An Adaptive Threshold in Mammalian Neocortical Evolution

Lewitus, Éric; Kelava, Iva; Kalinka, Alex T.; Tomančák, Pavel; Huttner, Wieland B.

doi:10.1371/journal.pbio.1002000

Cited by 148 publications

(167 citation statements)

References 89 publications

(120 reference statements)

Supporting

Mentioning

156

Contrasting

Order By: Relevance

“…Conversely, the proportion of PAX6+TBR2+ NSPCs, located in the basal VZ and SVZ and constituting BPs with neurogenic potential, showed a greater increase in chimpanzee than human cerebral organoids. In sum, two independent lines of evidence, the detailed analysis of AP mitosis phase lengths and the determination of the proportions of the various NSPC types, support the concept that a longer neurogenic period (Lewitus et al, 2014), which in turn implies a longer phase of NSPC proliferation (Otani et al, 2016), contributes to the greater expansion of the neocortex in humans than the great apes.…”

Section: Discussionmentioning

confidence: 84%

Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development

Mora-Bermúdez

Badsha

Kanton

et al. 2016

eLife

222

223

View full text Add to dashboard Cite

Human neocortex expansion likely contributed to the remarkable cognitive abilities of humans. This expansion is thought to primarily reflect differences in proliferation versus differentiation of neural progenitors during cortical development. Here, we have searched for such differences by analysing cerebral organoids from human and chimpanzees using immunohistofluorescence, live imaging, and single-cell transcriptomics. We find that the cytoarchitecture, cell type composition, and neurogenic gene expression programs of humans and chimpanzees are remarkably similar. Notably, however, live imaging of apical progenitor mitosis uncovered a lengthening of prometaphase-metaphase in humans compared to chimpanzees that is specific to proliferating progenitors and not observed in non-neural cells. Consistent with this, the small set of genes more highly expressed in human apical progenitors points to increased proliferative capacity, and the proportion of neurogenic basal progenitors is lower in humans. These subtle differences in cortical progenitors between humans and chimpanzees may have consequences for human neocortex evolution.DOI: http://dx.doi.org/10.7554/eLife.18683.001

show abstract

Section: Discussionmentioning

confidence: 84%

Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development

Mora-Bermúdez

Badsha

Kanton

et al. 2016

eLife

222

223

View full text Add to dashboard Cite

show abstract

“…One possibility is that stem mammals actually had a gyrified neocortex (Lewitus et al, 2014), as also proposed for the hypothetical placental ancestor (O’Leary et al, 2013). However, since lissencephaly is also common in extant mammals, another possibility might be that the key developmental mechanism(s) for gyrogenesis arose in stem mammals, which nevertheless remained lissencephalic, with actual gyrification evolving independently in diverse branches of mammals.…”

Section: Convolution Of the Dgmentioning

confidence: 90%

“…Based on such findings, recent hypotheses have proposed that neocortical gyri develop by enhanced local proliferation and basal migration of NSPCs (Kriegstein et al, 2006; Martínez-Cerdeño et al, 2006; Lui et al, 2011; Borrell and Götz, 2014; Lewitus et al, 2014). Migrating NSPCs in neocortex do not form histological streams like the DMS, but are rather more dispersed in the outer SVZ.…”

Section: Is Dg Convolution Relevant To Neocortical Gyrification?mentioning

confidence: 99%

Evolution of the mammalian dentate gyrus

Hevner

2015

J of Comparative Neurology

View full text Add to dashboard Cite

The dentate gyrus (DG), a part of the hippocampal formation, has important functions in learning, memory, and adult neurogenesis. Compared to homologous areas in sauropsids (birds and reptiles), the mammalian DG is larger and exhibits qualitatively different phenotypes: (1) folded (C- or V-shaped) granule neuron layer, concave towards the hilus, delimited by a hippocampal fissure; (2) non-periventricular adult neurogenesis; and (3) prolonged ontogeny involving extensive abventricular (basal) migration and proliferation of neural stem and progenitor cells (NSPCs). Although gaps remain, available data indicate that these DG traits are present in all orders of mammals, including monotremes and marsupials. The exception is Cetacea (whales, dolphins, and porpoises), in which DG size, convolution, and adult neurogenesis have undergone evolutionary regression. Parsimony suggests that increased growth and convolution of the DG arose in stem mammals, concurrently with non-periventricular adult hippocampal neurogenesis, and basal migration of NSPCs during development. These traits could all result from an evolutionary change that enhanced radial migration of NSPCs out of the periventricular zones, possibly by epithelial-mesenchymal transition, to colonize and maintain non-periventricular proliferative niches. In turn, increased NSPC migration and clonal expansion might be a consequence of growth in the cortical hem (medial patterning center), which produces morphogens such as Wnt3a, generates Cajal-Retzius neurons, and is regulated by Lhx2. Finally, correlations between DG convolution and neocortical gyrification (or capacity for gyrification) suggest that enhanced abventricular migration and proliferation of NSPCs played a transformative role in growth and folding of neocortex, as well as archicortex.

