Functional morphology of the feeding system in the ruff — Gymnocephalus cernua (L. 1758) — (Teleostei,Percidae)

The ruff, Gymnocephalus cernua, is a European freshwater fish that feeds by sucking up small invertebrates from the bottom of ponds and slow flowing rivers. The feeding movements have been studied by simultaneous electromyography of seventeen muscles of the head and cinematographic techniques. A theoretical model of movements imposes the functional demands of suction upon an abstraction of the form of a teleost head. Three phases in the feeding act, a preparatory phase, a suction phase and a transport phase, could be correlated with the observed movements and EMGs. Differences between the predicted and the actual movement are discussed. Two different types of feeding occur. The direction, magnitude and duration of the suction forces during feeding are modified, according to the position of the prey. A mechanism preventing early mandibular depression allows sudden and strong suction. Retardation of the suspensorial abduction during the overall expansion of the buccal cavity is ascribed to kinetic interrelations with the hyoid arch. Protrusion of the upper jaws also permits an earlier closure of the mouth and directs the food-containing waterflow posteriorly. When the fish is feeding on sinking prey, protrusion occurs later in the sequence of movements than when it is feeding from the bottom. As the protruded jaws produce a downwardly pointed mouth this retardation aims the suction force.     

Dynamics of human milk extraction: A comparative study of breast feeding and breast pumping

We describe a mathematical model of the flow and deformation in a human teat. Our aim is to compare the theoretical milk yield during infant breast feeding with that obtained through the use of a breast pump. Infants use a peristaltic motion of the tongue, along with some suction, to extract milk, whereas breast pumps use a cyclic pattern of suction only. Our model is based on quasi-linear poroelasticity whereby the teat is modelled as a cylindrical porous elastic material saturated with fluid. We impose a cyclic axial suction pressure difference across the teat and impose a radial compressive force moving along the teat which mimics infant suckling. This is compared to the case of cyclic and steady pumping only which models the action of breast pumps. The results illustrate that there is an optimal time to apply the compressive force during the suction cycle that will increase the flow rate in our theoretical teat. The model and results may be of use in the future design of effective breast pumps.     

The functional morphology of lingual prey capture in a scincid lizard,Tiliqua scincoides (Reptilia: Squamata)

We investigated the functional morphology of lingual prey capture in the blue‐tongued skink, Tiliqua scincoides, a lingual‐feeding lizard nested deep within the family Scincidae, which is presumed to be dominated by jaw‐feeding. We used kinematic analysis of high‐speed video to characterize jaw and tongue movements during prey capture. Phylogenetically informed principal components analysis of tongue morphology showed that, compared to jaw‐feeding scincids and lacertids, T. scincoides and another tongue‐feeding scincid, Corucia zebrata, are distinct in ways suggesting an enhanced ability for hydrostatic shape change. Lingual feeding kinematics show substantial quantitative and qualitative variation among T. scincoides individuals. High‐speed video analysis showed that T. scincoides uses significant hydrostatic elongation and deformation during protrusion, tongue‐prey contact, and retraction. A key feature of lingual prey capture in T. scincoides is extensive hydrostatic deformation to increase the area of tongue‐prey contact, presumably to maximize wet adhesion of the prey item. Adhesion is mechanically reinforced during tongue retraction through formation of a distinctive “saddle” in the foretongue that supports the prey item, reducing the risk of prey loss during retraction.     

