Properties of Persistent Postnatal Cortical Subplate Neurons

Torres-Reveron, Juan; Friedländer, Michael

doi:10.1523/jneurosci.1536-07.2007

Cited by 68 publications

(75 citation statements)

References 86 publications

(101 reference statements)

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“…Most subplate cells apoptose perinatally and postnatally, but some persist into adulthood as a thin layer (layer VIb) between cortex and white matter (Kostovic and Rakic, 1980;Al-Ghoul and Miller, 1989;Chun and Shatz, 1989;Kostovic and Rakic, 1990;Allendoerfer and Shatz, 1994). Differences in perikaryon location, anatomy, and physiology of 5-HT 3A -EGFP-positive WMICs and layer VIb neurons (Valverde and Facal-Valverde, 1988;Friauf et al, 1990;Luhmann et al, 2000;Hanganu et al, 2001Hanganu et al, , 2002Hanganu et al, , 2009Torres-Reveron and Friedlander, 2007;Kilb et al, 2008;Zhao et al, 2009) support the notion that in rodents GABAergic WMICs descend from lower intermediate zone GABAergic cells and not from subplate neurons (DeDiego et al, 1994;Tamamaki et al, 1997Tamamaki et al, , 2003aTamamaki et al, , 2003bOkhotin and Kalinichenko, 2003). In summary, we described here 5-HT 3A receptor-bearing GABAergic WMICs that resemble cortical interneurons based on morphology, interneuron marker expression, and electrophysiological features.…”

Section: Discussionmentioning

confidence: 68%

“…Basic morphological features of WMICs were indicative of a neuronal phenotype (Neuburger, 1922;Lund et al, 1975;Kostovic and Rakic, 1980;Chun and Shatz, 1989;Muller, 1994;Shering and Lowenstein, 1994;Eastwood and Harrison, 2005;Friedlander and Torres-Reveron, 2009;Loup et al, 2009), a notion that was also supported by electron microscopy data (Valverde and Facal-Valverde, 1988). While there is ample information about the immunohistochemical signature of WMICs, such as the expression of GABA and specific GABAergic interneuron markers (Innis et al, 1979;Adrian et al, 1983;Schmechel et al, 1984;Shults et al, 1984;Somogyi et al, 1984;Chan-Palay et al, 1985;Sandell, 1986;Yan et al, 1996;Bayraktar et al, 1997;Tao et al, 1999;Suárez-Solá et al, 2009), only a few studies focused on electrophysiological properties of WMICs (Clancy et al, 2001;Torres-Reveron and Friedlander, 2007;Friedlander and Torres-Reveron, 2009). The main hindrance for the identification of WMICs in acute slices is their scarcity.…”

Section: Introductionmentioning

confidence: 93%

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5-HT_3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

et al. 2011

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In addition to axons and surrounding glial cells, the corpus callosum also contains interstitial neurons that constitute a heterogeneous cell population. There is growing anatomical evidence that white matter interstitial cells (WMICs) comprise GABAergic interneurons, but so far there is little functional evidence regarding their connectivity. The scarcity of these cells has hampered electrophysiological studies. We overcame this hindrance by taking recourse to transgenic mice in which distinct WMICs expressed enhanced green fluorescence protein (EGFP). The neuronal phenotype of the EGFP-labeled WMICs was confirmed by their NeuN positivity. The GABAergic phenotype could be established based on vasoactive intestinal peptide and calretinin expression and was further supported by a firing pattern typical for interneurons. Axons and dendrites of many EGFP-labeled WMICs extended to the cortex, hippocampus, and striatum. Patch-clamp recordings in acute slices showed that they receive excitatory and inhibitory input from cortical and subcortical structures. Moreover, paired recordings revealed that EGFP-labeled WMICs inhibit principal cells of the adjacent cortex, thus providing unequivocal functional evidence for their GABAergic phenotype and demonstrating that they are functionally integrated into neuronal networks.

