Coleoid cephalopods (octopus, squid, and cuttlefish) are active, resourceful predators with a rich behavioral repertoire1. They have the largest nervous systems among the invertebrates2 and present other striking morphological innovations including camera-like eyes, prehensile arms, a highly derived early embryogenesis, and the most sophisticated adaptive coloration system among all animals1,3. To investigate the molecular bases of cephalopod brain and body innovations we sequenced the genome and multiple transcriptomes of the California two-spot octopus, Octopus bimaculoides. We found no evidence for hypothesized whole genome duplications in the octopus lineage4–6. The core developmental and neuronal gene repertoire of the octopus is broadly similar to that found across invertebrate bilaterians, except for massive expansions in two gene families formerly thought to be uniquely enlarged in vertebrates: the protocadherins, which regulate neuronal development, and the C2H2 superfamily of zinc finger transcription factors. Extensive mRNA editing generates transcript and protein diversity in genes involved in neural excitability, as previously described7, as well as in genes participating in a broad range of other cellular functions. We identified hundreds of cephalopod-specific genes, many of which showed elevated expression levels in such specialized structures as the skin, the suckers, and the nervous system. Finally, we found evidence for large-scale genomic rearrangements that are closely associated with transposable element expansions. Our analysis suggests that substantial expansion of a handful of gene families, along with extensive remodeling of genome linkage and repetitive content, played a critical role in the evolution of cephalopod morphological innovations, including their large and complex nervous systems.
We here report observations on the distribution of acetylcholinesterase (acetylcholine hydrolase, EC 3.1.1.7) in the striatum of the adult human, the rhesus monkey, and the cat. By the histochemical staining methods of Geneser-Jensen and Blackstad and of Karnovsky and Roots, compartments of low cholinesterase activity were identified in parts of the striatum in all three species. In frontal sections, these enzyme-poor zones appeared as a variable number of weakly stained t0.5-mm-wide zones embedded in a darkly stained background. The zones varied in cross-sectional shape from round to elongated and were sometimes branched. They were most prominent in the head of the caudate nucleus. Three-dimensional reconstructions of serial sections through the caudate nucleus in the human and cat suggest that over distances of at least several millimeters, the zones of low enzyme activity form nearly continuous labyrinths.The mammalian striatum is characterized by one of the highest concentrations of acetylcholinesterase (acetylcholine hydrolase, EC 3.1.1.7) in the brain. The presence of this enzyme is not in itself sufficient to establish the existence of cholinergic transmission in the striatum, but the caudoputamen has also been shown to contain cholinergic receptors (1) and the synthetic enzyme of the cholinergic mechanism, choline acetyltransferase (2). The histochemical demonstration of acetylcholinesterase has therefore come to be regarded as a useful indirect indicator of cholinergic activity in the striatum and has further attracted interest because of the remarkable similarity in distribution of dopamine histofluorescence and acetylcholinesterase activity in the caudoputamen and nucleus accumbens. We report here observations on the distribution of striatal acetylcholinesterase in the human, together with parallel observations in cat and monkey. The main finding of this study is that the cholinesterase of the adult striatum in all three species is characterized by a complex intrinsic architecture that can be visualized by the histochemical methods of Karnovsky and Roots (3) and Geneser-Jensen and Blackstad (4). These findings strongly suggest that in the human, as in the cat and monkey, the contrast between an architecturally highly differentiated cerebral cortex on the one hand and a structurally homogeneous striatum on the other' has been overdrawn. When considered in the context of other recent experimental studies of the mature and developing striatum (5-13), the present findings support the concept of a fundamental subdivision of the striatum into a mosaic of at least partially segregated, histochemically distinct units. Figs. 1-4 illustrate this pattern of staining in frontal sections passing through the caudate nucleus of the cat (Fig. 1), monkey (Fig. 2), and human (Figs. 3 and 4). Typically, 6 to 12 distinct regions of low enzyme activity appeared in the caudate nucleus in single sections near the levels illustrated. The average transverse diameter of the zones was 0.3-0.5 mm in the cat and 5723 ...
