Do subplate neurons comprise a transient population of cells in developing neocortex of rats?

Abstract

Studies were undertaken to determine whether neurons of the subplate layer represent a transient or stable population of cells in developing neocortex of rat. The first set of studies sought to determine the fraction of subplate neurons that is lost during early postnatal development. The optical dissector method was used to analyze fluorescently stained material in animals the age of postnatal day 0 (P0) to P40. These results demonstrate a reduction of slightly less than half of the total number of subplate neurons from P0 to P40. Counts of labeled cells in littermates at varied ages after [(3)H]thymidine or BRDU treatment on gestational day 14 (G14 - birthdate of occipital subplate neurons) or G18 (birthdate of layers III-IV neurons) demonstrate loss of approximately 50% of neurons in the subplate layer between P0 and P40, somewhat greater than the loss of neurons from cortical layers III-IV. The second set of studies investigated whether subplate neurons display cellular atrophy during postnatal development. Analysis of subplate neurons injected intracellularly with Lucifer yellow in fixed slice preparations indicates no reduction in soma size, number of dendrites, or extent of dendritic fields of subplate neurons taken from animals age P0 to P60. The third set of studies investigated whether functional markers of subplate neurons are reduced during postnatal development. Analysis of tissue stained histochemically for cytochrome oxidase or acetylcholinesterase, or stained immunocytochemically for GABA, somatostatin, or neuropeptide Y, demonstrate a remarkable loss of expression of staining patterns from late gestational ages to P20. These data demonstrate that, although subplate neurons seem not to be a transient population of cells in the usual sense of being eliminated by cell death or structural atrophy, the loss of histochemical and immunocytochemical markers indicates that they may be a functionally transient population of cells.

Functional Thalamocortical Synapse Reorganization from Subplate to Layer IV during Postnatal Development in theReeler-Like Mutant Rat (Shaking Rat Kawasaki)

“…In rats, however, a considerable fraction of subplate neurons seem to survive like other cortical plate cells (Robertson et al, 2000). These anatomical results are consistent with BrdU labeling, suggesting the survival of subplate and superplate neurons at P10.…”

Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974)

“…Initial studies (Sugita, 1917) had already demonstrated that the rodent subplate is not really a transient structure, but a well defined layer (VIb or VII) which persists as a part of the 'traditional' cortex throughout the rodent lifespan. In recent years, the rodent subplate ⁄ layer VII has been increasingly recognized as a 'special case' probably characteristic for this specific group of mammals and with significantly different developmental history and postnatal roles in comparison with primates and humans (Reep & Goodwin, 1988;Reep, 2000;Valverde et al 1989Valverde et al , 1995Robertson et al 2000;Clancy & Cauller, 1999;Clancy et al 2001Clancy et al , 2009Arias et al 2002;Tomioka et al 2005).…”

Properties of Persistent Postnatal Cortical Subplate Neurons

“…A period of programmed cell death in embryonic SP neurons has been demonstrated (Allendoerfer and Shatz, 1994;Robertson et al, 2000). To determine whether similar changes occur in the SP and WM regions, cells were immunolabeled using MAP-2 and NeuN between P2 and P30.…”

“…Alternatively, because some SP neurons (ϳ20%) survive, they may perform other functions in the postnatal neocortex, becoming integrated into the microcircuitry of the six major cortical laminase. Data in support of this alternative include the following: fluorescent tracers applied to layer I in juvenile and adult rats retrogradely label somata of SP and WM cells (Clancy and Cauller, 1999); SP neurons that survive programmed cell death do not show evidence of atrophy of their dendritic trees or nuclear shrinkage (Robertson et al, 2000); and SP cells receive functional synaptic input during the first days [postnatal day 0 (P0) to P3] of postnatal life in the rat (Hanganu et al, 2001(Hanganu et al, , 2002. However, the fate and functional properties of these cells beyond the immediate perinatal period are unknown.…”