TG, Hawrylycz M, Molnar Z (2017) Transcriptomic Perspectives on Neocortical Structure, Development, Evolution, and Disease. Annu Rev Neurosci 40:629–652.

  • Lengle JM, Chen M, Wakai RT (2001) Improved neuromagnetic detection of fetal and neonatal auditory evoked responses. Clin Neurophysiol 112:785–792.

  • Liao CC, Lee LJ (2011) Neonatal fluoxetine exposure affects the action potential properties and dendritic development in cortical subplate neurons of rats. Toxicol Lett 207:314–321.

  • Liao CC, Lee LJ (2012) Evidence for structural and functional changes of subplate neurons in developing rat barrel cortex. Brain Struct Funct 217:275–292.

  • Liao CC, Lee LJ (2014) Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats. Neuropharmacology 77:81–89.

  • Marx M, Qi G, Hanganu-Opatz IL, Kilb W, Luhmann HJ, Feldmeyer D (2015) Neocortical Layer 6B as a Remnant of the Subplate – A Morphological Comparison. Cereb Cortex.

  • McClendon E, Shaver DC, Degener-O’Brien K, Gong X, Nguyen T, Hoerder-Suabedissen A, Molnar Z, Mohr C, Richardson BD, Rossi DJ, Back SA (2017) Transient Hypoxemia Chronically Disrupts Maturation of Preterm Fetal Ovine Subplate Neuron Arborization and Activity. J Neurosci 37:11912–11929.

  • McConnell SK, Ghosh A, Shatz CJ (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245:978–982.

  • McConnell SK, Ghosh A, Shatz CJ (1994) Subplate pioneers and the formation of descending connections from cerebral cortex. J Neurosci 14:1892–1907.

  • McQuillen PS, Ferriero DM (2005) Perinatal subplate neuron injury: implications for cortical development and plasticity. Brain Pathol 15:250–260.

  • McQuillen PS, Sheldon RA, Shatz CJ, Ferriero DM (2003) Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia. J Neurosci 23:3308–3315.

  • Mehler J, Jusczyk P, Lambertz G, Halsted N, Bertoncini J, Amiel-Tison C (1988) A precursor of language acquisition in young infants. Cognition 29:143–178.

  • Meng X, Kao JP, Kanold PO (2014) Differential signaling to subplate neurons by spatially specific silent synapses in developing auditory cortex. J Neurosci 34:8855–8864.

  • Mikhailova A, Sunkara N, McQuillen PS (2017) Unbiased Quantification of Subplate Neuron Loss following Neonatal Hypoxia-Ischemia in a Rat Model. Dev Neurosci 39:171–181.

  • Molnar Z, Kaas JH, de Carlos JA, Hevner RF, Lein E, Nemec P (2014) Evolution and development of the mammalian cerebral cortex. Brain Behav Evol 83:126–139.

  • Montiel JF, Wang WZ, Oeschger FM, Hoerder-Suabedissen A, Tung WL, Garcia-Moreno F, Holm IE, Villalon A, Molnar Z (2011) Hypothesis on the dual origin of the Mammalian subplate. Front Neuroanat 5:25.

  • Nagode DA, Meng X, Winkowski DE, Smith E, Khan-Tareen H, Kareddy V, Kao JPY, Kanold PO (2017) Abnormal Development of the Earliest Cortical Circuits in a Mouse Model of Autism Spectrum Disorder. Cell Rep 18:1100–1108.

  • Nelken I (2004) Processing of complex stimuli and natural scenes in the auditory cortex. Curr Opin Neurobiol 14:474–480.

  • Nicolini C, Fahnestock M (2018) The valproic acid-induced rodent model of autism. Exp Neurol 299:217–227.

  • Porcaro C, Zappasodi F, Barbati G, Salustri C, Pizzella V, Rossini PM, Tecchio F (2006) Fetal auditory responses to external sounds and mother’s heart beat: detection improved by Independent Component Analysis. Brain research 1101:51–58.