The six-layered neocortex is a uniquely mammalian structure with evolutionary origins that remain in dispute. One long-standing hypothesis, based on similarities in neuronal connectivity, proposes that homologs of the layer 4 input and layer 5 output neurons of neocortex are present in the avian forebrain, where they contribute to specific nuclei rather than to layers. We devised a molecular test of this hypothesis based on layer-specific gene expression that is shared across rodent and carnivore neocortex. Our findings establish that the layer 4 input and the layer 5 output cell types are conserved across the amniotes, but are organized into very different architectures, forming nuclei in birds, cortical areas in reptiles, and cortical layers in mammals.T he evolutionary origins of the mammalian neocortex have been the subject of debate for over a century (1-3). Although the six-layered neocortex is remarkably well conserved in all extant mammals, it is not present in our closest living relatives, the reptiles and birds. Birds in particular are an extremely successful radiation with large brains, but the bird dorsal telencephalon does not include a morphologically identifiable cortex; it is, instead, a collection of nuclei (4).Studies of the neurochemistry, anatomy, and physiology of the central region of the bird telencephalon, which is called the dorsal ventricular ridge (DVR), have shown conclusively that the DVR is a pallial structure (2). In mammals the pallium (dorsal telencephalon) includes the neocortex and the nuclei of the piriform lobe, specifically the claustrum and parts of the amygdala. A classical hypothesis that has attracted renewed interest from modern neuroembryologists and neuromorphologists proposes a field homology between the nuclei of the bird DVR and the mammalian piriform lobe nuclei, including the amygdala (5, 6). A second, more controversial hypothesis proposes that, despite the gross differences in morphology between bird DVR and mammalian neocortex, these structures share a homology (7-9).The best evidence for neocortex-DVR homology lies in their circuitries. Both the mammalian neocortex and avian DVR receive ascending sensory input from the thalamus, and both send outputs to brainstem premotor areas. These input and output territories form specific, well-defined populations of neurons in both mammals and birds. In mammals, layer 4 neocortical neurons receive thalamic input, and layer 5 neocortical neurons project to the brainstem. In birds there are separate DVR nuclei that receive projections from the thalamus or send axons to the brainstem. The most developed version of the neocortex-DVR hypothesis proposes homology between these input and output neurons at the cell-type level (7); specifically, that the layer 4 input (L4/I) and layer 5 output (L5/O) neurons of the neocortex share a common ancestry with neurons that populate the input and output nuclei of the DVR.These two prevailing hypotheses about DVR homology are in direct conflict; one is a field homology argument comparing...
Little is known about how patterns of cell types are organized to form brain structures of appropriate size and shape. To study this process, we employed in vivo electroporation during midbrain development to create ectopic sources of Sonic Hedgehog, a signaling molecule previously shown to specify different neuronal cell types in a concentration-dependent manner in vitro. We provide direct evidence that a Sonic Hedgehog source can control pattern at a distance in brain development and demonstrate that the size, shape, and orientation of the cell populations produced depend on the geometry of the morphogen source. Thus, a single regulatory molecule can coordinate tissue size and shape with cell-type identity in brain development.
In an emerging model, area patterning of the mammalian cerebral cortex is regulated in part by embryonic signaling centers. Two have been identified: an anterior telencephalic source of fibroblast growth factors and the cortical hem, a medial structure expressing winglessint (WNT) and bone morphogenetic proteins. We describe a third signaling source, positioned as a mirror image of the cortical hem, along the lateral margin of the cortical primordium. The cortical antihem is identified by gene expression for three epidermal growth factor (EGF) family members, Tgf(alpha), Neuregulin 1, and Neuregulin 3, as well as two other signaling molecules, Fgf7 and the secreted WNT antagonist Sfrp2. We find that the antihem is lost in mice homozygous for the Small eye (Pax6) mutation and suggest the loss of EGF signaling at least partially explains defects in cortical patterning and cell migration in Small eye mice.
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