Talar trochlear morphology may not be a good skeletal indicator of locomotor behavior in humans and great apes

To reconstruct locomotor behaviors of fossil hominins and understand the evolution of bipedal locomotion in the human lineage, it is important to clarify the functional morphology of the talar trochlea in humans and extant great apes. Therefore, the present study aimed to investigate the interspecific-differences of the talar trochlear morphology among humans, chimpanzees, gorillas, and orangutans by means of cone frustum approximation to calculate an apical angle and geometric morphometrics for detailed variability in the shape of the talar trochlea. The apical angles in gorillas and orangutans were significantly greater than those in humans and chimpanzees, but no statistical difference was observed between humans and chimpanzees, indicating that the apical angle did not necessarily correspond with the degree of arboreality in hominoids. The geometric morphometrics revealed clear interspecific differences in the trochlear morphology, but no clear association between the morphological characteristics of the trochlea and locomotor behavior was observed. The morphology of the trochlea may not be a distinct skeletal correlate of locomotor behavior, possibly because the morphology is determined not only by locomotor behavior, but also by other factors such as phylogeny and body size.

Convergence of undulatory swimming kinematics across a diversity of fishes

Fishes exhibit an astounding diversity of locomotor behaviors from classic swimming with their body and fins to jumping, flying, walking, and burrowing. Fishes that use their body and caudal fin (BCF) during undulatory swimming have been traditionally divided into modes based on the length of the propulsive body wave and the ratio of head:tail oscillation amplitude: anguilliform, subcarangiform, carangiform, and thunniform. This classification was first proposed based on key morphological traits, such as body stiffness and elongation, to group fishes based on their expected swimming mechanics. Here, we present a comparative study of 44 diverse species quantifying the kinematics and morphology of BCF-swimming fishes. Our results reveal that most species we studied share similar oscillation amplitude during steady locomotion that can be modeled using a second-degree order polynomial. The length of the propulsive body wave was shorter for species classified as anguilliform and longer for those classified as thunniform, although substantial variability existed both within and among species. Moreover, there was no decrease in head:tail amplitude from the anguilliform to thunniform mode of locomotion as we expected from the traditional classification. While the expected swimming modes correlated with morphological traits, they did not accurately represent the kinematics of BCF locomotion. These results indicate that even fish species differing as substantially in morphology as tuna and eel exhibit statistically similar two-dimensional midline kinematics and point toward unifying locomotor hydrodynamic mechanisms that can serve as the basis for understanding aquatic locomotion and controlling biomimetic aquatic robots.

Comprehensive analysis of behavioral dynamics in the protochordate Ciona intestinalis

Locomotion is broadly conserved in the animal kingdom, yet our understanding of how complex locomotor behaviors are generated and have evolved is relatively limited by the lack of an accurate description of their structural organization. Here we take a neuroethological approach to break down the motor behavioral repertoire of one of our nearest invertebrate relative, the protochordate Ciona intestinalis, into basic building blocks. Using machine vision, we track thousands of swimming larvae to obtain a feature-rich description of larval swimming and show that most of the postural variance can be captured by six basic shapes, which we term Eigencionas. Using multiple complementary approaches, we built representations of the larval behavioral dynamics and systematically reveal the global structure of behavior. By employing matrix profiling and subsequence time-series clustering, we reveal that Ciona swimming is rich in stereotyped behavioral motifs. Combining pharmacological inhibition of bioamine signaling with Hidden Markov Model we discover underlying behavioral states including multiple modes of roaming and dwelling. Finally, performing a spatio-temporal embedding of the postural features onto a behavioral space provides insight into the behavioral repertoire by project it to a low-dimensional space and highlights subtle light stimulus evoked behavioral differences. Taken together, Ciona larvae generate their spontaneous swimming and visuomotor behavioral repertoire by altering both their motor modules and transitions between, which are amenable to pharmacological perturbations, facilitating future functional and mechanistic investigations.

