Targets and Laminar Distribution of Projection Neurons with ‘Inverted’ Morphology in Rabbit Cortex

Abstract

This study examines the axonal projections of so-called inverted pyramids and other neurons with their major dendritic shaft oriented in the direction of the white matter ('inverted cells') in the adult rabbit cortex. Single injections of horseradish peroxidase wheat germ agglutinin were made into cortical or subcortical sites. The resulting retrograde labelling in the cortex was analysed and the distribution across areas and layers of inverted cells contributing to each of these projections was estimated. In addition, the radial distribution of inverted cells was independently determined from rapid Golgi-impregnated and Nissl-stained material. All three procedures revealed that inverted cells lay overwhelmingly in infragranular layers, but congregated at the border between layers 5 and 6. Inverted cells, identified by retrograde labelling, seldom furnished non-telencephalic centres; in contrast, these cells constituted a major source for the projections to the ipsi- or the contralateral cortex, the claustrum or the nucleus caudatus. In general, each set of inverted cells (when defined by its specific destination as a group) was located below the typically oriented cells whose axons were aimed at the same target. Thus, the inverted cells of the rabbit cortex are characterized not only by their unique morphology and their corticocortical, corticoclaustral and corticostriatal projections, but also by their distinctive radial locations. These findings suggest that inverted cells, even though possibly composed of different cell types, are a specific class of projection neurons.

Projections, Partaken Circuits and Axon Initial Segments of Cortical Principal Neurons

“…Spiny inverted pyramidal cells are morphologically and numerically conspicuous among the cells of layers 5-6 furnishing the associative backward projection in rabbits and cats; these cells also originate an important proportion of commissural, cortico-claustral and cortico-striatal projections; they neglegeably project to extratelencephalic centres such as the geniculate nuclei, colliculi and pons [23,27,33]. See Table 1 for a summary and [28] for a review; see also Section 4 in this Chapter for more data on AIS of these cells.…”

“…This is the so-called associative forward projection [31]. In turn, the associative backward projection arise from cells sited in layers 2/3 and 5-6 of higher-order areas to innervate layers 1 and, to a lesser extent, 3, 5 and 6 of areas of lesser-order hierarchy [23,27,32]. This layer-segregation of forward and backward projections indicates that they target very different neuronal elements in recipient regions [18].…”

“…Most associative and commissural axons emerge from pyramidal cells sited in layers 2/3 and 5-6, and also from spiny inverted pyramidal cells and other polymorphic cells of layers 5-6 [23,27,28]. The axons of all these cells extend forward to innervate the layer 4 of cortical areas of higher-order hierarchy [23,[27][28][29][30]. This is the so-called associative forward projection [31].…”

“…Commissural axons result from a broad and anatomically diverse population of principal cells that are located primarily in layers 2/3, 5 and 6 of restricted areas; there are interspecies differences in the laminar address of commissural neurons; in ferrets, rabbits and rats the commissural neurons predominate in infragranular layers [23,26,27,34,35]. Commissural cells can be further defined based on patterns of collateral projections to the ipsi-and contralateral striata and cortices, as well as by the expression of combinations of molecular markers [36].…”

“…Upright pyramidal neurons can be further subdivided (see below). In addition to upright pyramidal neurons, in layers 5-6 there is another collection of projection cells, of spiny nature too, the polymorphic-cell subgroup [19][20][21][22][23]. The spiny stellate neurons of layer 4 are an exception to the spiny-cell/extrinsic-projection correlation, because they are implicated in the canonical thalamo-cortical reciprocal circuit.…”