Jesse W. Young

What Is the Shape of Developmental Change

Developmental trajectories provide the empirical foundation for theories about change processes during development. However, the ability to distinguish among alternative trajectories depends on how frequently observations are sampled. This study used real behavioral data, with real patterns of variability, to examine the effects of sampling at different intervals on characterization of the underlying trajectory. Data were derived from a set of 32 infant motor skills indexed daily during the first 18 months. Larger sampling intervals (2-31 days) were simulated by systematically removing observations from the daily data and interpolating over the gaps. Infrequent sampling caused decreasing sensitivity to fluctuations in the daily data: Variable trajectories erroneously appeared as step functions, and estimates of onset ages were increasingly off target. Sensitivity to variation decreased as an inverse power function of sampling interval, resulting in severe degradation of the trajectory with intervals longer than 7 days. These findings suggest that sampling rates typically used by developmental researchers may be inadequate to accurately depict patterns of variability and the shape of developmental change. Inadequate sampling regimes therefore may seriously compromise theories of development.

Ontogeny of long bone geometry in capuchin monkeys (Cebus albifrons and Cebus apella): implications for locomotor development and life history

Studies of a diverse array of animals have found that young individuals often have robust bones for their body size (i.e. augmented cross-sectional dimensions), limiting fracture risk despite general musculoskeletal immaturity. However, previous research has focused primarily on precocial taxa (e.g. rodents, lagomorphs, bovids, goats and emu). In this study, we examined the ontogenetic scaling of humeral and femoral cross-sectional robusticity in a mixed-longitudinal sample of two slow-growing, behaviourally altricial capuchin monkeys. Results showed that, when regressed against biomechanically appropriate size variables (i.e. the product of body mass and bone length), humeral and femoral bending strengths generally scale with negative allometry, matching the scaling patterns observed in previous studies of more precocial mammals. Additionally, bone strength relative to predicted loads (e.g. ‘safety factors’) peaks at birth and rapidly decreases during postnatal growth, falling to less than 5 per cent of peak values by weaning age. We suggest that increased safety factors during early ontogeny may be an adaptation to mitigate injury from falling during initial locomotor efforts. Overall, the results presented here suggest that ontogenetic declines in relative long bone strength may represent a common pattern among mammals that is perhaps preadaptive for different purposes among different lineages.

Anterograde transport blockade precedes deficits in retrograde transport in the visual projection of the DBA/2J mouse model of glaucoma.

Axonal transport deficits have been reported as an early pathology in several neurodegenerative disorders, including glaucoma. However, the progression and mechanisms of these deficits are poorly understood. Previous work suggests that anterograde transport is affected earlier and to a larger degree than retrograde transport, yet this has never been examined directly in vivo. Using combined anterograde and retrograde tract tracing methods, we examined the time-course of anterograde and retrograde transport deficits in the retinofugal projection in pre-glaucomatous (3 month-old) and glaucomatous (9–13 month old) DBA/2J mice. DBA/2J-Gpnmb+ mice were used as a control strain and were shown to have similar retinal ganglion cell densities as C57BL/6J control mice—a strain commonly investigated in the field of vision research. Using cholera toxin-B injections into the eye and FluoroGold injections into the superior colliculus (SC), we were able to measure anterograde and retrograde transport in the primary visual projection. In DBA/2J, anterograde transport from the retina to SC was decreased by 69% in the 9–10 month-old age group, while retrograde transport was only reduced by 23% from levels seen in pre-glaucomatous mice. Despite this minor reduction, retrograde transport remained largely intact in these glaucomatous age groups until 13-months of age. These findings indicate that axonal transport deficits occur in semi-functional axons that are still connected to their brain targets. Structural persistence as determined by presence of estrogen-related receptor beta label in the superficial SC was maintained beyond time-points where reductions in retrograde transport occurred, also supporting that transport deficits may be due to physiological or functional abnormalities as opposed to overt structural loss.

Kinematics of quadrupedal locomotion in sugar gliders (Petaurus breviceps): effects of age and substrate size

SUMMARY Arboreal mammals face unique challenges to locomotor stability. This is particularly true with respect to juveniles, who must navigate substrates similar to those traversed by adults, despite a reduced body size and neuromuscular immaturity. Kinematic differences exhibited by juveniles and adults on a given arboreal substrate could therefore be due to differences in body size relative to substrate size, to differences in neuromuscular development, or to both. We tested the effects of relative body size and age on quadrupedal kinematics in a small arboreal marsupial (the sugar glider, Petaurus breviceps; body mass range of our sample 33-97 g). Juvenile and adult P. breviceps were filmed moving across a flat board and three poles 2.5, 1.0 and 0.5 cm in diameter. Sugar gliders (regardless of age or relative speed) responded to relative decreases in substrate diameter with kinematic adjustments that promote stability; they increased duty factor, increased the average number of supporting limbs during a stride, increased relative stride length and decreased relative stride frequency. Limb phase increased when moving from the flat board to the poles, but not among poles. Compared with adults, juveniles (regardless of relative body size or speed) used lower limb phases, more pronounced limb flexion, and enhanced stability with higher duty factors and a higher average number of supporting limbs during a stride. We conclude that although substrate variation in an arboreal environment presents similar challenges to all individuals, regardless of age or absolute body size, neuromuscular immaturity confers unique problems to growing animals, requiring kinematic compensation.