  • Roullet FI, Lai JK, Foster JA (2013) In utero exposure to valproic acid and autism--a current review of clinical and animal studies. Neurotoxicol Teratol 36:47–56.

  • Sanes DH, Bao S (2009) Tuning up the developing auditory CNS. Curr Opin Neurobiol 19:188–199.

  • Schleussner E, Schneider U, Kausch S, Kahler C, Haueisen J, Seewald HJ (2001) Fetal magnetoencephalography: a non-invasive method for the assessment of fetal neuronal maturation. BJOG 108:1291–1294.

  • Schneider U, Schleussner E, Haueisen J, Nowak H, Seewald HJ (2001) Signal analysis of auditory evoked cortical fields in fetal magnetoencephalography. Brain Topogr 14:69–80.

  • Sheikh A, Meng X, Liu J, Mikhailova A, Kao JPY, McQuillen PS, Kanold PO (2018) Neonatal Hypoxia-Ischemia Causes Functional Circuit Changes in Subplate Neurons. Cereb Cortex.

  • Stoner R, Chow ML, Boyle MP, Sunkin SM, Mouton PR, Roy S, Wynshaw-Boris A, Colamarino SA, Lein ES, Courchesne E (2014) Patches of disorganization in the neocortex of children with autism. N Engl J Med 370:1209–1219.

  • Thompson BL, Levitt P, Stanwood GD (2009) Prenatal exposure to drugs: effects on brain development and implications for policy and education. Nature reviews Neuroscience 10:303–312.

  • Tian N, Copenhagen DR (2003) Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39:85–96.

  • Tolner EA, Sheikh A, Yukin AY, Kaila K, Kanold PO (2012) Subplate neurons promote spindle bursts and thalamocortical patterning in the neonatal rat somatosensory cortex. J Neurosci 32:692–702.

  • Viswanathan S, Bandyopadhyay S, Kao JP, Kanold PO (2012) Changing microcircuits in the subplate of the developing cortex. J Neurosci 32:1589–1601.

  • Viswanathan S, Sheikh A, Looger LL, Kanold PO (2016) (2017) Molecularly Defined Subplate Neurons Project Both to Thalamocortical Recipient Layers and Thalamus. Cereb Cortex 27:4759–4768.

  • Voegtline KM, Costigan KA, Pater HA, DiPietro JA (2013) Near-term fetal response to maternal spoken voice. Infant Behav Dev 36:526–533.

  • Wakai RT, Leuthold AC, Martin CB (1996) Fetal auditory evoked responses detected by magnetoencephalography. Am J Obstet Gynecol 174:1484–1486.

  • Wang WZ, Oeschger FM, Montiel JF, Garcia-Moreno F, Hoerder-Suabedissen A, Krubitzer L, Ek CJ, Saunders NR, Reim K, Villalon A, Molnar Z (2011) Comparative aspects of subplate zone studied with gene expression in sauropsids and mammals. Cereb Cortex 21:2187–2203.

  • Werner LA (2007) Issues in human auditory development. J Commun Disord 40:275–283.

  • Wess JM, Isaiah A, Watkins PV, Kanold PO (2017) Subplate neurons are the first cortical neurons to respond to sensory stimuli. Proceedings of the National Academy of Sciences of the United States of America 114:12602–12607.

  • Yang JW, Hanganu-Opatz IL, Sun JJ, Luhmann HJ (2009) Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J Neurosci 29:9011–9025.

  • Zappasodi F, Tecchio F, Pizzella V, Cassetta E, Romano GV, Filligoi G, Rossini PM (2001) Detection of fetal auditory evoked responses by means of magnetoencephalography. Brain research 917:167–173.

  • Zhao C, Kao JP, Kanold PO (2009) Functional excitatory microcircuits in neonatal cortex connect thalamus and layer 4. J Neurosci 29:15479–15488.

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