show abstract

“…1D), in line with the different, clade-specific relationships between A T and T, as shown in our original figure 3B (although we don't call these "clusters"). The two candidate groups to form different "clusters of gyrencephaly," primates and artiodactyls, are however not the "two mammalian groups" to which Lewitus et al refer in (5). Figure 1D shows that, for similar numbers of cortical neurons, artiodactyls have much larger folding indices than primates.…”

mentioning

confidence: 95%

“…Actually, it is worse; given that folding indices are by definition never smaller than 1.0, their mathematical analysis could never obtain an average folding index of 1.0 for any clade, given that all of them contain gyrencephalic species. O'Leary et al (13), cited by Lewitus et al (5), used a similarly flawed inference to conclude that the ancestral placental mammal was gyrencephalic.…”

mentioning

confidence: 99%

Response to Comments on “Cortical folding scales universally with surface area and thickness, not number of neurons”

Mota

Herculano‐Houzel

2016

Science

View full text Add to dashboard Cite

De Lussanet claims that our model that accounts for the degree of folding of the cerebral cortex based on the product of cortical surface area and the square root of cortical thickness is better reduced to the product of gray-matter proportion and folding index. Lewitus et al., in turn, claim that the assumptions of our model are in conflict with experimental data; that the model does not accurately fit the data; and that the ancestral mammalian brain was gyrencephalic. Here, we show that both claims are inappropriate. In our original Report (1), we showed for the first time that the relationship between total surface area (A T ) and exposed surface area (A E ) of the mammalian cerebral cortex can be universally described, across lissencephalic and gyrencephalic species alike, by the power, where T is the average thickness of the cortical gray matter (Fig. 1A). Our model predicts the degree of folding of the mammalian cerebral cortex (that is, the relationship between A T and A E ) with an r 2 of 0.998; that is, 99.8% of the variance in A T T 1/2 across species is explained by the variation in kA E 1.305 . The empirical function is very close to our theoretical function A T T 1/2 = kA E 1.25 that expresses the relationship between A T and A E , given T, that minimizes the effective free energy of a growing cortical volume-that is, the function that describes the most stable conformation of a growing, elastic, deformable cerebral cortex given its surface area and thickness. We thus propose that folding occurs as the expanding cortex, during development, settles at each moment in time into the most energetically favorable conformation, one that depends simply on its current combination of A T and T, not number of neurons.Based on the calculation from our data of values of k for the theoretical exponent of 1.25, de Lussanet notes that the residuals of the function, that is, k, vary systematically with increasing A E across species (2). This indicates a (presumably hidden) significant discrepancy between the exponent for A E predicted by our effective free energy-minimization theory and the empirical exponent 1.305 (excluding cetaceans) that is found in the data. Our original Report makes it clear that, with a value of 1.305 ± 0.010, the exponent for A E that best fits the data is close to, but statistically distinguishable (given the standard error) from, the theoretical exponent of 1.250, which is not surprising for a mean-field model based on a number of simplifying assumptions.The origin of the discrepancy of 0.055 in the scaling exponent is an important question. In purely theoretical terms, the use of A E as an order parameter was a necessary simplification, based on the expected relationship V T~AE 3/2 [made explicitly in the supplementary information in (1), and a good empirical approximation, given that we obtain V T~AE 1.52 ]. Whether modifications to correct for Gaussian curvature of the surface and the presence of deep nuclei would suffice to close the gap of 0.055 between theoretical and empirical e...

show abstract

An Adaptive Threshold in Mammalian Neocortical Evolution

Cited by 148 publications

References 89 publications

Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development

Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development

Evolution of the mammalian dentate gyrus

Response to Comments on “Cortical folding scales universally with surface area and thickness, not number of neurons”

Contact Info

Product

Resources

About