Quadrupedal Locomotion of Saimiri boliviensis: A Comparison of Field and Laboratory-based Kinematic Data

As a result of a plethora of lab-based studies focusing on primate quadrupedalism, it is well known that compared to most other mammals, primates exhibit distinctive quadrupedal kinematics when moving on artificial “terrestrial” or “arboreal” substrates. However, we have little knowledge of how quadrupedal kinematics are impacted by the complexity of natural habitats, in which pathways may be obstructed, unstable, or vary dramatically in size, orientation, shape, or texture. In this study, we compared data on the quadrupedal kinematics of Saimiri boliviensis in both laboratory and field settings by comparing kinematic responses across laboratory substrates (pole, floor) and natural substrates (branches that varied in size and orientation). Field results indicate that Saimiri boliviensis adjusted to larger branches by increasing limb duty factors, but used a wide variety of gait types (as measured by limb phase) across all branch sizes and orientations, rather than fine tuning limb phase to these aspects of substrate. Lab poles elicited similar average limb phases and duty factors, but reduced gait flexibility compared to branches. Lab studies would benefit from greater complexity of simulated arboreal substrates, and field studies should strive to measure numerous substrate characteristics to most effectively test hypotheses about the adaptive nature of primate locomotion.

Tail growth tracks the ontogeny of prehensile tail use in capuchin monkeys (Cebus albifrons and C. apella).

Physical anthropologists have devoted considerable attention to the structure and function of the primate prehensile tail. Nevertheless, previous morphological studies have concentrated solely on adults, despite behavioral evidence that among many primate taxa, including capuchin monkeys, infants and juveniles use their prehensile tails during a greater number and greater variety of positional behaviors than do adults. In this study, we track caudal vertebral growth in a mixed longitudinal sample of white-fronted and brown capuchin monkeys (Cebus albifrons and Cebus apella). We hypothesized that young capuchins would have relatively robust caudal vertebrae, affording them greater tail strength for more frequent tail-suspension behaviors. Our results supported this hypothesis. Caudal vertebral bending strength (measured as polar section modulus at midshaft) scaled to body mass with negative allometry, while craniocaudal length scaled to body mass with positive allometry, indicating that infant and juvenile capuchin monkeys are characterized by particularly strong caudal vertebrae for their body size. These findings complement previous results showing that long bone strength similarly scales with negative ontogenetic allometry in capuchin monkeys and add to a growing body of literature documenting the synergy between postcranial growth and the changing locomotor demands of maturing animals. Although expanded morphometric data on tail growth and behavioral data on locomotor development are required, the results of this study suggest that the adult capuchin prehensile-tail phenotype may be attributable, at least in part, to selection on juvenile performance, a possibility that deserves further attention.

Human quadrupeds, primate quadrupedalism, and Uner Tan Syndrome.

Since 2005, an extensive literature documents individuals from several families afflicted with “Uner Tan Syndrome (UTS),” a condition that in its most extreme form is characterized by cerebellar hypoplasia, loss of balance and coordination, impaired cognitive abilities, and habitual quadrupedal gait on hands and feet. Some researchers have interpreted habitual use of quadrupedalism by these individuals from an evolutionary perspective, suggesting that it represents an atavistic expression of our quadrupedal primate ancestry or “devolution.” In support of this idea, individuals with “UTS” are said to use diagonal sequence quadrupedalism, a type of quadrupedal gait that distinguishes primates from most other mammals. Although the use of primate-like quadrupedal gait in humans would not be sufficient to support the conclusion of evolutionary “reversal,” no quantitative gait analyses were presented to support this claim. Using standard gait analysis of 518 quadrupedal strides from video sequences of individuals with “UTS”, we found that these humans almost exclusively used lateral sequence–not diagonal sequence–quadrupedal gaits. The quadrupedal gait of these individuals has therefore been erroneously described as primate-like, further weakening the “devolution” hypothesis. In fact, the quadrupedalism exhibited by individuals with UTS resembles that of healthy adult humans asked to walk quadrupedally in an experimental setting. We conclude that quadrupedalism in healthy adults or those with a physical disability can be explained using biomechanical principles rather than evolutionary assumptions.

