Analysis of regional corpus callosum fiber composition reveals that callosal regions connecting primary and secondary sensory areas tend to have higher proportions of coarse-diameter, highly myelinated fibers than callosal regions connecting so-called higher-order areas. This suggests that in primary/secondary sensory areas there are strong timing constraints for interhemispheric communication, which may be related to the process of midline fusion of the two sensory hemifields across the hemispheres. We postulate that the evolutionary origin of the corpus callosum in placental mammals is related to the mechanism of midline fusion in the sensory cortices, which only in mammals receive a topographically organized representation of the sensory surfaces. The early corpus callosum may have also served as a substrate for growth of fibers connecting higher-order areas, which possibly participated in the propagation of neuronal ensembles of synchronized activity between the hemispheres. However, as brains became much larger, the increasingly longer interhemispheric distance may have worked as a constraint for efficient callosal transmission. Callosal fiber composition tends to be quite uniform across species with different brain sizes, suggesting that the delay in callosal transmission is longer in bigger brains. There is only a small subset of large-diameter callosal fibers whose size increases with increasing interhemispheric distance. These limitations in interhemispheric connectivity may have favored the development of brain lateralization in some species like humans.

Many intergenic long noncoding RNA (lncRNA) loci regulate the expression of adjacent protein coding genes. Less clear is whether intergenic lncRNAs commonly regulate transcription by modulating chromatin at genomically distant loci. Here, we report both genomically local and distal RNA-dependent roles of Dali, a conserved central nervous system expressed intergenic lncRNA. Dali is transcribed downstream of the Pou3f3 transcription factor gene and its depletion disrupts the differentiation of neuroblastoma cells. Locally, Dali transcript regulates transcription of the Pou3f3 locus. Distally, it preferentially targets active promoters and regulates expression of neural differentiation genes, in part through physical association with the POU3F3 protein. Dali interacts with the DNMT1 DNA methyltransferase in mouse and human and regulates DNA methylation status of CpG island-associated promoters in trans. These results demonstrate, for the first time, that a single intergenic lncRNA controls the activity and methylation of genomically distal regulatory elements to modulate large-scale transcriptional programmes.DOI: http://dx.doi.org/10.7554/eLife.04530.001

A cross-species ultrastructural study of the corpus callosum was performed in six domestic species: the rat, the rabbit, the cat, the dog, the horse and the cow. The results indicate cross-species conservatism in callosal fiber composition with a good interspecies relation between fiber number and brain size. Across species, increases in both brain size and callosal area indicate more callosal fibers, although less than expected from the estimated increase in cortical cell number. Within each species, the correlation between fiber number and brain weight tends to disappear, although in most cases a larger callosum implies a larger number of callosal fibers. The median fiber diameter was conservative across species (0.11–0.2 µm), indicating the maintenance of conduction velocity of most callosal fibers regardless of interhemispheric distance. Nevertheless, the maximal fiber diameters tended to be higher in species with larger brains. Therefore, there is a population of coarse-diameter fibers that tend to increase their diameter and conduction velocity with increasing brain size. However, allometric calculations suggest that the associated increase in velocity in these large fibers may not be sufficient to maintain a constant interhemispheric transmission time in different species.

There is currently a debate about the evolutionary origin of the earliest generated cortical preplate neurons and their derivatives (subplate and marginal zone). We examined the subplate with murine markers including nuclear receptor related 1 (Nurr1), monooxygenase Dbh-like 1 (Moxd1), transmembrane protein 163 (Tmem163), and connective tissue growth factor (Ctgf) in developing and adult turtle, chick, opossum, mouse, and rat. Whereas some of these are expressed in dorsal pallium in all species studied (Nurr1, Ctgf, and Tmem163), we observed that the closely related mouse and rat differed in the expression patterns of several others (Dopa decarboxylase, Moxd1, and thyrotropin-releasing hormone). The expression of Ctgf, Moxd1, and Nurr1 in the oppossum suggests a more dispersed subplate population in this marsupial compared with mice and rats. In embryonic and adult chick brains, our selected subplate markers are primarily expressed in the hyperpallium and in the turtle in the main cell dense layer of the dorsal cortex. These observations suggest that some neurons that express these selected markers were present in the common ancestor of sauropsids and mammals.

