Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species

The classical view of mammalian cortical development suggests that pyramidal neurons are generated in a temporal sequence, with all radial glial cells (RGCs) contributing to both lower and upper neocortical layers. A recent opposing proposal suggests there is a subgroup of fate-restricted RGCs in the early neocortex, which generates only upper-layer neurons. Little is known about the existence of fate restriction of homologous progenitors in other vertebrate species. We investigated the lineage of selected Emx2 + [vertebrate homeobox gene related to Drosophila empty spiracles (ems)] RGCs in mouse neocortex and chick forebrain and found evidence for both sequential and fate-restricted programs only in mouse, indicating that these complementary populations coexist in the developing mammalian but not avian brain. Among a large population of sequentially programmed RGCs in the mouse brain, a subset of self-renewing progenitors lack neurogenic potential during the earliest phase of corticogenesis. After a considerable delay, these progenitors generate callosal upper-layer neurons and glia. On the other hand, we found no homologous delayed population in any sectors of the chick forebrain. This finding suggests that neurogenic delay of selected RGCs may be unique to mammals and possibly associated with the evolution of the corpus callosum.S everal neural progenitor subtypes have been identified in the developing mammalian neocortex (1-4). At the onset of neurogenesis, multipotent proliferative radial glial cells (RGCs) reside at the ventricular surface. RGC divisions can be "self-renewing," a symmetrical division in which two identical RGCs are generated; "direct neurogenic," generating a neuroblast and a multipotent progenitor; or "indirect neurogenic," which gives rise to an intermediate progenitor that migrates to divide in the subventricular zone. The timing of these events is crucial for cell number and fate determination (5-7) and vary among different mammalian species. Importantly, very little is known about the homologous populations of RGCs in other vertebrate species and about their role in cortical evolution.Observations made from Golgi-stained material (4, 8), birthdating (5, 9), and lineage-tracing analysis (10-14) contributed to the formation of the "sequential" hypothesis. Accordingly, each RGC in the early brain generates most cortical cell types by sequential mitoses (15). Long-range subcortical projection neurons of the deep layers are generated first, followed by the callosal projection neurons of the upper layers, and finally the glial cells (16).However, recent genetic fate mapping of selected lineages has revealed a subpopulation of early RGCs expressing Cux2, which only gives rise to Satb2-positive upper-layer cortical neurons (17). This finding suggests that the early neurogenic brain may contain several types of cortical progenitors, each of which constrained to generating certain subpopulations of neurons, known as the "restricted progenitor hypothesis" (18). The existence of these restricted ...

Section: Emx2 Progenitors Support Both the Restricted And The Sequentialmentioning

confidence: 84%

Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain

García‐Moreno

Molnár

2015

“…The ontogenetic and phylogenetic increases in cortical volume would naturally allow for greater functional capacity without requiring a fundamental and sophisticated reorganization of the system (31). Importantly, the superficial layers of cortex, where this dynamics has been identified in vitro and in the anesthetized rat in vivo (15)(16)(17), expand most dramatically during both individual development and during the evolution of the cerebral cortex in advanced mammals (32).…”

