A quantitative analysis of the spinal motor pool and its target muscle during growth in the dogfish, <i>Scyliorhinus canicula</i>

116

Recent studies of the spinal motor systems of vertebrates allow us to begin to infer the organization of the motor apparatus of primitive vertebrates. This paper attempts to define some of the features of the motor system of early vertebrates based on studies of the motor systems in anamniotes and in Branchiostoma. It also deals with some changes in the primitive motor system during evolution. The primitive motor system consisted of myomeric axial muscles, with a functional subdivision of the musculature into non-spiking slow muscle fibers segregated in the myomeres from spiking fast ones. These fibers were innervated by two major classes of motoneurons in the cord - large motoneurons innervating faster fibers and small motoneurons innervating slow fibers. There was not a simple isomorphic mapping of the position of motoneurons in the motor column onto the location of the muscle fibers they innervated in the myomeres. Early vertebrates used these axial muscles to bend the body, and the different types of muscle fibers and motoneurons reflect the ability to produce slow swimming movements as well as very rapid bending associated with fast swimming or escapes, The premotor network producing bending was most likely a circuit composed of a class of descending interneurons (Dls) that provided excitation of ipsilateral motoneurons and other interneurons, and inhibitory commissural interneurons (CIs) that blocked contralateral activity and played an important role in generating the rhythmic alternating bending during swimming. This DI/CI network was retained in living anamniotes. At least two major descending systems linked the sensory systems in the head to these premotor networks in the spinal cord. The ability to turn on swimming by activation of DI/CI premotor networks in the cord resided at least in part in a midbrain locomotor region (MLR) that influenced spinal networks via projections to the reticular formation. Reticulospinal neurons were important not only for initiation of rhythmic swimming but also in the production of turning movements. The reticulospinal cells involved in turns produced their effects in part via monosynaptic connections with motor neurons and premotor interneurons, including some involved in rhythmic swimming. A prominent and powerful Mauthner cell was most likely present and important for rapid escape or startle movements. Some features of this primitive motor apparatus were conserved during the evolution of vertebrate motor systems, and others changed substantially. Many features of the early motor system were retained in living anamniotes; major changes occur among amniotes. Some of these changes include the breakup of the myomeres into a large number of discrete axial muscles, as well as the development of paired fins and limbs and the associated limb muscles. The primitive segregation of fiber types was lost in many of the muscles arising from the myomeres. Non-spiking slow fibers and spiking fast ones were retained in most vertebrates but were lost in most mammalian muscles. The moto...

Section: K5mentioning

confidence: 99%

“…In cartilaginous and bony fishes, the slow fibers form a red band of muscle along the superficial surface of the myo mere just beneath the skin, as illustrated in figure IB [Fctcho. 1986a;Mos and Williamson. 1986].…”

Section: Musculature Anil Its Innervationmentioning

confidence: 99%

The Spinal Motor System in Early Vertebrates and Some of Its Evolutionary Changes

Fetcho¹

1992

116

“…In general, increases in stri ated muscle mass (fiber number and/or diameter) be yond a certain body size are accompanied mainly by an increase in the diameter of myelinated axons ra ther than an increase in their number [Easter, 1979;van Raamsdonk el al., 1983;Mos and Williamson, 1986]. One exception was stingrays, for which increas ing myotomal muscle mass was correlated with in creasing motoneuron number throughout an animal's lifetime [Leonard etal., 1978],…”

Section: Sonic Motor Systemmentioning

confidence: 99%

Inter- and Intrasexual Dimorphisms in the Vocal Control System of a Teleost Fish: Motor Axon Number and Size

Bass

Andersen²

1991

In one species of vocalizing fish, the plainfin midshipman (Porichthys notatus), large, nest-guarding males ('type I') use striated muscles to produce acoustic communication signals that include short duration (< 1 s) 'burps' important in agonistic encounters and long duration (in the order of minutes) 'hums' which function in attracting females to nest sites during the breeding season. Females, and a second group of smaller reproductively active males ('type II') that 'sneak' spawn, do not generate hums, although they produce burps. Differences in vocal behavior are paralled by a relative increase of 6-fold in the sonic muscle of type I males. Inter- and intrasexual dimorphisms in sonic muscle mass were matched by those in the cross-sectional area of sonic motor axons, but not by those in number of axons. Thus, axon size was 2- to 3-fold larger in type I males than in females, type II males, or juveniles, none of which differed significantly from each other. Axon number was similar between type I males and females of a similar body size, despite the extreme dimorphism in sonic muscle mass. Axon number, however, was slightly greater (0.1-fold) in type I males and females compared to the smaller-sized juveniles and type II males. Type II males, in comparison to the non-reproductive juvenile males, have gonads that are about 20-fold larger and produce mature sperm. Nevertheless, the two groups resemble each other in body and swimbladder size, as well as sonic motor axon size and number. This suggests that type II males represent a subset of juvenile males that undergo precocious gonadal hypertrophy and spermiogenesis, but retain juvenile-like nongonadal traits. The results are discussed within the context of the development of vertebrate motor systems as well as the evolution of alternative reproductive tactics among teleost fishes.

“…and Retires. 1983], the axial muscle of dogfish sharks [Mos and Williamson. 1986], and the hindlimb muscles of amphib ians [Sperry.…”

Section: Changing Muscle Size: Central Nervous Systemmentioning

confidence: 99%

The Ontogeny of Inter- and Intrasexual Vocal Muscle Dimorphisms in a Sound-Producing Fish

Brantley

Tseng

Bass³

1993

This study documents the development of inter- and intrasexual dimorphisms in the vocal ('sonic') muscles of the swimbladder in the plainfin midshipman fish, Porichthys notatus. Midshipman have two male reproductive morphs, Types I and II. Only Type I males build nests and generate mate calls to attract females; Type II males sneak or satellite spawn. Vocal muscles in the mate-calling Type I males were 25-fold larger in absolute size (sixfold larger when scaled to body size) compared with females or non-calling Type II males. Dimorphisms in muscle mass were correlated with dimorphisms in fiber number and diameter. Only nascent Type I males experienced a pre-maturational, fourfold increase of fiber number followed by a rapid, fivefold increase in fiber cross-sectional area at sexual maturity. Also specific to Type I males was a striking change in cell structure: the ratio of sarcoplasm to myofibril area increased fivefold. By contrast, Type II males and females matured without showing any of these changes in sonic muscle – the trajectories which described juvenile growth continued to hold through maturity and adulthood. The results indicate distinct, non-sequential, ontogenetic trajectories for Type I and Type II males. The origin of the Type II male morphotype is described as paedomorphosis by progenesis: size distributions of free-living animals suggest that Type II males can mature precocially as one-year-old fish, whereas Type I males defer reproduction until they are at least two years of age.