Topographic Position of Forelimb Motoneuron Pools Is Conserved in Vertebrate Evolution

Abstract

The neuromotor conservatism hypothesis predicts that neuromotor patterns in homologous tetrapod muscles are conserved evolutionarily despite the musculoskeletal modifications of vertebrate limbs. A complete description of the anatomical organization of the neurons innervating homologous limb muscles is a prerequisite to any test of the neuromotor conservatism hypothesis. This study uses the retrograde neuronal tracer WGA-HRP to selectively label the motor neuron pools of seven homologous forelimb muscles in mice (Mus musculus) and iguanas (Iguana iguana): Mm. pectoralis, spinodeltoideus, biceps brachii, lateral and long heads of triceps brachii, and the supraspinatus and infraspinatus (in mice) or their reptilian homolog, the supracoracoideus (in iguanas). In vertebrates, motoneurons are arranged in longitudinal columns of cells in the ventral horn of the spinal cord. Mouse motor pools average 1,952 μm in length, except the pectoralis pool which averaged 2,949 μm in length. Iguana pools average 3,196 μm in length. The number of neurons per pool ranged from 70–199 in mice and from 58–114 neurons in iguanas. In both iguanas and mice the motor pools for the spinodeltoids, biceps, and the supracoracoideus (or its mammalian homologs) lie anterior to the pectoralis and triceps motor pools. In the transverse plane, the pectoralis pool lies medial to those of the triceps. The pools of the biceps and spinodeltoids are located dorsal and lateral to those of the pectoralis and supracoracoideus (or its homologs in mammals). The resulting motor pool maps support the hypothesis that the anatomical organization of motoneurons in ancestral reptiles has been retained in these two tetrapod descendents.

Neuromuscular Correlates to the Evolution of Flapping Flight in Birds

“…The supracoracoideus nucleus extends one to two segments more rostral than the pectoralis nucleus but its relative position to the motor nuclei of the shoulder muscles in reptiles and terrestrial and flying mammals remains the same. We agree with Ryan et al [1998] that the motor nucleus distribution of the supracoracoideus is conserved and does not reflect the muscle's new function in birds.…”

“…In recent studies designed to determine the variability of motor nuclei location within the motor column for specific homologous muscles across tetrapods, Ryan et al [1997Ryan et al [ , 1998] investigated the motor nuclei of four shoulder muscles (including the pectoralis, supracoracoideus and triceps) in the Iguana lizard (Iguana iguana), the Mouse (Mus musculus), and two species of bats, the Big Brown bat (Eptesicus fuscus) and the Little Brown bat (Myotis lucifugus). Ryan and colleagues compared their findings to the distribution patterns of motor nuclei in the only bird for which the data were available, the Domestic fowl (Gallus domesticus) [Ohmori et al, 1982].…”

Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: A retrograde carbocyanine dye analysis

“…The topographic organization of forelimb motoneurons in the rat spinal cord is concordant with the rostrocaudal pattern of motor column organization observed in divergent animals, including primates (Sherrington, 1898;Jenny and Inukai, 1983), bats (Ryan et al, 1997), mice, and iguanas (Ryan et al, 1998). The consistent position of triceps motoneurons in these disparate animals probably reflects a more caudal embryologic and, perhaps, phylogenetic development of the triceps muscle relative to the biceps (cf.…”

“…Accordingly, it has been proposed that spinal cord motor circuitry is highly conserved across diverse species (Romanes, 1964;Landmesser, 1978a,b;Horner and Kummel, 1993;Ryan et al, 1997Ryan et al, , 1998. There is far less acceptance, however, of suggested interspecies homologies in behavior.…”

Red nucleus projections to distinct motor neuron pools in the rat spinal cord

“…Proximal limb motoneurons are found on more rostral and more ventral levels. This motoneuronal pool location is highly conserved in tetrapods (Sterling and Kuypers, 1967;Jenny and Inukai, 1983;Horner and Kummel, 1993;Ryan et al, 1998). Figure 3B for orientation.…”