Rostro-Caudal and Caudo-Rostral Migrations in the Telencephalon: Going Forward or Backward?

Abstract

The generation and differentiation of an appropriate number of neurons, as well as its distribution in different parts of the brain, is crucial for the proper establishment, maintenance and plasticity of neural circuitries. Newborn neurons travel along the brain in a process known as neuronal migration, to finalize their correct position in the nervous system. Defects in neuronal migration produce abnormalities in the brain that can generate neurodevelopmental pathologies, such as autism, schizophrenia and intellectual disability. In this review, we present an overview of the developmental origin of the different telencephalic subdivisions and a description of migratory pathways taken by distinct neural populations traveling long distances before reaching their target position in the brain. In addition, we discuss some of the molecules implicated in the guidance of these migratory paths and transcription factors that contribute to the correct migration and integration of these neurons.

Concentric ring topology of mammalian cortical sectors and relevance for patterning studies

“…Neither Remedios et al () nor recently Ruiz‐Reig and Studer (), who accepted the doubtful dorsopallial interpretation of NLOT origin, seem to be aware of the interposed meso‐ and allocortical rings, since they do not discuss the interruption of these rings that their thesis would require (check Figures and ). If no part of the amygdalar neuroepithelium expresses Emx2 , as was stated by these authors, then it is conceivable that the NLOT source relates instead to the neighboring prethalamic eminence—check Figure —which does express Emx2 and other required markers such as Tbr1 (see figure 5D of Ruiz‐Reig & Studer, ). Omission of the mesocortex concept has led in this notable case (because the paper is very well done) to an apparently faulty conclusion being published in a major journal and surviving a number of years without realistic criticism.…”

“…Remedios et al (2007) traced the progenitor area for the amygdalar nucleus of the lateral olfactory tract (NTOL) as being singularly Emx2positive. This area appears roughly at the transition between hippocampus and amygdala (or between amygdala and prethalamic eminence; see inset to Figure 1c) and accordingly lies very far away from the dorsopallial cortex (anlage of neocortex), but was nevertheless presented as a "dorsal pallium area" (NTOL in Figure 1c figure 5D of Ruiz-Reig & Studer, 2017). Omission of the mesocortex concept has led in this notable case (because the paper is very well done) to an apparently faulty conclusion being published in a major journal and surviving a number of years without realistic criticism.…”

“…Is there an analogous allocortex-like and pallial amygdala-like dorsoventral structure? Notably, the PTHE expresses some typical pallium genes, such as Tbr1, Pax6, Lhx5, and Lhx9 (Puelles et al, 2000;Shimogori et al, 2010), and produces tangentially migrating Cajal-Retzius and mitral cell populations that eventually reach the neocortex or the olfactory bulb (review in Puelles, 2011; see also Ruiz-Reig & Studer, 2017;Ruiz-Reig et al, 2016, 2018.…”

“…Within the double ring pallial model, it is wholly impossible topologically that the apparent origin of this migration is neocortical, irrespective of any other data (compare Figure 1a-c). Neither Remedios et al (2007) norrecentlyRuiz-Reig and Studer (2017), who accepted the doubtful dorsopallial interpretation of NLOT origin, seem to be aware of the interposed meso-and allocortical rings, since they do not discuss the interruption of these rings that their thesis would require (checkFigures 1 and 4). If no part of the amygdalar neuroepithelium expresses Emx2, as was stated by these authors, then it is conceivable that the NLOT source relates instead to the neighboring prethalamic eminence-checkFigure 4-which does express Emx2 and other required markers such as Tbr1 (see…”

Identification of amygdala-expressed genes associated with autism spectrum disorder

“…The second phase of assessment consisted of visual analysis of in situ hybridization images from the Allen Developing Brain Atlas at E11.5, E13.5, E15.5, E18.5, and P4 for each of the 80 genes that fulfilled the above criteria. Specifically, at each time point, all sections through the mouse brain were assessed for expression in developing brain regions previously identified by us and others [25][26][27][28][29][30][31][32] to give rise to different nuclei of the amygdala. At E11.5, E13.5, and E15.5, these regions consisted of the telencephalic/diencephalic border region, ventral hypothalamus, and ventral pallial (VP) region of the developing cerebral cortex.…”