Small-scale pattern formation in a cortical area of the embryonic chicken telencephalon.

The parahippocampal area is a cortical region of the avian dorsomedial telencephalon. In the chicken embryo, it contains discrete clusters of cadherin-7-positive cells, which are embedded in a cadherin-7-negative matrix. In the present work, the development and spatial distribution of these clusters is studied in whole-mount specimens. The clusters form a complex, coherent pattern of patches of variable size, spacing, and staining intensity. The pattern is especially prominent and regularly spaced in the rostral part of the caudolateral parahippocampal area. Here, it consists of stripes and connecting bridges with an average periodicity of approximately 0.3 mm. This pattern vaguely resembles some animal fur patterns and the ocular dominance domain of the mammalian visual cortex. The cadherin-7-positive patches also differ from their surrounding area by their cytoarchitecture and their increased acetylcholinesterase activity, suggesting that they represent functionally specialized subregions within the parahippocampal area. During development, the patchiness is first observed between 9 and 10 days of incubation and gradually becomes more prominent until 15 days of incubation. Our results indicate that the patchy organization of cortical gray matter on a small scale of periodicity (below 1 mm), which is well studied in the mammalian neocortex, is also found in the avian telencephalon.

Cadherin expression coincides with birth dating patterns in patchy compartments of the developing chicken telencephalon.

Some gray matter regions of the vertebrate brain, e.g., the mammalian striatum, are organized into clusters of functionally similar neurons ("patches") that are surrounded by a gray matter matrix. A similar type of compartmentation recently has been found also in the avian telencephalon, based on two sorts of evidence. First, a birth dating study showed that, in some telencephalic areas, cells born at the same time form "isochronic" cell clusters, which differ in their birth dating pattern from their surrounding tissue. Second, patchy expression was found for different members of the cadherin family of adhesion molecules (R-cadherin, N-cadherin, and/or cadherin-7). The relation between these two findings has remained unclear. Here, we demonstrate a general spatial coincidence between the birth dating patterns and the heterogeneities in cadherin expression. This coincidence is found in areas of the avian ventral and lateral pallium (ventral hyperstriatum, neostriatum, and ectostriatum) and in a part of the archistriatum, which is of pallial origin. For example, in the neostriatum, a part of the ventral pallium, both the cadherin-7-positive patches and their R-cadherin-positive surroundings are born between embryonic day 5 and 7, but the cadherin-7-positive cells are born during a shorter time period than the R-cadherin-positive cells. We propose that the patchy gray matter architecture observed in the mammalian striatum and avian pallium are regulated by a common type of morphogenetic mechanism. This mechanism possibly involves the differential expression of adhesive factors, such as cadherins.

Patch/matrix patterns of gray matter differentiation in the telencephalon of chicken and mouse.

The mammalian striatum, a subpallial area, consists of two compartments (patches/striosomes and matrix) that differ in their neuronal birth dates, connectivity, neurochemistry, and molecular make-up. For example, members of the cadherin family of adhesion molecules (cadherin-8 and OL-protocadherin) are differentially expressed by the striosomes and the striatal matrix. A patch/matrix type of organization also has recently been found in the ventral hyperstriatum and the neostriatum of the chicken pallium, where cell clusters of similar birthdates ("isochronic" clusters) are surrounded by a matrix of cells that are born at a different time. Immunostaining with antibodies against cadherins reveals a similar arrangement of cell clusters. In the avian neostriatum, cadherin-7-positive cell clusters ("islands") are surrounded by a matrix of cells that express R-cadherin. The islands coincide, at least in part, with the isochronic cell clusters, as shown by pulse-labeling with bromodeoxyuridine. Likewise, isochronic clusters of the hyperstriatum ventrale relate to patchy heterogeneities in the cadherin-7 immunoreactivity pattern. Cadherins are known to mediate the aggregation and sorting of cells during development in many organs. Their differential expression by isochronic cell populations in the mammal subpallium and avian pallium suggests a common morphogenetic mechanism that regulates the formation of the patch/matrix patterns in these regions.