Patterns of strain in the macaque tibia during functional activity.

The strain environment of the tibial midshaft of two female macaques was evaluated through in vivo bone strain experiments using three rosette gauges around the circumference of the bones. Strains were collected for a total of 123 walking and galloping steps as well as several climbing cycles. Principal strains and the angle of the maximum (tensile) principal strain with the long axis of the bone were calculated for each gauge site. In addition, the normal strain distribution throughout the cross section was determined from the longitudinal normal strains (strains in the direction of the long axis of the bone) at each of the three gauge sites, and at the corresponding cross-sectional geometry of the bone. This strain distribution was compared with the cross-sectional properties (area moments) of the midshaft. For both animals, the predominant loading regime was found to be bending about an oblique axis running from anterolateral to posteromedial. The anterior and part of the medial cortex are in tension; the posterior and part of the lateral cortex are in compression. The axis of bending does not coincide with the maximum principal axis of the cross section, which runs mediolaterally. The bones are not especially buttressed in the plane of bending, but offer the greatest strength anteroposteriorly. The cross-sectional geometry therefore does not minimize strain or bone tissue. Peak tibial strains are slightly higher than the peak ulnar strains reported earlier for the same animals (Demes et al. [1998] Am J Phys Anthropol 106:87-100). Peak strains for both the tibia and the ulna are moderate in comparison to strains recorded during walking and galloping activities in nonprimate mammals.     

Mandibular corpus strain in primates: Further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force

Previous work indicates that compared to adult thick-tailed galagos, adult long-tailed macaques have much more bone strain on the balancing-side mandibular corpus during unilateral isometric molar biting (Hylander [1979a] J. Morphol. 159:253–296). Recently we have confirmed in these same two species the presence of similar differences in bone-strain patterns during forceful mastication. Moreover, we have also recorded mandibular bone strain patterns in adult owl monkeys, which are slightly smaller than the galago subjects. The owl monkey data indicate the presence of a strain pattern very similar to that recorded for macaques, and quite unlike that recorded for galagos. We interpret these bone-strain pattern differences to be importantly related to differences in balancing-side jaw-adductor muscle force recruitment patterns. That is, compared to galagos, macaques and owl monkeys recruit relatively more balancing-side jaw-adductor muscle force during forceful mastication. Unlike an earlier study (Hylander [1979b] J. Morphol. 160:223–240), we are unable to estimate the actual amount of working-side muscle force relative to balancing-side muscle force (i.e., the W/ B muscle force ratio) in these species because we have no reliable estimate of magnitude, direction, and precise location of the bite force during mastication. A comparison of the mastication data with the earlier data recorded during isometric molar biting, however, supports the hypothesis that the two anthropoids have a small W/ B jaw-adductor muscle force ratio in comparison to thick-tailed galagos. These data also support the hypothesis that increased recruitment of balancing-side jaw-adductor muscle force in anthropoids is functionally linked to the evolution of symphyseal fusion or strengthening. Moreover, these data refute the hypothesis that the recruitment pattern differences between macaques and thick-tailed galagos are due to allometric factors. Finally, although the evolution of symphyseal fusion in primates may be linked to increased stress associated with increased balancing-side muscle force, it is currently unclear as to whether the increased force is predominately vertically directed, transversely directed, or is a near equal combination of these two force components (cf. Ravosa and Hylander [1994] In Fleagle and Kay [eds.]: Anthropoid Origins. New York: Plenum, pp. 447–468). Am J Phys Anthropol 107:257-271, 1998. © 1998 Wiley-Liss, Inc.     

