Emerging Complexity of Layer I in Human Cerebral Cortex

Abstract

In this study we examine possible origins and migratory routes of human cortical neurons, with special emphasis on the preplate and layer I. In embryonic stages, two main cell types, Cajal-Retzius cells, and cells labeled with interneuron markers (calretinin, calbindin and GABA), were present in the preplate layer. In addition, a number of preplate GABAergic cells co-expressed either Nkx2.1 or Dlx transcription factors, findings consistent with their origin in the ganglionic eminence and subsequent tangential migration to the layer I. The orientation of the leading process indicates that some of these cells descend to the cortical plate. However, the finding of radially oriented GABAergic, NKX2.1 + and DLX + cells in the cortical ventricular zone, argues that, unlike in rodents, a significant subpopulation of these cells originates in the cortical ventricular zone. In embryonic stages, expression of Reelin in Cajal-Retzius cells as well as Reelin/DLX2 + cells in the embryonic ganglionic eminence and the olfactory region, suggest that these cells in human may have diverse origins. In later fetal stages in human (17-22 gestational weeks) layer I and the newly formed subpial granular layer, contained a population of small interneurons that originated mainly in the lateral ganglionic eminence, since the majority of these cells were double-labeled with DLX/GABA, and rarely with NKX2.1/GABA. Therefore, neurons in the human cortical layer I are heterogeneous, with more complex origin and migratory routes than in rodents. In addition to the ganglionic eminence, both the expended subventricular zone and subpial granular layer, contribute to the neuronal population of the developing layer I and underlining cortical plate.

Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell–derived neocortex

“…2 O-Q), the hESC-derived NE recapitulated the continuous self-formation of the cortex and LGE (striatum anlage) in adjacent positions as seen in vivo. The origin of human cortical interneurons may be an intriguing topic to be studied using this system, because they are suggested to arise not only from the subplallium but also from the cortical VZ/SVZ (31,32) in the human fetus.…”

Generation of human cortical neurons from a new immortal fetal neural stem cell line

“…GABAergic interneurons that are born in the ventral telencephalon reach the cortex by tangential migration [30; 44]. Interestingly, recent data have suggested that in primates, the majority of the cortical interneurons originate in the cortical ventricular and subventricular zones, and that there is a portion contributed by the ganglionic eminence of the ventral telencephalon [45][46][47]. We show here that differentiated hc-NSCs give rise to glutamatergic (10%) and a smaller population of GABAergic cells (about 1%).…”

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

“…These findings clearly show that an initial description of the subplate as layer VIb in the fetal cat (Marin-Padilla, 1971, 1972, 1978 was overly simplified and that it at best can only be applied to the first (earliest generated) wave of subplate neurons. For a detailed criticism of this original concept of the primordial plexiform layer (or preplate) see a recent review (Bystron et al 2008) as well as a number of recent studies which pointed out a previously unsuspected complexity of the early neocortical anlage in humans (Zecevic et al 1999;Meyer et al 2000;Zecevic & Rakic, 2001;Rakic & Zecevic, 2003;Bystron et al 2005Bystron et al , 2006 as well as in rodents (Rickmann et al 1977;Hevner et al 2003;Jimé nez et al 2003;Bielle et al 2005;García-Moreno et al 2007). …”