Current Status of the Hypothesis of a Claustro-Insular Homolog in Sauropsids

Abstract

The author worked before on the wide problem of the evolution of the vertebrate pallium. He proposed various Bauplan models based in the definition of a set of pallial sectors with characteristic (topologically invariant) mutual relationships and distinct molecular profiles. Out of one of these models, known as the ‘updated tetrapartite pallium model’, a modified definition of the earlier lateral pallium sector (LPall) emerged, which characterized it in mammals as consisting of an unitary claustro-insular transitional (mesocortical) complex intercalated between neocortex or dorsal pallium (DPall) above and olfactory cortex or ventral pallium (VPall) underneath. A distinctive molecular marker of the early-born deep claustral component of the LPall was found to be the transcription factor Nr4a2, which is not expressed significantly in the overlying insular cortex or in adjoining cortical territories (Puelles 2014). Given that earlier comparative studies had identified molecularly and topologically comparable VPall, LPall and DPall sectors in the avian pallium, an avian Nr4a2 probe was applied aiming to identify the reportedly absent avian claustro-insular complex. An early-born superficial subpopulation of the avian LPall that expresses selectively this marker through development was indeed found. This was proposed to be a claustrum homolog, whereas the remaining Nr4a2-negative avian LPall cells were assumed to represent a possible insular homolog (Puelles et al. 2016a). This last notion was supported by comparable selective expression of the mouse insular marker Cyp26b, also found restricted to the avian LPall (Puelles 2017). Some published data suggested that similar molecular properties and structure apply at the reptilian LPall. This analysis was reviewed in Puelles et al. (2017). The present commentary discusses 3-4 years later some international publications accrued in the interval that touch on the claustro-insular homology hypothesis. Some of them are opposed to the hypothesis whereas others corroborate or support it. This raises a number of secondary issues of general interest.

Evolving Views on the Pallium

“…1d), in mammals the lateral pallium produces the insular claustrum and insular cortex, but it does not produce any part of the piriform cortex and the pallial amygdala, while the ventral pallium produces the endopiriform/piriform region (with the exception of a group of migrated cells of the dorsal endopiriform nucleus; migra-tion represented with an arrow in Fig. 1d) and the pallial amygdala [Puelles et al, 2017;Puelles, 2017Puelles, , 2021.…”

Homology of neocortical areas in rats and primates based on cortical type analysis: an update of the Hypothesis on the Dual Origin of the Neocortex

“…Thus, the allocortex develops across vertebrates from two well-defined FMUs (medial and ventral pallia) and the neocortex (sensu stricto and non sensu stricto) from other two FMUs (dorsal and lateral pallia) (Medina et al 2011;Puelles 2017;Suryanarayana et al 2017;Pessoa et al 2019;Puelles et al 2019). The origin of the cerebral cortex across vertebrates in four pallial sectors has been systematized as the Tetrapartite Model of Pallial Development and Evolution by Luis Puelles (Puelles 2017(Puelles , 2021. This model has relevant implications for the Hypothesis on the Dual Origin of the Neocortex because it shows that, contrary to what Sanides and his contemporaries believed [e.g., Filimonoff (1947)], the rings of mammalian neocortex did not appear de novo in mammals out of rudimentary anlagen identified in reptiles but expanded within pallial sectors (lateral and dorsal pallia) that were likely present in the common ancestor of fish and land vertebrates.…”

“…a, Sketch of Fundamental Morphological Units (FMUs) of the mammalian telencephalon according to the Prosomeric Model Rubenstein 1993, 2015;Nieuwenhuys and Puelles 2016;Puelles 2018;Puelles et al 2019). Gray shading indicates pallial FMUs according to the Tetrapartite Model of Pallial Development and Evolution (Puelles 2017(Puelles , 2021. b, Sketch of FMUs of the mammalian pallium showing a hypothetical fifth pallial sector indicated with interrogation sign (?).…”

“…We frame the updated version of the Dual Origin of the Neocortex Hypothesis within two theories/models that explain the development of the neural tube [the Prosomeric Model Rubenstein 1993, 2015;Nieuwenhuys and Puelles 2016;Puelles 2018); see Fig. 8A] and of the cerebral cortex [The Tetrapartite Model of Pallial Development and Evolution (Puelles 2017(Puelles , 2021; see Fig. 8A].…”

Expression of Satb2 in adult brain of key non-mammalian vertebrates: insights from evolution

“…Recently, in amniotes it has been described that the claustrum is identi ed by the expression of different transcription factors, among others Satb2 (Bruguier et al 2020;Puelles 2022). Recently the origin and boundaries of the claustrum has been updated, being developed from the lateropallial domain (Puelles 2014(Puelles , 2017Watson and Puelles 2017), and the elements that compose the claustrum have been reliably identi ed in primates, rodents and sauropsids (Puelles 2014;Watson and Puelles 2017;Binks et al 2019;Puelles 2022). What we observed in the case of this pallial derivative in the models analyzed is that only sarcopterygians showed Satb2 expression in the lateral pallium (present results) in contrast to the lack of pallial expression observed in the rest of the models.…”