Selective early expression of the orphan nuclear receptor Nr4a2 identifies the claustrum homolog in the avian mesopallium: Impact on sauropsidian/mammalian pallium comparisons

Abstract

The transcription factor Nr4a2 was recently revealed as a very early developmental marker of the claustrum (CL) proper in the mouse. The earliest claustral primordium was identified superficially, dorsal to the olfactory cortex, and was subsequently covered by the Nr4a2-negative cells of the insular cortex. Some tangentially migrating claustral derivatives (subplate cells and some endopiriform elements) also expressed this marker. The present study employs the same genetic marker to explore the presence of a comparable pallial division in chicken in which, in principle, the same pallial sectors exist as in mammals. We were indeed able to delineate an early-developing Nr4a2-positive mantle domain at the expected topologic position within the developing chicken lateral pallium. In the chicken as well as in the turtle (from data in the literature), the earliest postmitotic lateropallial cells likewise express Nr4a2 and occupy a corticoid superficial stratum of the mesopallium, which is clearly comparable in spatial and chronological profile to the mouse CL. Other cells produced in this pallial sector include various tangentially migrating Nr4a2-labeled derivatives as well as Nr4a2-negative and Nr4a2-positive local deeper subpopulations that partially interdigitate, forming mesopallial core and shell populations. We hold that the deep avian and reptilian mesopallial formation developing under the superficial corticoid CL homolog represents a field homolog of the insula, although additional studies are required to underpin this hypothesis.

Comments on the Updated Tetrapartite Pallium Model in the Mouse and Chick, Featuring a Homologous Claustro-Insular Complex

“…This finding implied a sharp molecular heterogeneity within the classic lateral pallium, which was traced through all gnathostomes investigated so far. This result was first reported in mouse, chick, turtle, and frog material by Smith-Fernández et al [1998], and it was subsequently corroborated by the studies cited above, among others, and complemented recently by additional data reported by Hirata [2012-2014], Dugas-Ford et al [2012], Jarvis et al [2013], and Puelles et al [2016aPuelles et al [ , 2017, irrespectively of the fact that some of these authors interpreted such data in alternative ways [see comments in Puelles et al, 2017].…”

“…Apart from labeling separately sets of subplate and infragranular isocortical neurons and some subicular hippocampal populations, Nr4a2 labels the laterodorsal and ventromedial parts of the claustrum we had identified previously (these entities actually represent the claustrum proper and the subclaustral part of the subplate, respectively [Puelles, 2014]), as well as the dorsal endopiriform nucleus, but it does not label the olfactory cortex or the ventral endopiriform nucleus or any part of the pallial amygdala [Puelles, 2014;Puelles et al, 2016a;Watson and Puelles, 2017]. These new data (particularly the differential Nr4a2 labeling of the dorsal and ventral endopiriform nuclei), jointly with data from Gorski et al [2002] and Tole et al [2005], corroborated that the molecular differences between VPall and LPall remain an incontestable fact, requiring at least a tetrapartite solution for the fundamental causal organization of the pallium.…”

“…The solution offered was the updated tetrapartite pallium model, in which the whole olfactory cortex and most of the pallial amygdala were ascribed to the VPall, while the claustro-insular complex represents the redefined LPall, which probably also includes the perirhinal cortex, but does not contain amygdalar elements (Fig. 1c, 3d) [Puelles, 2014;Puelles et al, 2016a]. Unfortunately, because of these new definitions of VPall and LPall, there arise some semantic diffi-culties [Wullimann, 2017] that will be commented on in the next section.…”

Contribution of Genoarchitecture to Understanding Hippocampal Evolution and Development

“…However, the expression of conserved TF and other regulatory proteins during the development of the chicken is offering some light for that complex endeavor. In chicken, all APH subdivisions express Lmo4, ER81, and Lmo3 in different layers [Gupta et al, 2012;Abellán et al, 2014], but only the lateral APH (APHl or DL) shows distinct and high expression of Nr4a2/Nurr1 during middle stages of development [Puelles et al, 2016a]. This suggests that avian APHl/DL is comparable to the Sub, while the medial parts of avian APH (APHm+i/DM) may represent the CA1-like field.…”

“…Published data in the developing pallium of chicken on Prox1, Lmo4, and Lmo3 [Abellán et al, 2014], together with available data on ER81 [Gupta et al, 2012;Suzuki and Hirata, 2014] and Nr4a2/Nurr1 [Puelles et al, 2016a], allow the identification of some subdivisions roughly comparable to those in the mouse ( Table 2 ; Fig. 1 ).…”