A KINEMATIC STUDY OF SUCTION FEEDING AND ASSOCIATED BEHAVIOR IN THE LONG-FINNED PILOT WHALE, GLOBICEPHALA MELAS (TRAILL)

Analysis of videotaped feeding sequences provides novel documentation of suction feeding in captive juvenile long-finned pilot whales ( Globicephala melas ). Swimming and stationary whales were videotaped while feeding at the surface, mid-water, and bottom. The ingestion sequence includes a preparatory phase with partial gape followed by jaw opening and rapid hyoid depression to suck in prey at a mean distance of 14 cm (duration 90 msec), although prey were taken from much greater distances. Depression and retraction of the large, piston-like tongue generate negative intraoral pressures for prey capture and ingestion. Food was normally ingested without grasping by teeth yet was manipulated with lingual, hyoid, and mandibular movement for realignment; suction was then used to transport prey into the oropharynx. Whales frequently rolled or inverted before taking prey, presumably to avoid grasping and repositioning. Prey were sucked off the bottom or sides of the pool without direct contact; lateral suction was used to ingest items from the sides of the mouth.     

The ontogeny of feeding kinematics in a giant salamander Cryptobranchus alleganiensis: Does current function or phylogenetic relatedness predict the scaling patterns of movement?

Studies of the scaling of feeding movements in vertebrates have included three species that display both near-geometric growth and isometry of kinematic variables. These scaling characteristics allow one to examine the “pure” relationship of growth and movement. Despite similar growth patterns, the feeding movements of toads (Bufo) slow down more with increasing body size than those of bass (Micropterus), and sharks (Ginglymostoma). This variation might be due to major differences in the mechanism of prey capture; the bass and sharks use suction to capture prey in water, while the toad uses tongue prehension to capture prey on land. To investigate whether or not these different scaling patterns are correlated with differences in feeding mechanics, we examined the ontogenetic scaling of prey capture movements in the hellbender salamander (Cryptobranchus alleganiensis), which also has near-geometric growth. The hellbender suction feeds in the same general manner as the teleosts and shark, but is much more closely related to the toad. The feeding movements of the hellbender scale more similarly to the feeding movements of toads than to those of fishes or sharks, indicating that phylogenetic relatedness rather than biomechanical similarity predicts ontogenetic scaling patterns of movement.     

Molar occlusion and jaw mechanics of the Eocene primate Adapis

Wear facets on molars of the Eocene primate Adapis magnus are described. Striations on these wear facets indicate three separate directions of mandibular movement during mastication. One direction corresponds to a first stage of mastication involving orthal retraction of the mandible. The remaining two directions correspond to buccal and lingual phases of a second stage of mastication involving a transverse movement of the mandible. The mechanics of jaw adduction are analysed for both the orthal retraction and transverse stages of mastication. During the orthal retraction stage the greatest component of bite force is provided by the temporalis muscles acting directly against the food with the mandible functioning as a link rather than as a lever. A geometrical argument suggests that during the transverse stage of mastication bite force is provided by the temporalis muscles of both sides, the ipsilateral medial and lateral pterygoid muscles, and the contralateral masseter muscle.     

Twist and chew: three-dimensional tongue kinematics during chewing in macaque primates

Three-dimensional (3D) tongue movements are central to performance of feeding functions by mammals and other tetrapods, but 3D tongue kinematics during feeding are poorly understood. Tongue kinematics were recorded during grape chewing by macaque primates using biplanar videoradiography. Complex shape changes in the tongue during chewing are dominated by a combination of flexion in the tongue''s sagittal planes and roll about its long axis. As hypothesized for humans, in macaques during tongue retraction, the middle (molar region) of the tongue rolls to the chewing (working) side simultaneous with sagittal flexion, while the tongue tip flexes to the other (balancing) side. Twisting and flexion reach their maxima early in the fast close phase of chewing cycles, positioning the food bolus between the approaching teeth prior to the power stroke. Although 3D tongue kinematics undoubtedly vary with food type, the mechanical role of this movement—placing the food bolus on the post-canine teeth for breakdown—is likely to be a powerful constraint on tongue kinematics during this phase of the chewing cycle. The muscular drivers of these movements are likely to include a combination of intrinsic and extrinsic tongue muscles.     

Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics

Use of the tongue as a prehensile organ during the ingestion stage of feeding in lizards was studied cinegraphically in seven species. Within Squamata, lingual prehension is limited to a single clade, the Iguania (Iguanidae, Agamidae and Chamaeleontidae), which includes all 'fleshy-tongued' lizards. All remaining squamates (Scleroglossa) use the jaws alone for prey prehension. Lingual prehension and a 'fleshy' tongue are primitive squamate characteristics. Kinematically, lingual ingestion cycles are similar to previously described transport cycles in having slow open, fast open, fast close and slow close-power stroke phases. Tongue movements are sequentially correlated with jaw movements as they are in transport. However, during ingestion, anterior movement of the tongue includes an extra-oral, as well as intra-oral component. Tongue protrusion results in a pronounced slow open-II phase at a large gape distance. A high degree of variability in quantitative aspects of ingestion and transport cycles suggests that modulation through sensory feedback is an important aspect of lizard feeding. Preliminary evidence indicates an important role for hyoid movement in tongue protrusion. Our results are consistent with the Bramble & Wake (1985) model generalized feeding cycle and support their contention that specialized feeding mechanisms often represent modifications of a basic pattern, particularly modification of the slow open phase.     

Adjustment of the human arm viscoelastic properties to the direction of reaching

The viscoelastic properties of the human arm were measured by means of short force perturbations during fast reaching movements in two orthogonal directions. A linear spring model with time delay described the neuromuscular system of the human arm. The obtained viscoelastic parameters ensured movement stability in spite of the time delay of 50 ms. The stiffness and viscosity ellipses appeared to be predominantly orthogonal to the movement direction, which reduced the effect of force perturbation in the direction orthogonal to the reaching movement. Thus, it can be argued that the viscoelastic properties of the neuromuscular system of the human arm are adjusted to the direction of movement according to a “path preserving” strategy, which minimizes the deviation of the movement path from a straight line, when exposed to an unexpected external force.     

The ontogeny of premolar dental wear in Cercocebus albigena (cercopithecidae)

The orientation of striated wear facets on primate teeth serves as a useful guide for reconstructing jaw movements during mastication. Most wear facets on the molars are formed during one of the two well-documented movements, Phase I or Phase II, of the power stroke. Another jaw movement direction, “orthal retraction” (OR) has been proposed to account for a third set of facets occasionally present on the pointed tips of premolars and molars. Evidence advanced here indicates that OR facets on pointed anterior premolars (P₃) of cercopithecoids are actually Phase I facets that have become reoriented as a result of a rotation of this tooth during its eruption. “Orthal retraction” probably does not exist as a discrete masticatory phase.     

Prey capture in the pike-perch,Stizostedion lucioperca (teleostei,percidae): A structural and functional analysis

Summary The pike-perch,Stizostedion lucioperca, uses both suction and grasping during feeding. Type, size, and position of prey and predator determine the movement of catching. This is concluded from simultaneous motion analysis, electromyography, and the record of pressures inside the buccopharyngeal cavity during feeding. The EMG incorporates 24 muscles of the head, including the branchial basket and the anterior body musculature. When the pike-perch begins to feed acceleration and expansion of the head parts determine the negative buccopharyngeal pressure and therefore the suction force applied to different preys. Not the head muscles, but the epaxial and hypaxial body musculatures provide the main force for the rapid expansion of the head through movements of the neurocranium, pectoral girdle, and hyoid arch. Despite the lack of a true neck, the pike-perch is able to move its neurocranium in all directions to aim the suction force. The experiments revealed that ventral and lateral movements aid in the ingestion of a big prey after it has been grasped with the teeth. The head muscles are active as regulators of the opening movements and in the closing movements. Variable overlaps of ab- and adductor activity show that their contraction patterns are interdependent. Variations in the recorded pressures can be related largely to a series of EMGs showing different starting moments of adductor contraction. In this progressive series two patterns were distinguished, and their accompanying movements were compared and related to the type of prey. According to the feeding behavior and morphology, the pike-perch is classified as a rapacious predator. Comparison with some other voracious fishes shows that besides the total length of the lower jaw and the dentigerous area, the construction and dentition of the upper jaws and the anterior suspensorial and neurocranial parts are also important features of this ecological type. However it appears that the fishes selected for this comparison use suction rather than the teeth as the main means of catching the smaller, but commonly eaten prey. The teeth prevent escape after capture by sucking and they increase the maximum prey size that can be caught. In this group, the head ofStizostedion appears to be comparatively well adapted to sucking with grasping adaptations.     

