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A hypothesis for the evolution of the upper layers of the neocortex through co-option of the olfactory cortex developmental program.

ABSTRACT: The neocortex is unique to mammals and its evolutionary origin is still highly debated. The neocortex is generated by the dorsal pallium ventricular zone, a germinative domain that in reptiles give rise to the dorsal cortex. Whether this latter allocortical structure contains homologs of all neocortical cell types it is unclear. Recently we described a population of DCX+/Tbr1+ cells that is specifically associated with the layer II of higher order areas of both the neocortex and of the more evolutionary conserved piriform cortex. In a reptile similar cells are present in the layer II of the olfactory cortex and the DVR but not in the dorsal cortex. These data are consistent with the proposal that the reptilian dorsal cortex is homologous only to the deep layers of the neocortex while the upper layers are a mammalian innovation. Based on our observations we extended these ideas by hypothesizing that this innovation was obtained by co-opting a lateral and/or ventral pallium developmental program. Interestingly, an analysis in the Allen brain atlas revealed a striking similarity in gene expression between neocortical layers II/III and piriform cortex. We thus propose a model in which the early neocortical column originated by the superposition of the lateral olfactory and dorsal cortex. This model is consistent with the fossil record and may account not only for the topological position of the neocortex, but also for its basic cytoarchitectural and hodological features. This idea is also consistent with previous hypotheses that the peri-allocortex represents the more ancient neocortical part. The great advances in deciphering the molecular logic of the amniote pallium developmental programs will hopefully enable to directly test our hypotheses in the next future.

SUBMITTER: Luzzati F

PROVIDER: S-EPMC4429232 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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A hypothesis for the evolution of the upper layers of the neocortex through co-option of the olfactory cortex developmental program.

Luzzati Federico F

Frontiers in neuroscience 20150512

The neocortex is unique to mammals and its evolutionary origin is still highly debated. The neocortex is generated by the dorsal pallium ventricular zone, a germinative domain that in reptiles give rise to the dorsal cortex. Whether this latter allocortical structure contains homologs of all neocortical cell types it is unclear. Recently we described a population of DCX+/Tbr1+ cells that is specifically associated with the layer II of higher order areas of both the neocortex and of the more evol ...[more]

PMID: 26029038

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Project description:Neurons in the cerebral cortex stratify on the basis of their time of origin, axonal terminations and the molecular identities assigned during early development. Olfactory cortices share many feature with the neocortex, including clear lamination and similar cell types. The present study demonstrates that the markers differentially expressed in the projection neurons of the cerebral cortex are also found in olfactory areas. Three of the four regions examined (pars principalis of the anterior olfactory nucleus: AONpP, anterior and posterior piriform cortices: APC, PPC, and the olfactory tubercle) expressed transcription factors found in deep or superficial neurons in the developing neocortex, though large differences were found between areas. For example, while the AONpP, APC and PPC all broadly expressed the deep cortical marker CTIP2, NOR1 (NR4a3) levels were higher in AONpP and DAARP-32 was more prevalent in the APC and PPC. Similar findings were encountered for superficial cortical markers: all three regions broadly expressed CUX1, but CART was only observed in the APC and PPC. Furthermore, regional variations were observed even within single structures (e.g., NOR1 was found primarily in in the dorsal region of AONpP and CART expression was observed in a discrete band in the middle of layer 2 of both the APC and PPC). Experiments using the mitotic marker EDU verified that the olfactory cortices and neocortex share similar patterns of neuronal production: olfactory cells that express markers found in the deep neocortex are produced earlier than those that express superficial makers. Projection neurons were filled by retrograde tracers injected into the olfactory bulb to see if olfactory neurons with deep and superficial markers had different axonal targets. Unlike the cerebral cortex, no specificity was observed: neurons with each of the transcription factors examined were found to be labelled. Together the results indicate that olfactory cortices are complex: they differ from each other and each is formed from a variable mosaic of neurons. The results suggest that the olfactory cortices are not merely a remnant architype of the primordial forebrain but varied and independent regions.

Project description:Specific vulnerability of neurons in the human entorhinal cortex has been associated with the onset of disease. Gene expression is analyzed to define the molecular characteristic of those neurons. Experiment Overall Design: Human tissue collection and dissection. Brain samples were collected from four individuals with no clinical evidence of neurological disease and no neuropathological evidence of neurodegeneration. Tissue samples were obtained from the neurological tissue bank (UIPA) and from the Neurological Research Tissue Bank (BTIN, Madrid). The mean postmortem interval (PMI) of the tissue was 6 h and each subject died in hospital due to either cardiac or infectious diseases. The tissue was obtained according to local ethical and legal regulations concerning the use of human post-mortem tissue for biomedical research. Frozen tissue samples were collected from the entorhinal cortex [EC; Brodmann area (BA) 28], at coronal level 27 of the Atlas of Paxinos. Tissue samples corresponded to either upper (CES), lower (CEI) or the entire EC (CET). Two adjacent vertical columns comprising the full thickness of the EC were dissected under magnification with a Leica M50 stereomicroscope. One of them was then divided into two blocks, corresponding to CES and CEI, while the remaining column was processed as CET. RNA sample preparation. Cerebral tissue was homogenised in liquid nitrogen with a pestle and mortar, and the total RNA was isolated using the RNeasy Mini Kit and QIAshredder (Qiagen). The total RNA concentration and purity were determined using an Agilent2100 Bioanalyzer (Agilent Biotechnologies, Palo, Alto, CA) and by agarose gel electrophoresis. Subsequently, cDNA was synthesized using the One-Cycle cDNA Synthesis kit (Affymetrix), according to the protocol described in the Expression Analysis Technical Manual. Biotinylated cRNA probes were generated from each cDNA sample following the IVT Labeling kit instructions (Affymetrix), and the cRNA synthesized was purified with the GeneChip Sample Cleanup Module (Affymetrix). The concentration and purity of the biotinylated cRNA was determined using an Agilent2100 Bioanalyzer (Agilent Biotechnologies, Palo, Alto, CA) and by agarose gel electrophoresis.

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A hypothesis for the evolution of the upper layers of the neocortex through co-option of the olfactory cortex developmental program.

Publications

A hypothesis for the evolution of the upper layers of the neocortex through co-option of the olfactory cortex developmental program.

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