Identification of primitive hematopoietic progenitor cells in the rhesus macaque

The close phylogenetic relationship of macaques to humans has resulted in their widespread use as a preclinical model for bone marrow transplantation and stem cell gene therapy. To facilitate further use of this model, we undertook analysis of hematopoietic cells using multiparametric flow cytometric analysis. Rhesus CD34+CD38- cells displayed a number of characteristics of primitive hematopoietic cells, including low forward and orthogonal scatter and the lack of expression of lineage-specific markers or human lymphocyte antigen-DR. Four-color flow cytometric analysis demonstrated that rhesus CD34+CD38- cells were heterogenous with respect to Thy-1 expression and were CD59dim. Quantitative limiting dilution long-term culture-initiating cell (LTC-IC) analysis demonstrated that CD34+CD38- cells were approximately 150-fold enriched for LTC-IC as compared with unfractionated bone marrow, and occurred at a frequency similar to that previously reported in humans. Thus, as in humans, the CD34+38- population of rhesus macaque bone marrow is enriched for primitive, multipotent hematopoietic progenitor cells.     

Textural characteristics of the iliac-femoral trabecular pattern in a bipedally trained Japanese macaque

Previous research has revealed that Japanese macaques (Macaca fuscata) trained in bipedal performance (Saru-mawashi) display a number of functionally related external skeletal changes, as well as some site-specific endostructural cortical and cancellous adaptations. Through radiography assisted by digital image processing, we investigated the trabecular pattern of the ilium and femoral neck of Sansuke, a macaque habitually bipedally trained for 8 years. A set of eight regions of interest on Sansuke were recorded for subtle structural characterization of the cancellous network and compared to a sample of 5 ilia and 23 femurs from 26 adult wild Japanese macaques. The measured variables include trabecular thickness, trabecular bone volume, and degree of anisotropy. As a whole, the site-specific textural characteristics of the cancellous network detected on the ilium and proximal femur of the bipedally trained macaque can be interpreted as functional adaptive responses to more compressive loads dissipated along the axis from the sacro-iliac to the coxo-femoral joint, and back.     

Bone strain magnitude is correlated with bone strain rate in tetrapods: implications for models of mechanotransduction

Hypotheses suggest that structural integrity of vertebrate bones is maintained by controlling bone strain magnitude via adaptive modelling in response to mechanical stimuli. Increased tissue-level strain magnitude and rate have both been identified as potent stimuli leading to increased bone formation. Mechanotransduction models hypothesize that osteocytes sense bone deformation by detecting fluid flow-induced drag in the bone''s lacunar–canalicular porosity. This model suggests that the osteocyte''s intracellular response depends on fluid-flow rate, a product of bone strain rate and gradient, but does not provide a mechanism for detection of strain magnitude. Such a mechanism is necessary for bone modelling to adapt to loads, because strain magnitude is an important determinant of skeletal fracture. Using strain gauge data from the limb bones of amphibians, reptiles, birds and mammals, we identified strong correlations between strain rate and magnitude across clades employing diverse locomotor styles and degrees of rhythmicity. The breadth of our sample suggests that this pattern is likely to be a common feature of tetrapod bone loading. Moreover, finding that bone strain magnitude is encoded in strain rate at the tissue level is consistent with the hypothesis that it might be encoded in fluid-flow rate at the cellular level, facilitating bone adaptation via mechanotransduction.     

Time budget and activity patterns of the lion-tailed macaque (Macaca silenus)

We studied time budgeting of lion-tailed macaques in the Anamalai Wildlife Sanctuary, Tamil Nadu, India, with regard to seven activity categories. Groups spent >50% of their time feeding and foraging, 33% of the time resting, and 15% moving. More energetic activities were spread uniformly through the day. Feeding had two annual peaks: one closely following the northeast monsoon and the other corresponding to the southwest monsoon. These also coincided with peaks of food availability and mating. Time saved in feeding was spent mostly on resting. Ranging showed a pattern contrary to that of time spent moving and was related more to weather than to food availability; it increased during cooler periods. The middle and upper stories of the canopy were used >93% of the time. The ground was used rarely. Time budgeting characteristics of the lion-tailed macaque are primarily frugiinsectivorous adaptations to a wet evergreen forest habitat.     