Section: Scale Invariance In Time Nlfp Amplitude and Finite-size Scmentioning

confidence: 98%

Spontaneous cortical activity in awake monkeys composed of neuronal avalanches

Petermann

Thiagarajan

Lebedev

et al. 2009

534

541

Spontaneous neuronal activity is an important property of the cerebral cortex but its spatiotemporal organization and dynamical framework remain poorly understood. Studies in reduced systems-tissue cultures, acute slices, and anesthetized ratsshow that spontaneous activity forms characteristic clusters in space and time, called neuronal avalanches. Modeling studies suggest that networks with this property are poised at a critical state that optimizes input processing, information storage, and transfer, but the relevance of avalanches for fully functional cerebral systems has been controversial. Here we show that ongoing cortical synchronization in awake rhesus monkeys carries the signature of neuronal avalanches. Negative LFP deflections (nLFPs) correlate with neuronal spiking and increase in amplitude with increases in local population spike rate and synchrony. These nLFPs form neuronal avalanches that are scale-invariant in space and time and with respect to the threshold of nLFP detection. This dimension, threshold invariance, describes a fractal organization: smaller nLFPs are embedded in clusters of larger ones without destroying the spatial and temporal scale-invariance of the dynamics. These findings suggest an organization of ongoing cortical synchronization that is scale-invariant in its three fundamental dimensions-time, space, and local neuronal group size. Such scale-invariance has ontogenetic and phylogenetic implications because it allows large increases in network capacity without a fundamental reorganization of the system. neuronal synchronization ͉ resting state ͉ rhesus monkey ͉ spontaneous activity ͉ ongoing activity T he cerebral cortex displays spontaneous activity, also known as 'ongoing' or 'resting state' activity, which persists in the absence of sensory stimuli or motor outputs. The ongoing activity is a robust feature of cortical dynamics as it is only modulated to a small extent by stimulus presentation (1), but contributes significantly to the large variability observed in stimulus responses (2-5). In fact, ongoing activity has been found to reflect multiple aspects of neuronal processing. The activity is similar to that observed during stimulus presentation (1, 6-8), incorporates previously acquired information (9), and carries information about the underlying neuronal network [for review see (10)]. Indeed, correlations during resting state activity are altered in disease states such as schizophrenia or chronic pain (11, 12), which raises the question whether there is a general framework that describes the statistics in the spatiotemporal organization of this dynamics.Recently, we found that spontaneous cortical activity in slice cultures, acute slices, and in the anesthetized rat in vivo has a scale-invariant dynamics called neuronal avalanches (13)(14)(15). These spontaneous bursts of synchronized activity occur in clusters of sizes s (where s is the number of active sites in an electrode array) that distribute according to a power law with exponent ␣:where ␣ usually lies between ...

“…Several observations indicate that upper layers have undergone expansion and remodeling in primates relative to rodents. Layers II and III are relatively thicker in primates (19,20), and layer III neurons in primates, particularly in higher-order association cortices, have protracted spinogenesis (21)(22)(23). The relationship between these supragranular molecular innovations and corticocortical connectivity is still unclear.…”

Section: Significancementioning

confidence: 99%

Transcriptional profiles of supragranular-enriched genes associate with corticocortical network architecture in the human brain

Krienen

Yeo

et al. 2016

214

203

The human brain is patterned with disproportionately large, distributed cerebral networks that connect multiple association zones in the frontal, temporal, and parietal lobes. The expansion of the cortical surface, along with the emergence of long-range connectivity networks, may be reflected in changes to the underlying molecular architecture. Using the Allen Institute's human brain transcriptional atlas, we demonstrate that genes particularly enriched in supragranular layers of the human cerebral cortex relative to mouse distinguish major cortical classes. The topography of transcriptional expression reflects large-scale brain network organization consistent with estimates from functional connectivity MRI and anatomical tracing in nonhuman primates. Microarray expression data for genes preferentially expressed in human upper layers (II/III), but enriched only in lower layers (V/VI) of mouse, were cross-correlated to identify molecular profiles across the cerebral cortex of postmortem human brains (n = 6). Unimodal sensory and motor zones have similar molecular profiles, despite being distributed across the cortical mantle. Sensory/motor profiles were anticorrelated with paralimbic and certain distributed association network profiles. Tests of alternative gene sets did not consistently distinguish sensory and motor regions from paralimbic and association regions: (i) genes enriched in supragranular layers in both humans and mice, (ii) genes cortically enriched in humans relative to nonhuman primates, (iii) genes related to connectivity in rodents, (iv) genes associated with human and mouse connectivity, and (v) 1,454 gene sets curated from known gene ontologies. Molecular innovations of upper cortical layers may be an important component in the evolution of long-range corticocortical projections.corticocortical connectivity | human transcriptome | association cortex | supragranular | brain evolution P atterns of gene expression in the cerebral cortex are generally conserved across species, reflecting strong constraints in the development and evolution of cortical architecture (1-6). Previous work examining transcriptional variation in nonhuman primates and rodents indicate that molecular similarities between cortical regions in the adult brain are best explained by spatial proximity (7, 8). Molecular variation often takes the form of graded expression along a principal axis, in many cases appearing as rostrocaudal gradients across the cortex (8). The strong tendency for transcriptional variation to follow spatial proximity in the adult cortex likely reflects both functional gradients, as well as their developmental origins in terms of physical and temporal adjacency during neurogenesis of cells destined for neighboring locations in the cortex (at least for cells derived from the ventricular proliferative pool) (7).Spatial proximity likely captures the major features governing how molecular profiles vary across the cortex in all species, including humans. However, the expansion of the cerebral cortex in primates...