Functional correlates of lemur masticatory muscle fiber architecture visualized in 3D using DiceCT

Abstract

The functional morphology of primate masticatory musculature has been the subject of many studies. However, with the exception of analyses of four taxa, these have always described this anatomy using traditional, destructive, gross anatomical dissections. In the current study, we use diffusible iodine‐based contrast‐enhanced computed tomography (DiceCT), in which specimens are stained with Lugol’s iodine that binds to the glycogen in muscle fibers to increase their radio‐opacity to the point of being able to discriminate between fascicles using x‐ray‐based imagery, to examine the masticatory muscle fiber architecture of nine strepsirrhine species across four genera of lemurid and Propithecus, Daubentonia and Otolemur. Not only do we report data on the traditional architectural variables of muscle volume, fascicle length (FL), physiological cross‐sectional area (PCSA), but also on variables unattainable except through three‐dimensional visualization: fascicular curvature and 3D orientation. The breadth of this sample more than triples the number of primates for which DiceCT has been applied to questions of fascicular architecture, allowing, for the first time, functional interpretation using this non‐destructive visualization technique. We have confirmed that this approach yields similar FL and PCSA measurements compared to those collected using destructive dissection. Further, this approach allows findings unavailable without this three‐dimensional visualization. Namely, fascicle angularity seems to relate to gouging – Daubentonia fascicles clearly align with its anteroposterior jaw motions. Further, fascicular compression seems relate to diet, with the most folivorous taxon in our sample, Propithecus, having 7% lower fascicular compression at near occlusion than that of Varecia, our most frugivorous taxon which has the highest arc:chord ratio (1.16) in the sample. While the scanning and subsequent “digital dissection” of the fascicles costs more time and money than does architectural data collection using traditional gross dissection, these expenses are coming down as scanners are becoming better and cheaper and digital tools (including improved selection algorithms) will allow faster fascicular analysis. Most importantly, these techniques not only yield data non‐destructively (allowing the study of specimens too precious to physically dissect), but they also preserve important three‐dimensional spatial relationships previously unavailable. This allows for the first analyses of true in situ fascicular orientation which is important for understanding naturalistic force vectors – a feature that may have important benefits for more accurate computer modeling of this complicated system – and fascicular compression – a feature with implications for understanding variable muscle activation during the chewing cycle – something previously only ever attainable with invasive live animal experimentation.