Model-based identification of motion sensor placement for tracking retraction and elongation of the tongue

Electromagnetic articulography (EMA) is designed to track facial and tongue movements. In practice, the EMA sensors for tracking the movement of the tongue’s surface are placed heuristically. No recommendation exists. Within this paper, a model-based approach providing a mathematical analysis and a computational-based recommendation for the placement of sensors, which is based on the tongue’s envelope of movement, is proposed. For this purpose, an anatomically detailed Finite Element (FE) model of the tongue has been employed to determine the envelope of motion for retraction and elongation using a forward simulation. Two optimality criteria have been proposed to identify a set of optimal sensor locations based on the pre-computed envelope of motion. The first one is based on the assumption that locations exhibiting large displacements contain the most information regarding the tongue’s movement and are less susceptible to measurement errors. The second one selects sensors exhibiting each the largest displacements in the anterior-posterior, superior-inferior, medial-lateral and overall direction. The quality of the two optimality criteria is analysed based on their ability to deduce from the respective sensor locations the corresponding muscle activation parameters of the relevant muscle fibre groups during retraction and elongation by solving the corresponding inverse problem. For this purpose, a statistical analysis has been carried out, in which sensor locations for two different modes of deformation have been subjected to typical measurement errors. Then, for tongue retraction and elongation, the expectation value, the standard deviation, the averaged bias and the averaged coefficient of variation have been computed based on 41 different error-afflicted sensor locations. The results show that the first optimality criteria is superior to the second one and that the averaged bias and averaged coefficient of variation decrease when the number of sensors is increased from 2, 4 to 6 deployable sensors.     

Kinematics of the jaw and hyolingual apparatus during feeding in Caiman crocodilus

Movements of the neck, jaws, and hyolingual apparatus during inertial feeding in Caiman crocodilus were studied by cineradiography. Analysis reveals two kinds of cycles: inertial bites (reposition, kill/crush, and transport) and swallowing cycles. They differ in their gape profile and in displacement of the neck, cranium, and hyolingual apparatus. Inertial bites are initiated by an elevation of the neck and cranium; the head is then retracted backward, the prey simultaneously being lifted by the hyolingual apparatus. Next the lower jaw is depressed, and the prey is rapidly pushed further upward by the hyolingual apparatus. Thereafter fast mouth-closure occurs with the neck and cranium being abruptly depressed, the lower jaw elevated, and the hyolingual apparatus rapidly retracted ventrally. Depression of the neck and cranium thrusts the head forward and impacts the backward moving prey more posteriorly in the oral cavity. Swallowing cycles initially involve movement of the hyoid in front of the prey followed by rapid posteroventrad retraction of the hyoid, forcing the prey into the esophagus during opening and closing of the mouth. After mouth-closure, the hyoid apparatus is again protracted. Jaws, neck, tongue, and hyoid apparatus play an active role during intertial feeding sequences. At the beginning of a feeding sequence, the hyolingual apparatus mainly moves dorsoventrally, whereas toward the end of a sequence anteroposterior displacements of the hyoid are prominent. © 1992 Wiley-Liss, Inc.     

