Area‐specific substratification of deep layer neurons in the rat cortex

Watakabe, Akiya; Hirokawa, Junya; Ichinohe, Noritaka; Ohsawa, Sonoko; Kaneko, Takeshi; Rockland, Kathleen S.; Yamamori, Tetsuo

doi:10.1002/cne.23160

Cited by 37 publications

(28 citation statements)

References 65 publications

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“…The present results also reveal differences in cellular density between the two layers, as well as the presence of geniculate terminations throughout 6A but not 6B. Prior reports of V1 lamination largely consider layer 6 as a single layer that blends into the ventral white matter (Lund, 1973; Lund et al, 1988; Casagrande and Kaas, 1994), but subtle differences between upper and lower tier cells in this layer have been considered (Levitt et al, 1996; Yamamori and Rockland, 2006; Watakabe et al, 2012, 2006). Our results, in combination with recent studies of layer- and cellular-specific gene expression, suggest that layer 6 is made up of two functional subdivisions; a superficial sublayer with sparse geniculate inputs as well as intrinsic and extrinsic visual projections, and a deep sublayer with separate inputs and functions.…”

Section: Discussionsupporting

confidence: 52%

Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity

Balaram

Kaas

2014

Front. Neuroanat.

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Primary visual cortex (V1) is clearly distinguishable from other cortical areas by its distinctive pattern of neocortical lamination across mammalian species. In some mammals, primates in particular, the layers of V1 are further divided into a number of sublayers based on their anatomical and functional characteristics. While these sublayers are easily recognizable across a range of primates, the exact number of divisions in each layer and their relative position within the depth of V1 has been inconsistently reported, largely due to conflicting schemes of nomenclature for the V1 layers. This conflict centers on the definition of layer 4 in primate V1, and the subdivisions of layer 4 that can be consistently identified across primate species. Brodmann’s (1909) laminar scheme for V1 delineates three subdivisions of layer 4 in primates, based on cellular morphology and geniculate inputs in anthropoid monkeys. In contrast, Hässler’s (1967) laminar scheme delineates a single layer 4 and multiple subdivisions of layer 3, based on comparisons of V1 lamination across the primate lineage. In order to clarify laminar divisions in primate visual cortex, we performed NeuN and VGLUT2 immunohistochemistry in V1 of chimpanzees, Old World macaque monkeys, New World squirrel, owl, and marmoset monkeys, prosimian galagos and mouse lemurs, and non-primate, but highly visual, tree shrews. By comparing the laminar divisions identified by each method across species, we find that Hässler’s (1967) laminar scheme for V1 provides a more consistent representation of neocortical layers across all primates, including humans, and facilitates comparisons of V1 lamination with non-primate species. These findings, along with many others, support the consistent use of Hässler’s laminar scheme in V1 research.

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Section: Discussionsupporting

confidence: 52%

Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity

Balaram

Kaas

2014

Front. Neuroanat.

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“…By double ISH, we found that the nurr1 + neurons in both mouse and macaque claustrum co-express VGluT1 mRNA (Figure 4 and data not shown). (2) In our previous study, moreover, we reported that excitatory neurons in layer 6 of rats can be classified as either pcp4 + or cck + cells, and that nurr1 + cells express cck mRNA (Watakabe et al, 2012). In both rodents and monkeys, cck mRNA was expressed in the claustrum but not in the striatum (data not shown).…”

Section: Discussionmentioning

confidence: 96%

“…The FastBlue injection and the subsequent ISH were performed as previously (Watakabe et al, 2007). The FluoroGold injection and the following ISH was performed as previously (Watakabe et al, 2012). …”

Section: Methodsmentioning

confidence: 99%

Characterization of claustral neurons by comparative gene expression profiling and dye-injection analyses

Watakabe

Ohsawa

Ichinohe

et al. 2014

Front. Syst. Neurosci.

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The identity of the claustrum as a part of cerebral cortex, and in particular of the adjacent insular cortex, has been investigated by connectivity features and patterns of gene expression. In the present paper, we mapped the cortical and claustral expression of several cortical genes in rodent and macaque monkey brains (nurr1, latexin, cux2, and netrinG2) to further assess shared features between cortex and claustrum. In mice, these genes were densely expressed in the claustrum, but very sparsely in the cortex and not present in the striatum. To test whether the cortical vs. claustral cell types can be distinguished by co-expression of these genes, we performed a panel of double ISH in mouse and macaque brain. NetrinG2 and nurr1 genes were co-expressed across entire cortex and claustrum, but cux2 and nurr1 were co-expressed only in the insular cortex and claustrum. Latexin was expressed, in the macaque, only in the claustrum. The nurr1+ claustral neurons expressed VGluT1, a marker for cortical glutamatergic cells and send cortical projections. Taken together, our data suggest a partial commonality between claustral neurons and a subtype of cortical neurons in the monkey brain. Moreover, in the embryonic (E110) macaque brain, many nurr1+ neurons were scattered in the white matter between the claustrum and the insular cortex, possibly representing their migratory history. In a second set of experiments, we injected Lucifer Yellow intracellularly in mouse and rat slices to investigate whether dendrites of insular and claustral neurons can cross the border of the two brain regions. Dendrites of claustral neurons did not invade the overlying insular territory. In summary, gene expression profile of the claustrum is similar to that of the neocortex, in both rodent and macaque brains, but with modifications in density of expression and cellular co-localization of specific genes.

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“…These tracers, largely fluorescent, can be used to map the connections emerging from an area of interest or the regions projecting onto the region of interest. This approach, recently utilized in the mouse (Wang et al, 2011) and the rat (Watakabe et al, 2012), can be combined with 3D modeling to provide details on the functional relationship between areas. Additionally, these paradigms can also be applied in developmental studies to determine when areas become wired together and therefore the relative hierarchy of individual areas (e.g., the establishment of thalamocortical connections in the mouse) (Little et al, 2009; Deck et al, 2013).…”

Section: How Are Visual Cortical Areas Defined?mentioning

confidence: 99%

Mapping arealisation of the visual cortex of non-primate species: lessons for development and evolution

Homman‐Ludiye

Bourne

2014

Front. Neural Circuits

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The integration of the visual stimulus takes place at the level of the neocortex, organized in anatomically distinct and functionally unique areas. Primates, including humans, are heavily dependent on vision, with approximately 50% of their neocortical surface dedicated to visual processing and possess many more visual areas than any other mammal, making them the model of choice to study visual cortical arealisation. However, in order to identify the mechanisms responsible for patterning the developing neocortex, specifying area identity as well as elucidate events that have enabled the evolution of the complex primate visual cortex, it is essential to gain access to the cortical maps of alternative species. To this end, species including the mouse have driven the identification of cellular markers, which possess an area-specific expression profile, the development of new tools to label connections and technological advance in imaging techniques enabling monitoring of cortical activity in a behaving animal. In this review we present non-primate species that have contributed to elucidating the evolution and development of the visual cortex. We describe the current understanding of the mechanisms supporting the establishment of areal borders during development, mainly gained in the mouse thanks to the availability of genetically modified lines but also the limitations of the mouse model and the need for alternate species.

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Area‐specific substratification of deep layer neurons in the rat cortex

Cited by 37 publications

References 65 publications

Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity

Towards a unified scheme of cortical lamination for primary visual cortex across primates: insights from NeuN and VGLUT2 immunoreactivity

Characterization of claustral neurons by comparative gene expression profiling and dye-injection analyses

Mapping arealisation of the visual cortex of non-primate species: lessons for development and evolution

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