Comparative morphology of gigantopyramidal neurons in primary motor cortex across mammals

Abstract

Gigantopyramidal neurons, referred to as Betz cells in primates, are characterized by large somata and extensive basilar dendrites. Although there have been morphological descriptions and drawings of gigantopyramidal neurons in a limited number of species, quantitative investigations have typically been limited to measures of soma size. The current study thus employed two separate analytical approaches: a morphological investigation using the Golgi technique to provide qualitative and quantitative somatodendritic measures of gigantopyramidal neurons across 19 mammalian species from 7 orders; and unbiased stereology to compare the soma volume of layer V pyramidal and gigantopyramidal neurons in primary motor cortex between 11 carnivore and 9 primate species. Of the 617 neurons traced in the morphological analysis, 181 were gigantopyramidal neurons, with deep (primarily layer V) pyramidal (n = 203) and superficial (primarily layer III) pyramidal (n = 233) neurons quantified for comparative purposes. Qualitatively, dendritic morphology varied considerably across species, with some (sub)orders (e.g., artiodactyls, perissodactyls, feliforms) exhibiting bifurcating, V-shaped apical dendrites. Basilar dendrites exhibited idiosyncratic geometry across and within taxonomic groups. Quantitatively, most dendritic measures were significantly greater in gigantopyramidal neurons than in superficial and deep pyramidal neurons. Cluster analyses revealed that most taxonomic groups could be discriminated based on somatodendritic morphology for both superficial and gigantopyramidal neurons. Finally, in agreement with Brodmann, gigantopyramidal neurons in both the morphological and stereological analyses were larger in feliforms (especially in the Panthera species) than in other (sub)orders, possibly due to specializations in muscle fiber composition and musculoskeletal systems.

Comparative neocortical neuromorphology in felids: African lion, African leopard, and cheetah

“…In general, the neuronal types observed in the African lion, African leopard, and cheetah appeared consistent with those in other nondomestic felids (Jacobs et al, ; Johnson et al, ). Although there were morphological similarities across neurons in the three species studied, those traced in the cheetah tended to have more complex dendrites than those in the African leopard, despite their similar brain masses.…”

“…First, the relatively poor Golgi stain quality in the lion tissue, perhaps because of a prolonged storage time, prohibited quantitative comparisons with the other felids. The necessity for this exclusion becomes clear when one compares the average TDL values of M1 pyramidal neurons (5,399 ± 312 μm; soma depth = 1,087 ± 78 μm) in the lion from Jacobs et al () to the average TDL values obtained in the current study (4,135 ± 187 μm; soma depth = 984 ± 87 μm). The discrepancy is even greater for M1 gigantopyramidal neurons, with TDL at 8,600 ± 814 μm in Jacobs et al () but only 1,872 ± 215 μm in the current study.…”

“…The necessity for this exclusion becomes clear when one compares the average TDL values of M1 pyramidal neurons (5,399 ± 312 μm; soma depth = 1,087 ± 78 μm) in the lion from Jacobs et al () to the average TDL values obtained in the current study (4,135 ± 187 μm; soma depth = 984 ± 87 μm). The discrepancy is even greater for M1 gigantopyramidal neurons, with TDL at 8,600 ± 814 μm in Jacobs et al () but only 1,872 ± 215 μm in the current study. Nevertheless, the broader sampling of neuron types (Figure ) in the present study provides a valuable supplement to the pyramidal and gigantopyramidal tracings in Jacobs et al ().…”

“…As noted by Arnold Scheibel, it is “one of the only histological techniques with personality” (Scheibel & Scheibel, , p. 90), meaning that one cannot predict the outcome of any given stain (Friedland, Los, & Ryugo, ). Moreover, the stain is sensitive to postmortem delay variations, as well as types and length of fixation (Butti et al, ; Jacobs et al, ; Jacobs et al, ; Johnson et al, ). Especially relevant for quantitative investigations is the fact that dendritic measures (especially in larger neurons) are usually attenuated because of the 120 μm section thickness (Anderson et al, ; Jacobs et al, ; Jacobs & Scheibel, ), and that spine measures in light microscopy are always underestimations (Jacobs et al, ; Jacobs et al, ).…”

“…Both Golgi and stereological techniques also provided size comparisons of gigantopyramidal neuron somata across the three species. Given previous findings for Panthera , M1 gigantopyramidal neurons in both the African lion and African leopard were expected to be exceptionally large relative to other carnivore species, potentially due to their specialized hunting behaviors (Jacobs et al, ; Johnson et al, ). However, the somatodendritic characteristics of M1 gigantopyramidal neurons in the cheetah have not been documented previously.…”