Gradients in cytoarchitectural landscapes of the isocortex: Diprotodont marsupials in comparison to eutherian mammals

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The isocortex of many mammals can be subdivided into six layers. Neurons across the depth of the isocortex can be further distinguished by their patterns of connectivity, with neurons located in supragranular and granular layers (layers II–IV) predominantly connecting to other cortical structures whereas many lower‐layer neurons (layers V–VI) project to subcortical structures (Barbas, 1986; Gilbert & Kelly, 1975; Hof, Nimchinsky, & Morrison, 1995; Nudo & Masterton, 1985). During development, newly born neurons migrate from the proliferative zones to the cortical plate. Neurons born earlier in development migrate to assume locations within lower layers and neurons born later in development are positioned within upper layers (Bayer & Altman, 1991; Rakic, 1974; Sanderson & Weller, 1990). Consequently, neurons across the depth of the cortex and across the cortical surface are organized according to their birth order and connectivity patterns (Gaspard & Vanderhaeghen, 2011).
Several recent quantitative comparisons have been made to examine the evolution of upper and lower‐layer neuron numbers across mammals. This approach is useful in identifying evolutionary changes in distributions of neurons projecting cortically from those projecting subcortically. It is also useful in relating cross‐cortical variation in neuron numbers with the developmental mechanisms that generate them (Charvet, Reep, & Finlay, 2016b; Cheung et al., 2010; Finlay & Uchiyama, 2015). Recent studies have shown that primates possess disproportionately more upper‐layer neurons than many other mammals, which suggests that primates possess increased numbers of corticocortically projecting neurons (Charvet, Cahalane, & Finlay, 2015; Charvet et al., 2016a, 2016b; O'Kusky & Colonnier, 1982).
There is extensive variation in neuron numbers across the isocortex of primates (Beaulieu, 1993; Beaulieu & Colonnier, 1989; Charvet et al., 2015; Collins, Airey, Young, Leitch, & Kaas, 2010; Srinivasan, Carlo, & Stevens, 2015). In primates, neuron numbers vary systematically across the isocortex, with more neurons per unit of cortical surface area found toward the posterior pole (i.e., primary visual cortex) than toward the anterior pole (Cahalane, Charvet, & Finlay, 2012; Collins et al., 2010; Turner et al., 2016). Most of this variation is accounted for by upper‐layer neurons (Charvet et al., 2015). In other species examined to date, such as rodents, carnivores, and manatees, the variation in neuron numbers per unit of cortical surface area is not as extensive as it is in primates (Beaulieu, 1993; Beaulieu & Colonnier, 1989; Charvet et al., 2015). Yet, we still know very little about cross‐cortical variation in neuron numbers in mammals other than rodents, primates, and a few other species.
Marsupials represent an interesting infraclass of mammals to investigate variation in cortical neuron distributions. Marsupials comprise a highly diverse taxonomic group in that they exhibit a wide range of adaptations (Karlen & Krubitzer, 2007) and they diverged from other mammals more than 125–140 million years ago. Consequently, they are distantly related to eutherian mammals (Bininda‐Emonds et al., 2007; Luo, Yuan, Meng, & Ji, 2011). It has been claimed that marsupial mammals possess fewer isocortical neurons and especially few upper‐layer neurons per unit of cortical surface area compared to eutherian mammals. This notion primarily derives from a handful of studies that almost exclusively focused on the gray short‐tailed opossum (e.g., Monodelphis domestica, Cheung et al., 2010; Haug, 1987; Seelke, Dooley, & Krubitzer, 2013). As such, how neuron densities vary across this diverse taxonomic group remains poorly understood.
In the present study, we quantified neuron numbers per unit of cortical surface area in upper (layers II–IV) and lower layers (layers V–VI) systematically across the rostral to caudal and medial to lateral axes of the isocortex of several diprotodont marsupial species, including red kangaroo (Macropus rufus), parma wallaby (Macropus parma), and koala (Phascolarctos cinereus).
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