Motor control in the epaxial musculature of bluegill sunfish in feeding and locomotion

ABSTRACT Fishes possess an impressive repertoire of feeding and locomotor behaviors that in many cases rely on the same power source: the axial musculature. As both functions employ different skeletal systems, head versus body, integrating these functions would likely require modular motor control. Although there have been many studies of motor control in feeding or locomotion in fishes, only one study to date has examined both functions in the same individuals. To characterize bilateral motor control of the epaxial musculature in feeding and locomotion, we measured muscle activity and shortening in bluegill sunfish (Lepomis macrochirus) using electromyography and sonomicrometry. We found that sunfish recruit epaxial regions in a dorsal-to-ventral manner to increase feeding performance, such that high-performance feeding activates all the epaxial musculature. In comparison, sunfish seemed to activate all three epaxial regions irrespective of locomotor performance. Muscle activity was present on both sides of the body in nearly all feeding and locomotor behaviors. Feeding behaviors used similar activation intensities on the two sides of the body, whereas locomotor behaviors consistently used higher intensities on the side undergoing muscle shortening. In all epaxial regions, fast-starts used the highest activation intensities, although high-performance suction feeding occasionally showed near-maximal intensity. Finally, active muscle volume was positively correlated with the peak rate of body flexion in feeding and locomotion, indicating a continuous relationship between recruitment and performance. A comparison of these results with recent work on largemouth bass (Micropterus salmoides) suggests that centrarchid fishes use similar motor control strategies for feeding, but interspecific differences in peak suction-feeding performance are determined by active muscle volume.

Genetic modeling of GNAO1 disorder delineates mechanisms of Gαo dysfunction

GNAO1 encephalopathy is a neurodevelopmental disorder with a spectrum of symptoms that include dystonic movements, seizures and developmental delay. While numerous GNAO1 mutations are associated with this disorder, the functional consequences of pathological variants are not completely understood. Here, we deployed the invertebrate C. elegans as a whole-animal behavioral model to study the functional effects of GNAO1 disorder-associated mutations. We tested several pathological GNAO1 mutations for effects on locomotor behaviors using a combination of CRISPR/Cas9 gene editing and transgenic overexpression in vivo. We report that all three mutations tested (G42R, G203R and R209C) result in strong loss of function defects when evaluated as homozygous CRISPR alleles. In addition, mutations produced dominant negative effects assessed using both heterozygous CRISPR alleles and transgenic overexpression. Experiments in mice confirmed dominant negative effects of GNAO1 G42R, which impaired numerous motor behaviors. Thus, GNAO1 pathological mutations result in conserved functional outcomes across animal models. Our study further establishes the molecular genetic basis of GNAO1 encephalopathy, and develops a CRISPR-based pipeline for functionally evaluating mutations associated with neurodevelopmental disorders.

A terrain treadmill to study small animal locomotion through large obstacles

A major challenge to understanding locomotion in complex 3-D terrain with large obstacles is to create tools for controlled, systematic lab experiments. Existing terrain arenas only allow observations at small spatiotemporal scales (~10 body length, ~10 stride cycles). Here, we create a terrain treadmill to enable high-resolution observations of small animal locomotion through large obstacles over large spatiotemporal scales. An animal moves through modular obstacles on an inner sphere, while a rigidly-attached, concentric, transparent outer sphere rotated with the opposite velocity via closed-loop feedback to keep the animal on top. During sustained locomotion, a discoid cockroach moved through pillar obstacles for 25 minutes (≈ 2500 strides) over 67 m (≈ 1500 body lengths), and was contained within a radius of 4 cm (0.9 body length) for 83% of the duration, even at speeds of up to 10 body length/s. The treadmill enabled observation of diverse locomotor behaviors and quantification of animal-obstacle interaction.

Frequency modulation of body waves to improve performance of sidewinding robots

Sidewinding is a form of locomotion executed by certain snakes and has been reconstructed in limbless robots; the gait is beneficial because it is effective in diverse terrestrial environments. Sidewinding gaits are generated by coordination of horizontal and vertical traveling waves of body undulation: the horizontal wave largely sets the direction of sidewinding with respect to the body frame while the vertical traveling wave largely determines the contact pattern between the body and the environment. When the locomotor’s center of mass leaves the supporting polygon formed by the contact pattern, undesirable locomotor behaviors (such as unwanted turning or unstable oscillation of the body) can occur. In this article, we develop an approach to generate desired translation and turning by modulating the vertical wave. These modulations alter the distribution of body–environment contact patches and can stabilize configurations that were previously statically unstable. The approach first identifies the spatial frequency of the vertical wave that statically stabilizes the locomotor for a given horizontal wave. Then, using geometric mechanics tools, we design the coordination between body waves that produces the desired translation or rotation. We demonstrate the effectiveness of our technique in numerical simulations and on experiments with a 16-joint limbless robot locomoting on flat hard ground. Our scheme broadens the range of movements and behaviors accessible to sidewinding locomotors at low speeds, which can lead to limbless systems capable of traversing diverse terrain stably and/or rapidly.

