Our observations of the attachment points of the MLC3F-nlacZ mouse TSP muscles correlate well with the general pattern reported in some species of mice (M. musculus and Micromys minutus) (Hesse et al.,2010) and other mammals (Slijper,1946; Brink and Pfaff,1980; Stubbs et al.,2006), with muscles existing in the space between the transverse and spinous processes and attaching in a regular, repeated pattern to bony sites throughout the lumbar spine.
Although the general pattern of TSP muscle attachment through the lumbar spine is similar across species, there are differences in the number of vertebral segments spanned by muscles attaching to a single vertebral level. In the human (Homo sapiens) and horse (Equus ferus caballus), muscles span at least four vertebral segments (Macintosh et al.,1986; Stubbs et al.,2006), in the golden hamster the maximum span is two vertebral levels (Salih and Kent,1964), and in the Albino rat fibers pass “more than four vertebrae” (Brink and Pfaff, 1980). Rinker (1954) observed these muscles in the cotton rat (Sigmodon), rice rat (Oryzomys), wood rat (Neotoma), and deer mouse (Peromyscus maniculatus), stating that the TSP muscles in these animals spanned only three segments. A recent investigation by Hesse et al. (2010) examined the paravertebral muscles of Mus musculus and Micromys minutus. They described a multifidus muscle originating from the transverse process and spanning four vertebrae to attach to the spinous process of the fourth vertebrae craniad, and the rotatores muscles are described as spanning only one vertebral level. This indicates that Hesse et al. (2010) found no TSP muscle fibers spanning two or three vertebral levels, and therefore the observations in these mouse species differ from the results of our investigation. Although we also found that some TSP muscles spanned four vertebral segments, our specimens also had muscle fibers spanning one, two, three, and four vertebral levels. Therefore, it appears that there is some variation in the extent and attachments of the TSP muscles between mouse species.
In the human and horse, several studies have reported that the lumbar TSP muscles at each spinal level are effectively separated into a set of distinct muscles, each having a distinct caudal attachment (Macintosh et al.,1986; Stubbs et al.,2006; Rosatelli et al.,2008). However, in the laboratory mouse, we find that the TSP muscle at each segmental level is formed from one continuous group of muscle fibers with no sign of differentiation into separate muscles. Our findings are similar to those reported in the lumbar spine of various species of rat (Rinker,1954; Brink and Pfaff, 1981), mouse (Rinker,1954), and golden hamster (Salih and Kent,1964). Slijper (1946) has also found such unseparated lumbar TSP muscles in the dugong and the sloth (Bradypus), along with many other mammals including possum (Trichosurus vulpecular), moonrat (Echinosorex gymnura), shrew (Sorex), tree shrew (Tupaia), and sand rat (Psammomys). Interestingly, Slijper (1946) indicated that the TSP muscles in many animals can be well separated and defined in the prediaphragmatic region though remain unseparated in the postdiaphragmatic area, with this arrangement also seen in the Albino rat (Brink and Pfaff, 1981). We did not examine the prediaphragmatic region in our study; however, casual observation of the caudal thoracic region suggested an undifferentiated structure of the TSP muscles in the laboratory mouse. Whether such variations are due to the size of the animal or to differences in function between the regions remain unclear.
The only variation between our results and those from other authors investigating common laboratory rodents was that a cleavage plane was always apparent between the intermammillares muscle and the rest of the TSP muscle “bundle.” Whether muscle “differentiation” into well-defined and separate muscular elements occurs as a result of animal size in mammalian development, or relates to differences in function, is as yet unknown. This “undefined” TSP muscle arrangement raises the question: how are individual TSP muscles confidently identified when no cleavage plane exists? Using the “length-based” definitions of Slijper (1946), rotatores brevis and longus span one and two vertebral levels, respectively, the multifidus muscle spans “either three or four segments,” and the semispinalis muscle four or more. The interpretation of our results using Slijper's system therefore suggests that the fibers spanning one to three segments could be classified as contributing to the rotatores brevis, rotatores longus, and multifidus muscles, with the longer fibers spanning four segments nominated as part of either multifidus or semispinalis.
