Dynamic integration of subplate neurons into the cortical barrel field circuitry during postnatal development in the Golli‐tau‐eGFP (GTE) mouse

Abstract

In the Golli-tau-eGFP (GTE) transgenic mouse the reporter gene expression is largely confined to the layer of subplate neurons (SPn), providing an opportunity to study their intracortical and extracortical projections. In this study, we examined the thalamic afferents and layer IV neuron patterning in relation to the SPn neurites in the developing barrel cortex in GTE mouse at ages embryonic day 17 (E17) to postnatal day 14 (P14). Serotonin transporter immunohistochemistry or cytochrome oxydase histochemistry was used to reveal thalamic afferent patterning. Bizbenzimide staining identified the developing cytoarchitecture in coronal and tangential sections of GTE brains. Enhanced green fluorescent protein (GFP)-labelled neurites and thalamic afferents were both initially diffusely present in layer IV but by P4-P6 both assumed the characteristic periphery-related pattern and became restricted to the barrel hollows. This pattern gradually changed and by P10 the GFP-labelled neurites largely accumulated at the layer IV-V boundary within the barrel septa whereas thalamic afferents remained in the hollows. To investigate whether this reorganisation is dependent on sensory input, the whiskers of row 'a' or 'c' were removed at P0 or P5 and the organisation of GFP-labelled neurites in the barrel cortex was examined at P6 or P10. In the contralateral region corresponding to row 'a' or 'c' the lack of hollow to septa rearrangement of the GFP-labelled neurites was observed after P0 row removal at P10 but not at P6. Our findings suggest a dynamic, sensory periphery-dependent integration of SPn neurites into the primary somatosensory cortex during the period of barrel formation.

Development, evolution and pathology of neocortical subplate neurons

“…Some neurites subsequently reach into barrel septa while avoiding barrel hollows, whereas others remain restricted to below layer 4 at P10 (REF. 69). This process is experience dependent: removal of a row of whiskers at birth delayed the relocation of fibres from barrel hollow to barrel septum 69 (FIG.…”

“…69). This process is experience dependent: removal of a row of whiskers at birth delayed the relocation of fibres from barrel hollow to barrel septum 69 (FIG. 4).…”

“…In fact, in mice, subplate neurites undergo several stages of pruning or remodelling. Shortly after birth, some subplate cell neurites extend to the marginal zone 68,69 . With further maturation, neurites from this group of cells coalesce into barrel hollows in mouse primary sensory cortex at P6 but then further retract until they end below layer 4 by P8.…”

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

“…The section was fixed in 4% paraformaldehyde for 24 h and washed in 0.01 M PBS. Serial 200-m-thick tangential slices of flattened barrel cortex were cut on a cryotome and stained for serotonin transporter (5-HTT) using a modification of a previously published protocol (Piñon et al, 2009). Slices were washed with PBS, followed by blocking and permeabilization with 7% normal goat serum and 0.8% Triton in PBS [2 h at room temperature (RT)] and incubated overnight at RT in rabbit anti-serotonin transporter polyclonal antibody (1:1000, AB9726; Millipore Bioscience Research Reagents).…”

Subplate in the developing cortex of mouse and human

“…They are also necessary for the maturation of inhibition in cortical layer 4 in areas innervated by the thalamus (Kanold & Shatz, 2006), and drive oscillations in the gap junction-coupled early cortical syncytium (Dupont et al 2006). During development, subplate neurons are electrically active and capable of firing action potentials (Hanganu et al 2001;Moore et al 2009) while incorporating, at least transiently, into the cortical and subcortical circuitry (Friauf & Shatz, 1991;Higashi et al 2002Higashi et al , 2005Kanold et al 2003;Piñ on et al 2009). Subplate neurons develop both intracortical and subcortical projections (Allendoerfer & Shatz, 1994).…”