Trabecular bone patterning across the human hand

Abstract

Hand bone morphology is regularly used to link particular hominin species with behaviors relevant to cognitive/technological progress. Debates about the functional significance of differing hominin hand bone morphologies tend to rely on establishing phylogenetic relationships and/or inferring behavior from epigenetic variation arising from mechanical loading and adaptive bone modeling. Most research focuses on variation in cortical bone structure, but additional information about hand function may be provided through the analysis of internal trabecular structure. While primate hand bone trabecular structure is known to vary in ways that are consistent with expected joint loading differences during manipulation and locomotion, no study exists that has documented this variation across the numerous bones of the hand. We quantify the trabecular structure in 22 bones of the human hand (early/extant modern Homo sapiens) and compare structural variation between two groups associated with post-agricultural/industrial (post-Neolithic) and foraging/hunter-gatherer (forager) subsistence strategies. We (1) establish trabecular bone volume fraction (BV/TV), modulus (E), degree of anisotropy (DA), mean trabecular thickness (Tb.Th) and spacing (Tb.Sp); (2) visualize the average distribution of site-specific BV/TV for each bone; and (3) examine if the variation in trabecular structure is consistent with expected joint loading differences among the regions of the hand and between the groups. Results indicate similar distributions of trabecular bone in both groups, with those of the forager sample presenting higher BV/TV, E, and lower DA, suggesting greater and more variable loading during manipulation. We find indications of higher loading along the ulnar side of the forager sample hand, with high site-specific BV/TV distributions among the carpals that are suggestive of high loading while the wrist moves through the 'dart-thrower's' motion. These results support the use of trabecular structure to infer behavior and have direct implications for refining our understanding of human hand evolution and fossil hominin hand use.

Trabecular variation in the first metacarpal and manipulation in hominids

“…In contrast to these RBV/TV results, high DA throughout the human Mc1 head, while not overall significantly different from any species except gorillas, does not match our prediction of the highest DA at radiopalmar landmarks ( H1c ). Stephens et al () found slightly lower average DA values in a similar human Mc1 sample, likely due to their sampling of the whole distal epiphysis, but also found little regional differentiation across the Mc1 head in agreement with the results here. The present result may reflect the higher frequency of forceful prehensile thumb use in humans than in other extant hominids.…”

“…Therefore, we predict flexion will be the dominant habitual movement in these grips, rather than adduction, reflected by the trabecular distribution in the nonhuman primate TMc joint (Figure b, bottom). In humans we predict RBV/TV and DA will be greater in the radiopalmar aspect of the Mc1 base ( H2c ; Figure a), due to habitual abduction and flexion during precision grasping (D'Agostino, Dourthe, Kerkhof, Stockmans, et al, ; Feix et al, ; Napier, ) as has been demonstrated before for RBV/TV (Stephens et al, ).…”

“…Humans displayed both significantly higher RBV/TV at radial landmarks and higher DA throughout the subarticular Mc1 head than in other great apes ( H1c ). A radiopalmar concentration has also been found in a similar sample of humans, using a method that analyzed absolute BV/TV in the whole distal epiphysis of the Mc1 rather than just the subarticular region (Stephens et al, ). Further, a significantly larger radial palmar epicondyle in the human Mc1 head, relative to other great apes, may also indicate the importance of this region of the Mc1 head to human manipulation (Galletta et al, ).…”

“…Indeed the region of the trapeziometacarpal (TMc) joint in which osteoarthritis first develops, thought to therefore endure the most substantial habitual load (Koff et al, ), is also the area in which trabecular bone is densest on the Mc1 (Stephens, Kivell, Pahr, Hublin, & Skinner, ). Preserved trabeculae in fossil hominins have been used to infer habitual loading and reconstruct locomotor (e.g., Barak, Lieberman, Raichlen, et al, ; DeSilva & Devlin, ; Ryan et al, ; Su, Wallace, & Nakatsukasa, ; Zeininger, Patel, Zipfel, & Carlson, ) and manipulative (e.g., Skinner et al, , ; Stephens et al, ) behaviors during human evolution. These functional inferences are based on the comparative context of extant great apes and an association between variation in their trabecular architecture and assumptions about the joint postures they most commonly use (Orr, ).…”

“…Specifically, the human Mc1 base has a greater concentration of trabecular bone in its palmar aspect relative to human nonpollical metacarpals (Wong, Meals, & Ruff, ) and the Mc1 of Pan (Skinner et al, , ). Where Skinner et al (, ) inferred function by qualitatively analyzing three‐dimensional (3D) trabecular models, Stephens et al () quantitatively analyzed an expanded sample of foragers and post‐Neolithic humans and found that BV/TV was greatest in the radiopalmar segments of the Mc1 head and base, consistent with a flexed, abducted thumb in precision grips. This study also found that DA was lower in the Mc1 base of foragers relative to a sample of post‐Neolithic humans, and related this to more varied loading at this, and other manual, joints in the forager population (Stephens et al, ).…”