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The isocortex is a distinctive feature of mammalian brains, which has no clear counterpart in the cerebral hemispheres of other amniotes. This paper speculates on the evolutionary processes giving rise to the isocortex. As a first step, we intend to identify what structure may be ancestral to the isocortex in the reptilian brain. Then, it is necessary to account for the transformations (developmental, connectional, and functional) of this ancestral structure, which resulted in the origin of the isocortex. One long-held perspective argues that part of the isocortex derives from the ventral pallium of reptiles, whereas another view proposes that the isocortex originated mostly from the dorsal pallium. We consider that, at this point, evidence tends to favor correspondence of the isocortex with the dorsal cortex of reptiles. In any case, the isocortex may have originated partly as a consequence of an overall “dorsalizing” effect (that is, an expansion of the territories expressing dorsal-specific genes) during pallial development. Furthermore, expansion of the dorsal pallium may have been driven by selective pressures favoring the development of associative networks between the dorsal cortex, the olfactory cortex, and the hippocampus, which participated in spatial or episodic memory in the early mammals. In this context, sensory projections that in reptiles end in the ventral pallium, are observed to terminate in the isocortex (dorsal pallium) of mammals, perhaps owing to their participation in these associative networks.

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The thorniest problem in comparative neurobiology is the identification of the particular brain region of birds and reptiles that corresponds to the mammalian neocortex [Butler AB, Reiner A, Karten HJ (2011) Ann N Y Acad Sci 1225:14-27; Wang Y, BrzozowskaPrechtl A, Karten HJ (2010) Proc Natl Acad Sci USA 107(28):12676-12681]. We explored which genes are actively transcribed in the regions of controversial ancestry in a representative bird (chicken) and mammal (mouse) at adult stages. We conducted four analyses comparing the expression patterns of their 5,130 most highly expressed one-to-one orthologous genes that considered global patterns of expression specificity, strong gene markers, and coexpression networks. Our study demonstrates transcriptomic divergence, plausible convergence, and, in two exceptional cases, conservation between specialized avian and mammalian telencephalic regions. This large-scale study potentially resolves the complex relationship between developmental homology and functional characteristics on the molecular level and settles long-standing evolutionary debates.cerebral cortex | Wulst | equivalent circuit hypothesis | brain evolution | dorsal ventricular ridge D espite recent advances in our knowledge of comparative aspects of cortical neurogenesis, migration, clonal relationships, and gene expression patterns, there is no consensus on how these processes evolved together to determine the adult brain structures across diverse amniotes (1-5). Anatomical, hodological, embryological, and gene expression data (based on few select genes) provide conflicting answers on brain homology across vertebrates. Studies of embryonic neurogenesis and cell migration have informed homology of developmental territories (6-8), but the striking similarities in lamination, connectivity, and physiological properties observed between adult forms derived from noncorresponding pallial regions remain unexplained (3-5, 9). Comparative transcriptomics is a powerful approach to interrogating regional correspondence without resorting to limited lists of selected genetic markers. Recent methodological advances in profiling mammalian cerebral cortical layer transcriptomes (10-12) could objectively test the validity of proposed, yet controversial, relationships between regions of adult mammalian and avian brains. These comparisons are motivated by our understanding of the evolution of mammals from a reptilian subclass, represented by the synapsid condition (with a cranial opening in the cheek region of the skull), and of birds from another reptilian subclass, represented by the diapsid condition (two postorbital skull openings). ResultsWe extended our previous transcriptomic analysis of cortical layers in the adult mouse (13) to additional structures, 16 in total, and compared these with seven regions of the adult chicken brain (Fig. 1A and SI Appendix, Figs. S1 and S2). All dissected regions in both species (except the striatum, which is subpallial) develop primarily from one of four morphogenetically delineated sector...