Predicting long bone loading from cross-sectional geometry

Long bone loading histories are commonly evaluated using a beam model by calculating cross-sectional second moments of areas (SMAs). Without in vivo strain data, SMA analyses commonly make two explicit or implicit assumptions. First, while it has long been known that axial compression superimposed on bending shifts neutral axes away from cross-sectional area centroids, most analyses assume that cross-sectional properties calculated through the area centroid approximate cross-sectional strength. Second, the orientation of maximum bending rigidity is often assumed to reflect the orientation of peak or habitual bending forces the bone experiences. These assumptions are tested in sheep in which rosette strain gauges mounted at three locations around the tibia and metatarsal midshafts measured in vivo strains during treadmill running at 1.5 m/sec. Calculated normal strain distributions confirm that the neutral axis of bending does not run through the midshaft centroid. In these animals, orientations of the principal centroidal axes around which maximum SMAs (Imax) are calculated are not in the same planes in which the bones experienced bending. Cross-sectional properties calculated using centroidal axes have substantial differences in magnitude (up to 55%) but high correlations in pattern compared to cross-sectional properties calculated around experimentally determined neutral axes. Thus interindividual comparisons of cross-sectional properties calculated from centroidal axes may be useful in terms of pattern, but are subject to high errors in terms of absolute values. In addition, cross-sectional properties do not necessarily provide reliable data on the orientations of loads to which bones are subjected.     

The instantaneous center of rotation during human jaw opening and its significance in interpreting the functional meaning of condylar translation

Mandibular condyles translate back and forth during mouth closing and opening in primates and most other mammals. To account for the functional significance of this phenomenon, several hypotheses have been proposed. The sarcomere-length hypothesis holds that condylar translation provides a mechanical advantage by minimizing sarcomere-length changes in the masseter-medial pterygoid complex throughout a wide range of jaw openings. As the hypothesis is inherently associated with the locations of the instantaneous centers of rotation (ICRs) of the mandible, a more accurate determination of this variable would help test this hypothesis. This study investigated ICRs in the sagittal plane during human symmetrical mandibular opening based on a recently developed analytical method. The results confirmed that, with inter- and intraindividual variation, the natural opening was a simultaneous rotational and translational motion. In addition, the ICR was found to lie closer to the condyle during the first 10° than during the rest of the rotation. This suggests that for the condyles the rotational component is somewhat more significant at the early phase than at the late phase of the opening stroke. For the whole range of the natural opening, the grossly approximated centers of rotation (CRs) scattered below the palpable lateral condylar poles in the superior half of the ramus. This study supports neither the ICR path determined by Grant ([1973], J. Biomech. 6:109–113) nor the conclusions reached by recording manually operated jaw movements in human cadavers (Rees [1954] Br. Dent. J. 6:125–133). Moss's suggestion ([1960] Disorders of the Temporomandibular Joint (Philadelphia: W.B. Saunders), pp. 73–88) that the center of rotation lies at the lingula is also not confirmed. Although the new data cannot reject the sarcomere-length hypothesis, they do not strongly support it either. Another hypothesis is proposed in this study as plausible. With this hypothesis, translation is regarded as an adaptation to the use of the inferior head of the lateral pterygoid as a jaw depressor in noncarnivorous mammals. Potential functional advantages of this portion of the muscle are also discussed. Am J Phys Anthropol 106:35–46, 1998. © 1998 Wiley-Liss, Inc.     

Efficiency of coding in macaque vocal communication

A key characteristic of human language efficiency is that more frequently used words tend to be shorter in length—the ‘law of brevity’. To date, no test of this relationship between frequency of use and length has been carried out on non-human animal vocal communication. We show here that the vocal repertoire of the Formosan macaque (Macaca cyclopis) conforms to the pattern predicted by the law of brevity, with an inverse relationship found between call duration and rate of utterance. This finding provides evidence for coding efficiency in the vocal communication system of this species, and indicates commonality in the basic structure of the coding system between human language and vocal communication in this non-human primate.     