Control of leg protraction in the stick insect: a targeted movement showing compensation for externally applied forces

Summary In stick insects, the swing of each rear leg is aimed at the ipsilateral middle leg. The control of this targeted movement was investigated by applying external force to aid or oppose protraction of one rear leg as stick insects walked on a treadwheel.In the first condition studied, the target middle leg was stationary during the protraction of the rear leg (Figs. 1a, 2). The opposing forces tested were 14 and 32 times greater than the peak force exerted during unobstructed protraction. Nevertheless, the rear leg continued to step to a constant position behind the middle leg (Fig. 3).In the second condition, the target middle leg also walked on the wheel. As the force opposing protraction increased, the endpoint of rear leg protraction shifted caudally, the speed of protraction decreased, and the total protraction duration increased (Fig. 5; Table 1). The middle leg's position at the end of rear leg protraction shifted caudally but its posterior extreme position remained virtually unchanged. When the onset of the external force was abrupt, compensation often occurred within 20 ms (Fig. 6a).External forces aiding protraction increased protraction speed only slightly (Table 2). When the force was suddenly removed, the leg continued moving forward but with reduced velocity (Fig. 6b).It is concluded that position information is used only to determine the swing endpoint and that velocity is controlled during the movement. The results are compared with movements to a target by vertebrates and with models of motor control in general.Abbreviations AEP anterior extreme position - PEP posterior extreme position     

Mechanotransduction of mesenchymal melanoma cell invasion into 3D collagen lattices: Filopod-mediated extension–relaxation cycles and force anisotropy

Mesenchymal cell migration in interstitial tissue is a cyclic process of coordinated leading edge protrusion, adhesive interaction with extracellular matrix (ECM) ligands, cell contraction followed by retraction and movement of the cell rear. During migration through 3D tissue, the force fields generated by moving cells are non-isotropic and polarized between leading and trailing edge, however the integration of protrusion formation, cell–substrate adhesion, traction force generation and cell translocation in time and space remain unclear. Using high-resolution 3D confocal reflectance and fluorescence microscopy in GFP/actin expressing melanoma cells, we here employ time-resolved subcellular coregistration of cell morphology, interaction and alignment of actin-rich protrusions engaged with individual collagen fibrils. Using single fibril displacement as sensitive measure for force generated by the leading edge, we show how a dominant protrusion generates extension–retraction cycles transmitted through multiple actin-rich filopods that move along the scaffold in a hand-over-hand manner. The resulting traction force is oscillatory, occurs in parallel to cell elongation and, with maximum elongation reached, is followed by rear retraction and movement of the cell body. Combined live-cell fluorescence and reflection microscopy of the leading edge thus reveals step-wise caterpillar-like extension–retraction cycles that underlie mesenchymal migration in 3D tissue.     

Traction force microscopy in rapidly moving cells reveals separate roles for ROCK and MLCK in the mechanics of retraction

Retraction is a major rate-limiting step in cell motility, particularly in slow moving cell types that form large stable adhesions. Myosin II dependent contractile forces are thought to facilitate detachment by physically pulling up the rear edge. However, retraction can occur in the absence of myosin II activity in cell types that form small labile adhesions. To investigate the role of contractile force generation in retraction, we performed traction force microscopy during the movement of fish epithelial keratocytes. By correlating changes in local traction stress at the rear with the area retracted, we identified four distinct modes of retraction. “Recoil” retractions are preceded by a rise in local traction stress, while rear edge is temporarily stuck, followed by a sharp drop in traction stress upon detachment. This retraction type was most common in cells generating high average traction stress. In “pull” type retractions local traction stress and area retracted increase concomitantly. This was the predominant type of retraction in keratocytes and was observed mostly in cells generating low average traction stress. “Continuous” type retractions occur without any detectable change in traction stress, and are seen in cells generating low average traction stress. In contrast, to many other cell types, “release” type retractions occur in keratocytes following a decrease in local traction stress. Our identification of distinct modes of retraction suggests that contractile forces may play different roles in detachment that are related to rear adhesion strength. To determine how the regulation of contractility via MLCK or Rho kinase contributes to the mechanics of detachment, inhibitors were used to block or augment these pathways. Modulation of MLCK activity led to the most rapid change in local traction stress suggesting its importance in regulating attachment strength. Surprisingly, Rho kinase was not required for detachment, but was essential for localizing retraction to the rear. We suggest that in keratocytes MLCK and Rho kinase play distinct, complementary roles in the respective temporal and spatial control of rear detachment that is essential for maintaining rapid motility.     