However, using a system based solely on the location of physical attachment points is far from ideal when one addresses issues such as biomechanical modeling. By definition (Standring,2008), individual muscles are surrounded by their own sheath of epimysium. This creates a paradox when examining and naming individual TSP muscles arising from a single vertebral level in the lumbar spine of small mammals, where to a large degree this encapsulation by an epimysial sheath and separation of muscles by a definite cleavage plane does not occur. Using the example of undefined and well-separated TSP muscles, it is suggested that the nomenclature used to identify individual lumbar TSP muscles could be revisited to clarify the muscular elements that exist in this region.
It is also noteworthy that existing descriptions of the human muscles in this region only consist of one muscle, multifidus, yet in other mammals the intermammillares, rotatores longus and brevis, multifidus, and semispinalis are all described (Slijper,1946). The reasons for the inconsistency in terminology between humans and other mammals are not discussed in the literature.
The mouse TSP muscles consisted entirely of muscle bundles and fascicles with single MEP regions, located approximately at their mid-point. The absence of multiple MEP bands shows that the muscles are not constructed of a series of fibers arranged along the muscle length, but rather that single muscle fibers extend from tendon to tendon. This is of particular interest, because of the embryological origin of these muscles from the segmental myotome. During development in the rat (Rattus rattus), the TSP muscles arise by reorientation and elongation of the myotomal fibers, during which process adjacent myotomes blend together (Deries et al.,2008). Thus, it seemed likely that the longer fascicles of the TSP muscles might be constructed of fibers from multiple segments arranged in an end-to-end series. The results presented here show this is not the case, but rather that the mouse TSP muscles have a simple parallel-fibered arrangement consistent with that seen in most other small mammalian muscles, rather than the in-series arrangement seen in many larger mammalian muscles (Richmond and Armstrong,1988; Gans and Gaunt,1991; Paul et al.,2004).
Suggestions can be made about the likely functional significance of this arrangement. The neural activation and subsequent development of force are potentially more complex in those muscles that have multiple MEP zones (Gans and Gaunt,1991; Heron and Richmond,1993; Sheard et al.,2002), although the speed of contraction is potentially greater than in muscles with only one zone of MEPs (Gaunt and Gans,1992; Heron and Richmond,1993). This is because an in-series muscle fiber arrangement is thought to allow a more synchronous contraction of a long muscle bundle, because there are multiple points at which neuromuscular activation occurs. However, muscles with multiple MEP zones are thought to have a poorer ability to manage tasks requiring fine motor control (Sheard,2000) because efficient contraction requires synchronous activation of multiple motor units. The in-parallel arrangement of fibers within these muscles suggests that they are not designed to generate large forces, but are more appropriate for making small adjustments in length, thus producing “fine tuning” of the movements of the vertebral column.
This study provides morphological information about the paravertebral muscles in the laboratory mouse, with the TSP muscles in the lumbar spine of the MLC3F-nlacZ mouse appearing as homogeneous segmental bundles, each consisting of an “undifferentiated” mass of muscle fibers. Muscle fibers serially attach to the caudal tip of the lumbar spinal process, passing caudolaterally to insert into the mamillary process of the fourth vertebra caudad and into sites located on all vertebrae in between. Investigations showed that there was one MEP per individual muscle fiber, located approximately half way along each fiber. The many differences in nomenclature encountered while researching the TSP muscles makes interspecies comparisons difficult, and thus hinders our understanding of these muscles. Furthermore, existing descriptions of individual TSP muscles do not fit well with the framework used to classify skeletal muscles, therefore highlighting why current definitions and nomenclature involving the TSP muscles should be revisited. These results facilitate an understanding of the morphogenesis of epaxial muscles in the mouse and other animals and provide a useful comparison for refining our understanding of the development and function of paravertebral muscles in larger mammals.