Distinct Development of the Cerebral Cortex in Platypus and Echidna

Abstract

Both lineages of the modern monotremes have distinctive features in the cerebral cortex, but the developmental mechanisms that produce such different adult cortical architecture remain unknown. Similarly, nothing is known about the differences and/or similarities between monotreme and therian cortical development. We have used material from the Hill embryological collection to try to answer key questions concerning cortical development in monotremes. Our findings indicate that gyrencephaly begins to emerge in the echidna brain shortly before birth (crown-rump length 12.5 mm), whereas the cortex of the platypus remains lissencephalic throughout development. The cortices of both monotremes are very immature at the time of hatching, much like that seen in marsupials, and both have a subventricular zone (SubV) within both the striatum and pallium during post-hatching development. It is particularly striking that in the platypus, this region has an extension from the palliostriatal angle beneath the developing trigeminoreceptive part of the somatosensory cortex of the lateral cortex. The putative SubV beneath the trigeminal part of S1 appears to accommodate at least two distinct types of cell and many mitotic figures and (particularly in the platypus) appears to be traversed by large numbers of thalamocortical axons as these grow in. The association with putative thalamocortical fibres suggests that this region may also serve functions similar to the subplate zone of Eutheria. These findings suggest that cortical development in each monotreme follows distinct paths from at least the time of birth, consistent with a long period of independent and divergent cortical evolution.

Neural progenitors, patterning and ecology in neocortical origins

“…The subplate is barely discernible in marsupials and increases in complexity as the neocortex expands in size in different species ( Aboitiz et al, 2005 ; Montiel et al, 2011 ). In monotremes, a subplate-like structure has been identified in the lateral hemisphere that is traversed by thalamocortical axons ( Ashwell and Hardman, 2012 ). In reptiles, subplate markers appear scattered in the superficial cell layer of the turtle dorsal cortex, while markers of the deep neocortical layer VI are found in the deep cellular layer of the dorsal cortex.…”

“…On the other hand, a SVZ containing intermediate progenitors is still lacking or is minimal in most reptiles, but appears in the subpallium of crocodiles (phylogenetically close to birds) and is maximally expressed in the embryonic avian nidopallium. The SVZ is also present in the hyperpallium of some birds who have developed this structure, possibly associated to binocularity (see below; Charvet et al, 2009 ; Cheung et al, 2010 ; Heesy and Hall, 2010 ; Aboitiz, 2011 ; Ashwell and Hardman, 2012 ).…”

Quantitative Analysis of the Timing of Development of the Cerebellum and Precerebellar Nuclei in Monotremes, Metatherians, Rodents, and Humans

“…The 33 monotreme embryos, hatchlings, and juveniles (22 platypuses, Ornithorhynchus anatinus ; 11 short‐beaked echidnas, Tachyglossus aculeatus ) are held at the MfN or the AMNH and have been used in previous studies of the development of the monotreme nervous system and brainstem by our group (Ashwell, ; Ashwell et al, ; Ashwell and Hardman, ). The AMNH specimens had been kindly made available by Professor U. Zeller (previously of MfN).…”

The evolution of cortical development: the synapsid-diapsid divergence

“…Most marsupials, such as the opossum or koala, have a smooth cortex, but in the kangaroo, it is folded, although not extensively. Even in monotremes, platypus is lissencephalic, whereas echidnas have a highly gyrated cortex (Ashwell and Hardman, 2012). A correlation exists between folding and body size in a given mammalian phylum but not across phyla.…”