Comparative anatomy and evolutionary history of suction feeding in cetaceans

Some odontocetes possess unique features of the hyolingual apparatus that are involved in suction feeding. The hyoid bone and associated musculature generates rapid, piston‐like retraction, and depression of the hyoid and tongue. “Capture” suction feeders (e.g., Globicephala) use suction for capturing and swallowing prey. “Combination” feeders (i.e., Lagenorhynchus) use both raptorial feeding (to capture prey) and suction (to ingest prey). In “capture” suction feeders, features of the hyoid and skull have been attributed to creating suction (i.e., large surface area and mandibular bluntness). In addition to odontocetes, a mysticete, the gray whale (Eschrichtius robustus), is considered a benthic suction feeder. However, anatomical studies of purported suction‐feeding structures of the gray whale are lacking. In addition, few studies have utilized evolutionary approaches to understand the history of suction feeding in cetaceans. This study incorporates quantitative and qualitative hyoid and cranial data from 35 extant and 14 extinct cetacean species into a multivariate principal component analysis and comparative phylogenetic analyses. Conclusions from these analyses are that some commonly attributed features (i.e., ventral throat grooves and mandibular bluntness) and one principal component are significantly correlated with suction feeding. Finally, ancestral state reconstructions indicate that suction feeding likely evolved once, early in cetacean evolutionary history.     

Movement curvature planning through force field internal models

Human motion studies have focused primarily on modeling straight point-to-point reaching movements. However, many goal-directed reaching movements, such as movements directed towards oneself, are not straight but rather follow highly curved trajectories. These movements are particularly interesting to study since they are essential in our everyday life, appear early in development and are routinely used to assess movement deficits following brain lesions. We argue that curved and straight-line reaching movements are generated by a unique neural controller and that the observed curvature of the movement is the result of an active control strategy that follows the geometry of one’s body, for instance to avoid trajectories that would hit the body or yield postures close to the joint limits. We present a mathematical model that accounts for such an active control strategy and show that the model reproduces with high accuracy the kinematic features of human data during unconstrained reaching movements directed toward the head. The model consists of a nonlinear dynamical system with a single stable attractor at the target. Embodiment-related task constraints are expressed as a force field that acts on the dynamical system. Finally, we discuss the biological plausibility and neural correlates of the model’s parameters and suggest that embodiment should be considered as a main cause for movement trajectory curvature.     

Hyoid morphology and movements relative to abducting forces during feeding in Astatotilapia elegans (Teleostei: Cichlidae)

In fishes, the abducting hyoid bars push the suspensoria outwards. This force transmission is generally assumed to be important during fast suction feeding (strenuous activity). In Astatotilapia elegans the hyoid symphysis can best be modelled as an oblique hinge. The relevance of this hinge morphology on the force transmission has been studied by means of a three-dimensional (3D) model simulating the displacements of the hyoid-suspensorial system. It appears that the transmission force factor increases throughout feeding in the case of the hinge model. Reduction of the hyoid symphysis to a point articulation (as was done formerly in attempts to quantify the transmission by means of planar models) suggests an unfavourable decline of the transmission force to zero during maximal mouth expansion. The angle between the hinge axis of the symphysis and the longitudinal axis of the hyoid bar is 45°. Such a configuration allows for a maximal increase in the volume of the buccal cavity for suction. This functional aspect, together with the apparent maximization of the force transmission during feeding, suggests that constructional and neuromotoric factors have been improved during the evolutionary development of the hyoid-suspensorial system.