Comparative morphology of gigantopyramidal neurons in primary motor cortex across mammals

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Gigantopyramidal neurons in primary motor cortex (M1), referred to as Betz cells in primates (Betz, 1874), are generally characterized by large somata (Brodmann, 1909) and idiosyncratic basilar dendritic arrays (Scheibel & Scheibel, 1978a; Walshe, 1942). Investigations of these neurons have historically focused on soma size and shape (Vogt & Vogt, 1942; von Bonin, 1938; von Economo & Koskinas, 1925), with only qualitative descriptions of dendritic morphology in a limited number of species: human (Braak & Braak, 1976; Rivara, Sherwood, Bouras, & Hof, 2003), monkey (species unspecified; Gatter, Sloper, & Powell, 1978), domestic cat (Kaiserman‐Abramof & Peters, 1972; Lewis, 1878), and sheep (Ebinger, 1975; Lewis, 1878). Betz initially observed similarities in the form and location of these “Riesenpyramiden” (p. 578) between primates and canids. Later, Brodmann observed variation in gigantopyramidal soma size across species. Recently, quantitative investigations have included measures of dendritic extent in individual species (giraffe: Jacobs, Harland, et al., 2015; Siberian tiger, clouded leopard: Johnson et al., 2016). Nevertheless, there are currently no quantitative studies comparing dendritic measures in gigantopyramidal neurons across multiple species. To this end, using available tissue of sufficient quality, the present investigation documents both qualitative and quantitative aspects of gigantopyramidal neurons in the primary motor cortices of 19 species across 7 phylogenetic orders: carnivores: suborder caniforms (African wild dog, domestic dog), carnivores: suborder feliforms (banded mongoose, caracal, clouded leopard, Siberian tiger, African lion), perissodactyls (mountain zebra, plains zebra), artiodactyls (blue wildebeest, greater kudu, giraffe), primates (ring‐tailed lemur, golden lion tamarin, chacma baboon, human), a lagomorph (Flemish giant rabbit), a murid rodent (Long‐Evans rat), and a diprotodont marsupial (Bennett's wallaby). To supplement these findings and to determine whether Brodmann's observations of substantially larger gigantopyramidal neurons in carnivores than in primates hold across a broader range of species, we also employed unbiased stereology to explore layer V pyramidal and gigantopyramidal neuron volumes in M1 between carnivores (11 species) and primates (9 species).
In humans, early counts suggested approximately 30,000 Betz cells per hemisphere (Campbell, 1905; Lassek, 1940; Scheibel & Scheibel, 1978a); however, more recent stereological investigation suggests over four times this number (∼125,290) in layer Vb of left M1 (Rivara et al., 2003). Within M1, 75% of these neurons are located in the dorsal third of the gyrus, which contains representations of the lower limb, 18% are found in the medial third, corresponding to the upper limb, and 7% are located in the inferior third, representing the face region (Lassek, 1940). Both soma size and density are graded along the mediolateral axis of the precentral gyrus such that the largest somata are found in areas controlling the lower limb, with the greatest density of gigantopyramidal neurons located in areas controlling the upper limb (Lassek, 1940; Rivara et al., 2003; von Bonin, 1949). Physiologically, gigantopyramidal neurons appear to be phasically active, exhibiting a rapid bursting pattern believed to introduce partial inhibition of the extensor muscles along with flexor facilitation prior to a movement, and a restoration of extensor tone immediately after the movement (Evarts, 1965; Lundberg & Voorhoeve, 1962). It has therefore been suggested that these neurons modulate the output of surrounding deep pyramidal neurons during the initiation of motor programs (Scheibel, Davies, Lindsay, & Scheibel, 1974). For the lower limb, this system appears to play a major role in the control of anti‐gravity muscles involved in posture and locomotion (Scheibel & Scheibel, 1978a; Scheibel et al., 1974; Scheibel, Tomiyasu, & Scheibel, 1977). For the upper limb, gigantopyramidal neurons appear to be involved in the fine motor control of the hand and wrist (Lemon, 2008; Lemon, Kirkwood, Maier, Nakajima, & Nathan, 2004).
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