Architectural properties of the musculoskeletal system in the shoulder of two callitrichid primate species derived from virtual dissection

Callitrichidae are small, arboreal New World primates that utilize a variety of locomotor behaviors including trunk-to-trunk leaping (TTL) and horizontal locomotion which involve differential functional demands. Little is known about the relationship between the preferred locomotor behavior and musculoskeletal architecture of these primates. In this study, we compared the musculoskeletal architecture of selected shoulder muscles in two cadavers each of the trunk-to-trunk leaper Cebuella pygmaea and the mainly pronograde quadrupedally moving Saguinus imperator subgrisescens. Contrast-enhanced microfocus computed tomography (µCT) was used to virtually dissect the cadavers, produce muscle maps, and create 3D reconstructions for an image-based analysis of the muscles. Muscle lengths, muscle volumes, and osteological muscle moment arms were measured, and the anatomical cross-sectional areas (ACSA) were calculated. We expected the muscles of the forelimb of S. imperator to be larger in volume and to be relatively shorter with a larger ACSA due to a higher demand for powerful extension in the forelimbs of this horizontally locomoting species. For C. pygmaea, we expected relatively larger moment arms for the triceps brachii, supraspinatus, infraspinatus and subscapularis, as larger moment arms present an advantage for extensive vertical clinging on the trunk. The muscles of S. imperator were relatively larger in volume than in C. pygmaea and had a relatively larger ACSA. Thus, the shoulder muscles of S. imperator were suited to generate relatively larger forces than those of C. pygmaea. Contrary to our expectations, there were only slight differences between species in regard to muscle lengths and moment arms, which suggests that these properties are not dependent on the preferred locomotor mode. The study of this limited dataset demonstrates that some but not all properties of the musculoskeletal architecture reflect the preferred locomotor behavior in the two species of Callitrichidae examined.

Metabolic control of daily locomotor activity mediated by tachykinin in Drosophila

Metabolism influences locomotor behaviors, but the understanding of neural curcuit control for that is limited. Under standard light-dark cycles, Drosophila exhibits bimodal morning (M) and evening (E) locomotor activities that are controlled by clock neurons. Here, we showed that a high-nutrient diet progressively extended M activity but not E activity. Drosophila tachykinin (DTk) and Tachykinin-like receptor at 86C (TkR86C)-mediated signaling was required for the extension of M activity. DTk neurons were anatomically and functionally connected to the posterior dorsal neuron 1s (DN1ps) in the clock neuronal network. The activation of DTk neurons reduced intracellular Ca2+ levels in DN1ps suggesting an inhibitory connection. The contacts between DN1ps and DTk neurons increased gradually over time in flies fed a high-sucrose diet, consistent with the locomotor behavior. DN1ps have been implicated in integrating environmental sensory inputs (e.g., light and temperature) to control daily locomotor behavior. This study revealed that DN1ps also coordinated nutrient information through DTk signaling to shape daily locomotor behavior.

Intranasal delivery of mitochondria for treatment of Parkinson’s Disease model rats lesioned with 6-hydroxydopamine

The feasibility of delivering mitochondria intranasally so as to bypass the blood–brain barrier in treating Parkinson's disease (PD), was evaluated in unilaterally 6-OHDA-lesioned rats. Intranasal infusion of allogeneic mitochondria conjugated with Pep-1 (P-Mito) or unconjugated (Mito) was performed once a week on the ipsilateral sides of lesioned brains for three months. A significant improvement of rotational and locomotor behaviors in PD rats was observed in both mitochondrial groups, compared to sham or Pep-1-only groups. Dopaminergic (DA) neuron survival and recovery > 60% occurred in lesions of the substantia nigra (SN) and striatum in Mito and P-Mito rats. The treatment effect was stronger in the P-Mito group than the Mito group, but the difference was insignificant. This recovery was associated with restoration of mitochondrial function and attenuation of oxidative damage in lesioned SN. Notably, P-Mito suppressed plasma levels of inflammatory cytokines. Mitochondria penetrated the accessory olfactory bulb and doublecortin-positive neurons of the rostral migratory stream (RMS) on the ipsilateral sides of lesions and were expressed in striatal, but not SN DA neurons, of both cerebral hemispheres, evidently via commissural fibers. This study shows promise for intranasal delivery of mitochondria, confirming mitochondrial internalization and migration via RMS neurons in the olfactory bulb for PD therapy.