Histology and 3D Modeling of the Connective Tissue Skeleton in the Trunk of a Lamprey (Petromyzon marinus)

Abstract

Agnathan lampreys play a key role in the reconstruction of the evolutionary history of vertebrates and, more specifically, in the analysis of the biomechanics underlying piscine undulatory locomotion. However, the morphology of the fibrous skeletal framework for their trunk musculature is still incompletely understood, mainly because of the complex spatial configuration of the segmentally arranged myosepta and muscle fibers within the myomeres. To contribute to a better understanding of how contractile muscular forces are transmitted via the fibrous skeletal framework of the trunk, the architecture and composition of the connective tissue structures (dermis, dorsal longitudinal ligament, hypodermis, myosepta, perimysial lamellae, notochord, fasciae) and their relationship to the muscle fibers of the myomeres were analyzed through histological techniques (in addition to MRI and microdissection described elsewhere) and 3D modeling based on a 3D reconstruction of serial histological sections treated with special stains (e.g., Movat Pentachrome, Ladewig Trichrome). These stains, however, did not differentiate tissue types as expected, probably because lamprey tissue fiber types differ biochemically from mammalian ones, but they discriminate a wide range of fiber types. As to the distribution of connective tissue fibers, the dermis comprises about 25 layers of helically arranged collagen fibers with the most superficial layers anchoring to the basement membrane of the epidermis and the deepest layers connecting to fibers of the hypodermis, which is separated by the pigment layer from the dermis. Radially arranged collagen fibers interconnect the basement membrane and hypodermis. Also within the hypodermis, the dorsal longitudinal ligament collects and interbraids collagen fibers from the dermis, hypodermis, and dorsal vertical septum, and, ultimately, the myosepta. The latter comprise tendon fibers connecting the roughly longitudinally oriented muscle fibers of adjacent myomeres and are traversed by thick collagen fiber bundles that run from the dermis to the central periaxial and perivisceral fasciae, as well as by thin reticulated fibers that support intramyoseptal nerves and blood vessels. The muscle blocks of the myomeres are separated by radially arranged perimysial lamellae running from the hypodermis to the periaxial and perivisceral fasciae. During undulations, contracting muscle fibers between the myosepta shorten and expand radially. This expansion is resisted by the radially arranged collagen fibers within the myosepta and perimysial lamellae. As a result, the internal pressure and, hence, the turgidity of the trunk is raised. A detailed understanding of the connective tissue fiber configuration in lampreys provides the necessary basis for building dynamic 3D models of the biomechanics involved in locomotion and other behaviors.Support or Funding InformationGrant‐In‐Aid of Research from Sigma Xi, the Scientific Research Society, to Bradley M. Wood; LSU Foundation support to Dominique G. HombergerThis abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.