A novel biomechanical analysis of gait changes in the MPTP mouse model of Parkinson’s disease

Parkinson’s disease (PD) is an age-associated neurodegenerative disorder hallmarked by a loss of mesencephalic dopaminergic neurons. Accurate recapitulation of the PD movement phenotype in animal models of the disease is critical for understanding disease etiology and developing novel therapeutic treatments. However, most existing behavioral assays currently applied to such animal models fail to adequately detect and subsequently quantify the subtle changes associated with the progressive stages of PD. In this study, we used a video-based analysis system to develop and validate a novel protocol for tracking locomotor performance in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) mouse model of PD. We anticipated that (1) treated mice should use slower, shorter, and less frequent strides and (2) that gait deficits should monotonically increase following MPTP administration, as the effects of neurodegeneration become manifest. Video-based biomechanical analyses, utilizing behavioral measures motivated by the comparative biomechanics literature, were used to quantify gait dynamics over a seven-day period following MPTP treatment. Analyses revealed shuffling behaviors consistent with the gait symptoms of advanced PD in humans. Here we also document dramatic gender-based differences in locomotor performance during the progression of the MPTP-induced lesion, despite male and female mice showing similar losses of striatal dopaminergic cells following MPTP administration. Whereas female mice appeared to be protected against gait deficits, males showed multiple changes in gait kinematics, consistent with the loss of locomotor agility and stability. Overall, these data show that the novel video analysis protocol presented here is a robust method capable of detecting subtle changes in gait biomechanics in a mouse model of PD. Our findings indicate that this method is a useful means by which to easily and economically screen preclinical therapeutic compounds for protecting against or reversing neuropathology associated with PD neurodegeneration.

Behavioral implications of ontogenetic changes in intrinsic hand and foot proportions in olive baboons (Papio Anubis)

OBJECTIVES Relatively long digits are considered to enhance grasping performance in primates. We tested whether growth-related changes in intrinsic hand and foot proportions may have behavioral implications for growing animals, by examining whether ontogenetic changes in digital proportions are related to variation in voluntary grasping behaviors in baboons. MATERIALS AND METHODS Longitudinal morphological and behavioral data were collected on 6 captive olive baboons (Papio anubis) as they aged from 5 to 22 months. The length of digits and metapodials, measured from radiographs, were used to calculate phalangeal indices (i.e., PIs: summed length of non-distal phalanges relative to corresponding metapodial length). We also examined the allometric scaling of digital bones relative to body mass. We observed baboon positional behaviors over a 15-day period following the radiographic sessions, quantifying the frequency of forelimb and hindlimb grasping behaviors. RESULTS PIs for all digits declined during growth, a result of the differential scaling of metapodials (which scaled to body mass with isometry) versus phalanges (which scaled with negative allometry). The incidence of forelimb and hindlimb grasping behaviors declined with age. Though we found no relationship between forelimb grasping and hand proportions, the incidence of hindlimb grasping was directly correlated with postaxial digit PIs. DISCUSSION Only changes in the intrinsic proportions of the pedal digits are associated with variation in grasping activity in growing baboons. This finding accords previous biomechanical and neuroanatomical studies showing distinct functional roles for the hands and feet during primate locomotion, and has important implications for reconstructing primate locomotor evolution.

A user's guide for the quantitative analysis of substrate characteristics and locomotor kinematics in free-ranging primates

OBJECTIVES Laboratory studies have yielded important insights into primate locomotor mechanics. Nevertheless, laboratory studies fail to capture the range of ecological and structural variation encountered by free-ranging primates. We present techniques for collecting kinematic data on wild primates using consumer grade high-speed cameras and demonstrate novel methods for quantifying metric variation in arboreal substrates. MATERIALS AND METHODS These methods were developed and applied to our research examining platyrrhine substrate use and locomotion at the Tiputini Biodiversity Station, Ecuador. Modified GoPro cameras equipped with varifocal zoom lenses provided high-resolution footage (1080 p.; 120 fps) suitable for digitizing gait events. We tested two methods for remotely measuring branch diameter: the parallel laser method and the distance meter photogrammetric method. A forestry-grade laser rangefinder was used to quantify substrate angle and a force gauge was used to measure substrate compliance. We also introduce GaitKeeper, a graphical user interface for MATLAB, designed for coding quadrupedal gait. RESULTS Parallel laser and distance meter methods provided accurate estimations of substrate diameter (percent error: 3.1-4.5%). The laser rangefinder yielded accurate estimations of substrate orientation (mean error = 2.5°). Compliance values varied tremendously among substrates but were largely explained by substrate diameter, substrate length, and distance of measurement point from trunk. On average, larger primates used relatively small substrates and traveled higher in the canopy. DISCUSSION Ultimately, these methods will help researchers identify more precisely how primate gait kinematics respond to the complexity of arboreal habitats, furthering our understanding of the adaptive context in which primate quadrupedalism evolved.