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Section: Discussionmentioning

confidence: 68%

Section: Introductionmentioning

confidence: 93%

5-HT_3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

et al. 2011

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“…In fact, in more matured brains, most of the SPns are RS-type (Torres-Reveron and Friedlander 2007). We therefore speculate that a subset of SStype SPns are immature cortical neurons and might become RS-type SPns during early postnatal days.…”

Section: Discussionmentioning

confidence: 79%

“…This paired-pulse response was comparable to the findings of SPns in the visual cortex of P10-20 rats (Torres-Reveron and Friedlander 2007). Functionally speaking, paired-pulse facilitation implied the reduction in presynaptic transmitter release (Lu et al 2006;Torres-Reveron and Friedlander 2007). To further support this notion, we applied MK-801, an irreversible, use-dependent, NMDA receptor blocker to the SPns in rats of different ages (Fig.…”

Section: Maturation Of Passive and Active Membrane Properties Of Subpmentioning

confidence: 93%

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Evidence for structural and functional changes of subplate neurons in developing rat barrel cortex

Liao

Lee

2011

Brain Struct Funct

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In the developing sensory cortex, the subplate could serve as a transient relay station between the thalamus and cortical plate and assists the formation of thalamocortical projection. While the thalamus-layer IV connection is formed, the thalamic activation of subplate is diminished. In the present study, we aimed to explore the mechanism which may attribute to the decline of subplate activity. To resolve this issue, the developmental changes of subplate neurons (SPns) in rat somatosensory cortex were examined during the first two postnatal weeks which covers the stages prior and subsequent to the establishment of thalamocortical connection. During development, more SPns exhibited regular-spiking firing pattern and the membrane properties of SPns displayed a continual trend of maturation. In the meantime, the excitability of SPns decreased as revealed by increasing rheobase and rightwardly shifted frequency-current curves. On the other hand, increasing paired-pulse ratio and slowing MK-801 blocking rate were noted during development, implying the reduction of presynaptic transmitter release. Morphologically, the size of SPn soma increased with age while the shape became flat. The total length, branching nodes and segments of dendrites increased significantly during the first week. However, after peaking around day 10, these values decreased, implying a pruning process. Our findings here propose that the reduction of neuronal excitability, synaptic transmission and dendritic complexity may attribute to the decline of functional connectivity between thalamus and subplate and reduction of subplate activity while the thalamocortical pathway is established.

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Differential distribution of neurons in the gyral white matter of the human cerebral cortex

García-Marín

Blázquez-Llorca

Toledo-Rodriguez

et al. 2010

J of Comparative Neurology

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The neurons in the cortical white matter (WM neurons) originate from the first set of postmitotic neurons that migrates from the ventricular zone. In particular, they arise in the subplate that contains the earliest cells generated in the telencephalon, prior to the appearance of neurons in gray matter cortical layers. These cortical WM neurons are very numerous during development, when they are thought to participate in transient synaptic networks, although many of these cells later die, and relatively few cells survive as WM neurons in the adult. We used light and electron microscopy to analyze the distribution and density of WM neurons in various areas of the adult human cerebral cortex. Furthermore, we examined the perisomatic innervation of these neurons and estimated the density of synapses in the white matter. Finally, we examined the distribution and neurochemical nature of interneurons that putatively innervate the somata of WM neurons. From the data obtained, we can draw three main conclusions: first, the density of WM neurons varies depending on the cortical areas; second, calretinin-immunoreactive neurons represent the major subpopulation of GABAergic WM neurons; and, third, the somata of WM neurons are surrounded by both glutamatergic and GABAergic axon terminals, although only symmetric axosomatic synapses were found. By contrast, both symmetric and asymmetric axodendritic synapses were observed in the neuropil. We discuss the possible functional implications of these findings in terms of cortical circuits.

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Properties of Persistent Postnatal Cortical Subplate Neurons

Cited by 68 publications

References 86 publications

5-HT_3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

5-HT_3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

Evidence for structural and functional changes of subplate neurons in developing rat barrel cortex

Differential distribution of neurons in the gyral white matter of the human cerebral cortex

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Properties of Persistent Postnatal Cortical Subplate Neurons

Cited by 68 publications

References 86 publications

5-HT3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

5-HT3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

Evidence for structural and functional changes of subplate neurons in developing rat barrel cortex

Differential distribution of neurons in the gyral white matter of the human cerebral cortex

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5-HT_3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks

5-HT_3AReceptor-Bearing White Matter Interstitial GABAergic Interneurons Are Functionally Integrated into Cortical and Subcortical Networks