猕猴发育过程中肠肝组织生长抑素及其受体表达演变规律

探讨在猕猴发育过程中生长抑素(somatostatin,SST)及其受体在肠肝组织的演变规律。通过手术途径获得胚胎6月、新生2 d、新生45 d和成年猕猴的回肠、肝脏、门静脉和外周血等标本。应用放射免疫分析法测定各标本中的SST含量; 通过免疫组化方法观察SST在肠、肝组织内的分布;利用原位杂交检测SST受体2(somatostatin receptor 2,SSTR2)的表达。结果显示:(1)胚胎6月的猕猴,小肠内SST含量为(27．3±16．6)ng／mg蛋白;黏膜隐窝处SST呈弱阳性染色,肌层 SST染色阴性。在发育过程中,小肠内SST含量逐渐增加,成年期时达最高水平(120．1±35．3)ng／mg蛋白,较胚胎6月显著增加(P<0．01)。(2)成年小肠黏膜隐窝处及肌间神经丛SST呈强阳性染色。(3)胚胎6月,小肠粘膜上皮可见大量SSTR2 表达,成年时SSTR2表达下调,且主要定位于腺上皮隐窝处;胚胎及新生期肌层SSTR2染色阴性,成年时小肠肌间神经丛则可见阳性SSTR2染色。(4)肝脏在发育过程中SST及SSTR2含量逐渐降低;发育的各个时期,小肠组织的SST含量均明显高于肝脏组织含量,门静脉SST水平也始终高于外周血。总之,位于小肠黏膜隐窝处的SST和SSTR2随着发育逐渐增加,来自肠道的SST进入门静脉后迅速被降解。SST阳性的肠肌间神经丛仅在发育成熟后才出现。     

Endocytosis in spermatids during spermiogenesis of the mouse

In the course of spermiogenesis in the mouse, spermatid cytoplasm contains numerous membrane pits, vesicles and membranous tubules which are frequently anastomosed. Pale and dense multivesicular bodies (MVB) and secondary lysosome-like structures are also present in the cytoplasm. In order to study the pathway of non-specific adsorptive endocytosis in spermatids, cationic ferritin (CF) was directly microinjected into the lumen of seminiferous tubules, and added to germinal cell culture. Tissue and cultures were fixed at various time intervals after injection. Two-5 hr after microinjection of tracer, CF was found simultaneously in vesicles, tubules, MVB and in lysosome-like bodies present in spermatids at all steps of spermiogenesis. Various membranous components of the Golgi medulla, and the innermost transsaccule of the Golgi cortex were labelled simultaneously. In primary cultures of spermatids, the vesicles contained the marker 5 min after its deposition; 10 min after deposition, CF was evident in tubules; at 30 min, CF was present in pale MVB; at 1 hr, the dense MVB and lysosome-like bodies were labelled. Finally, at 2 hr 30 min, vesicles and tubules of the Golgi medulla contained CF grains. Apparently spermatids are very active cells in the process of adsorptive endocytosis throughout spermiogenesis. Endocytosis in spermatids is probably one of the mechanisms involved in the uptake of material used to build up spermatozoa components. The strong labelling of the Golgi region probably point to its role in recycling endocytosed membranes.     

Postthaw survival of rhesus macaque sperm: variation in the response of individual males to different freezing protocols

This study was designed to assess the effects of various cryopreservation protocols on the postthaw survival of rhesus macaque sperm. Multiple ejaculates of five mature males were collected and frozen by each of four different methods. Cryopreservation significantly reduced motility in all samples, regardless of the method, and the response of different ejaculates of the same male to each method proved to be consistent. The freezing method was a significant factor in determining the immediate postthaw motility, although this effect disappeared after 4 hr. Moreover, there was a significant interaction between individual males and freezing method suggesting that developing a single freezing protocol that is universally suitable may be difficult.