Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex

Luhmann, Heiko J.; Kilb, Werner; Hanganu‐Opatz, Ileana L.

doi:10.3389/neuro.05.019.2009

Cited by 88 publications

(88 citation statements)

References 93 publications

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“…Interstitial white matter neurons thinly populate the superficial white matter of healthy adult brains (Hardiman et al, 1988;Ramó n y Cajal, 1995;Suárez-Solá et al, 2009;García-Marín et al, 2010). They are believed to be remnants of the embryonic subplate (Chun and Shatz, 1989) that have either failed to undergo programmed cell death (Luhmann et al, 2009) or are the result of disrupted migrational processes (Chevassus-au-Louis and Represa, 1999). Their density is increased at the gyral crown relative to the sulcus (Akbarian et al, 1993), which is consistent with our finding of increased blurring in the gyrus.…”

Section: Discussionsupporting

confidence: 79%

Individual Differences in Verbal Abilities Associated with Regional Blurring of the Left Gray and White Matter Boundary

Blackmon¹,

Halgren²,

Barr³

et al. 2011

J. Neurosci.

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Blurring of the cortical gray and white matter border on MRI is associated with normal aging, pathological aging, and the presence of focal cortical dysplasia. However, it remains unclear whether normal variations in signal intensity contrast at the gray and white matter junction reflect the functional integrity of subjacent tissue. This study explores the relationship between verbal abilities and gray and white matter contrast (GWC) in healthy human adults. Participants were scanned at 3 T MRI and administered standardized measures of verbal expression and verbal working memory. GWC was estimated by calculating the non-normalized T1 image intensity contrast above and below the cortical gray/white matter interface. Spherical averaging and whole-brain correlational analyses were performed. Sulcal regions exhibited higher contrast compared to gyral regions. We found a strongly lateralized and regionally specific profile with reduced verbal expression abilities associated with blurring in left hemisphere inferior frontal cortex and temporal pole. Reduced verbal working memory was associated with blurring in widespread left frontal and temporal cortices. Such lateralized and focal results provide support for GWC as a measure of regional functional integrity and highlight its potential role in probing the neuroanatomical substrates of cognition in healthy and diseased populations.

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Section: Discussionsupporting

confidence: 79%

Individual Differences in Verbal Abilities Associated with Regional Blurring of the Left Gray and White Matter Boundary

Blackmon¹,

Halgren²,

Barr³

et al. 2011

J. Neurosci.

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“…Anatomical and electrophysiological criteria for identification of SP neurons were previously established in animal and human research (32)(33)(34). SP neurons have greater cell diameters than the postmitotic neurons migrating through the SP zone ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Connexin hemichannels contribute to spontaneous electrical activity in the human fetal cortex

Moore

Zhou

Sirois

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Before the human cortex is able to process sensory information, young postmitotic neurons must maintain occasional bursts of action-potential firing to attract and keep synaptic contacts, to drive gene expression, and to transition to mature membrane properties. Before birth, human subplate (SP) neurons are spontaneously active, displaying bursts of electrical activity (plateau depolarizations with action potentials). Using whole-cell recordings in acute cortical slices, we investigated the source of this early activity. The spontaneous depolarizations in human SP neurons at midgestation (17-23 gestational weeks) were not completely eliminated by tetrodotoxin-a drug that blocks action potential firing and network activity-or by antagonists of glutamatergic, GABAergic, or glycinergic synaptic transmission. We then turned our focus away from standard chemical synapses to connexinbased gap junctions and hemichannels. PCR and immunohistochemical analysis identified the presence of connexins (Cx26/ Cx32/Cx36) in the human fetal cortex. However, the connexin-positive cells were not found in clusters but, rather, were dispersed in the SP zone. Also, gap junction-permeable dyes did not diffuse to neighboring cells, suggesting that SP neurons were not strongly coupled to other cells at this age. Application of the gap junction and hemichannel inhibitors octanol, flufenamic acid, and carbenoxolone significantly blocked spontaneous activity. The putative hemichannel antagonist lanthanum alone was a potent inhibitor of the spontaneous activity. Together, these data suggest that connexin hemichannels contribute to spontaneous depolarizations in the human fetal cortex during the second trimester of gestation.UP states | brain development | glutamate | GABA | preterm infants I n the adult brain, neuronal network activity is essentially driven by chemical synapses (1-3), whereas in the developing brain, neuronal activity is largely independent of sensory inputs (4-6). Membrane depolarizations during the earliest stages of brain development play an important role in the transition between the immature and mature signaling properties of neurons, as well as in shaping the mature functional neuronal network (7)(8)(9)(10)(11)(12). Recent studies performed in the rodent model of cortical development have implicated subplate (SP) neurons as key regulators of early electrical activity and network oscillations (13,14). Their essential role in the establishment of thalamocortical connections and cortical columns (15-18), extensive connectivity within the early synaptic network (19-21), and dense gap junction coupling (22, 23), as well as the abundant innervation by neuromodulatory transmitter systems (24, 25), put SP neurons in an ideal position to synchronize cortical activity during early development. Disruptions to the SP zone during development have been implicated in several major neurological disorders including schizophrenia, cerebral palsy, and autism (26,27).Most of the physiological studies on SP neurons have been performed in ...

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“…The situation is different in P0 -P1 animals, since layer II/III and, most likely, layer IV have not yet been formed at this early age. In somatosensory cortex of newborn rodents, the thalamic input predominantly innervates the subplate and is subsequently relayed to different cortical layers (for review, see Luhmann et al, 2009;Kanold and Luhmann, 2010). Accordingly in P0 -P1 rats, an LTP was observed in both upper cortical layers and deep layers (Fig.…”

Section: Discussionmentioning

confidence: 99%

Long-Term Potentiation in the Neonatal Rat Barrel Cortex In Vivo

Yang²,

Sun³

et al. 2012

Journal of Neuroscience

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Long-term potentiation (LTP) is important for the activity-dependent formation of early cortical circuits. In the neonatal rodent barrel cortex, LTP has been studied only in vitro. We combined voltage-sensitive dye imaging with extracellular multielectrode recordings to study whisker stimulation-induced LTP in the whisker-to-barrel cortex pathway of the neonatal rat barrel cortex in vivo. Single whisker stimulation at 2 Hz for 10 min induced an age-dependent expression of LTP in postnatal day (P) 0 to P14 rats, with the strongest expression of LTP at P3-P5. The magnitude of LTP was largest in the activated barrel-related column, smaller in the surrounding septal region, and no LTP could be observed in the neighboring barrel. Current source density analyses revealed an LTP-associated increase of synaptic current sinks in layer IV/lower layer II/III at P3-P5 and in the cortical plate/upper layer V at P0 -P1. Our study demonstrates for the first time an age-dependent and spatially confined LTP in the barrel cortex of the newborn rat in vivo.

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Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex

Cited by 88 publications

References 93 publications

Individual Differences in Verbal Abilities Associated with Regional Blurring of the Left Gray and White Matter Boundary

Individual Differences in Verbal Abilities Associated with Regional Blurring of the Left Gray and White Matter Boundary

Connexin hemichannels contribute to spontaneous electrical activity in the human fetal cortex

Long-Term Potentiation in the Neonatal Rat Barrel Cortex In Vivo

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