Review: Depth, navigation and orientation in crabs: Angular acceleration, gravity and hydrostatic pressure sensing during path integration

This review shows how well the published work on the neural basis of balance and hydrostatic pressure reception in crabs agrees with the analyses and models of path integration. Fiddler crabs allow analyses at the level of behaviour. With considerable accuracy, they continuously show the direction to home with their body orientation and use idiothetic path integration to calculate a home vector from the internal measurements of their locomotion. All crabs have a well-developed vestibular system in the statocyst with horizontal and vertical canals which is used for angular acceleration sensing and depth reception. Large identified interneurones abstract the component of angular acceleration in one of the three orthogonal planes. These have properties consistent with a key role in path integration, combining vestibular and proprioceptor information with a central excitatory drive from the hemiellipsoid bodies. They have been monitored during walking, swimming and even in freefall for a 22 s period in parabolic flight.     

Structure of reciprocal connections in visual cortical areas 17 and 18 in cats

Single cortical columns of areas 17, 18 in the cat were microiontophoretically injected with horseradish peroxidase. Spatial and laminar distributions of retrogradell labelled cells in both areas were investigated. Following injections in area 17 or in area 18 the labelled cells' region in area 17 was elongated (in a tangential plane) along the representation of visual field horizontal meridian. However the labelled cells' region in area 18 was elongated along the representation of vertical meridian. Such projection patterns appear to be common in these cortical areas throughout the central 10 degrees on various elevations (from -40 degrees to +10 degrees) of the visual field representation. Thus the spatial arrangement of intrinsic and extrinsic connections in each area coincides, at the same time in area 17 they are orthogonal to area 18. The following visual information exchange scheme may be suggested. Area 17 may supply the area 18 with more detailed information on the horizontal component of the visual image, and in the opposite direction the information on the vertical component of the same image may be supplied.     

How do low horizontal forces produce disproportionately high torques in human locomotion?

Although horizontal ground forces are only approximately 15% of vertical forces, they account for 47% and 33% of the metabolic cost in walking and running. To explain these disproportionately high metabolic costs, we hypothesized that low horizontal ground forces generate relatively high torques on body segments during locomotion and this is mediated by long moment arms. We compared external force moment arms and discreet torques applied to the body segments by horizontal and vertical forces during walking and running. Sixteen subjects (21.9+/-1.9 years) walked at 1.5m/s and ten subjects (23.2+/-2.0 years) ran at 3.83 m/s. Segmental torques in the sagittal plane were partitioned into components due to horizontal and vertical forces and quantified by their angular impulses. The mean (+/-S.E.) ratios of horizontal to vertical ground forces (GF ratio) and angular impulses (AI ratio) in walking were 0.131 (+/-0.003, 95% confidence interval (CI) 0.124-0.137) and 0.530 (+/-0.018, CI 0.497-0.569). Results were similar in running. In both gaits the AI ratios were significantly greater than the GF ratios because the respective CI's did not overlap. The horizontal forces produced 53% and 41% as much angular impulse on the body segments, as did the vertical forces in walking and running despite being only 13% as large. In the two movements the moment arms for the horizontal forces averaged across foot, leg, thigh, and trunk body segments were 3.8 fold larger than those for the vertical forces. The data supported the hypothesis and suggest that the relatively low horizontal vs. vertical forces accounted for a disproportionately higher percentage of the angular impulses placed on the body segments and this effect was due to relatively long moment arms for horizontal forces. These results partially explain the relatively large metabolic cost of generating relatively low horizontal forces.     

Directional sensitivity of wind-sensitive giant interneurons in the cave cricket Troglophilus neglectus.

Unlike the situation in most cockroach and cricket species studied so far, the wind-sensitive cerci of the cave cricket Troglophilus neglectus Krauss (Rhaphidophoridae, Orthoptera) are not oriented parallel to the body axis but perpendicular to it. The effects of this difference on the morphology, and directional sensitivity of cercal giant interneurons (GIs), were investigated. In order to test the hypothesis that the 90 degrees change in cercal orientation causes a corresponding shift in directional sensitivity of GIs, their responses in both the horizontal and vertical planes were tested. One ventral and four dorsal GIs (corresponding to GIs 9-1a and 9-2a, 9-3a, 10-2a, 10-3a of gryllid crickets) were identified. The ventral GI 9-1a of Troglophilus differed somewhat from its cricket homologue in its dendritic arborisation and its directional sensitivity in the horizontal plane. The morphology and horizontal directionality of the dorsal GIs closely resembled that of their counterparts in gryllids. In the vertical plane, the directionality of all GIs tested was similar. They were all excited mainly by wind puffs from the axon-ipsilateral quadrant. The results suggest that directional sensitivity to air currents in the horizontal plane is maintained despite the altered orientation of the cerci. This is presumably due to compensatory modifications in the directional pReferences of the filiform hairs.     

How to climb a tree: lizards accelerate faster,but pause more,when escaping on vertical surfaces

Many species of lizards effectively traverse both two and three‐dimensional habitats. However, few studies have examined maximum locomotor performance on different inclines. Do maximum acceleration and velocity differ on a level and inclined surface? Do lizards pause more on an inclined surface? To address these questions, Sceloporus woodi lizards (N = 12) were run in the laboratory on a level trackway and a vertical tree trunk. This species is known to frequently utilize both vertical and horizontal aspects of its habitat. Average maximum acceleration on the vertical surface exceeded that on the level surface, although average maximum velocity exhibited the opposite pattern. The average number of pauses during level locomotion was lower compared to vertical locomotion. In addition, the average location of the first pause on the level surface was 0.51 m, which is farther than the average for vertical locomotion where the first pause was at 0.35 m. The combination of performance and pause data suggests that the relative lack of pausing during level locomotion allows individuals to reach higher maximum velocities on level surfaces because they accelerate over greater distances. The increased pausing when moving vertically could be a result of high energetic demands of vertical locomotion, or greater microhabitat complexity as a result of branching and/or refuges. The faster acceleration exhibited during vertical locomotion by S. woodi likely offsets the frequent pauses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 83–90.     

Three-dimensional space: locomotory style explains memory differences in rats and hummingbirds

While most animals live in a three-dimensional world, they move through it to different extents depending on their mode of locomotion: terrestrial animals move vertically less than do swimming and flying animals. As nearly everything we know about how animals learn and remember locations in space comes from two-dimensional experiments in the horizontal plane, here we determined whether the use of three-dimensional space by a terrestrial and a flying animal was correlated with memory for a rewarded location. In the cubic mazes in which we trained and tested rats and hummingbirds, rats moved more vertically than horizontally, whereas hummingbirds moved equally in the three dimensions. Consistent with their movement preferences, rats were more accurate in relocating the horizontal component of a rewarded location than they were in the vertical component. Hummingbirds, however, were more accurate in the vertical dimension than they were in the horizontal, a result that cannot be explained by their use of space. Either as a result of evolution or ontogeny, it appears that birds and rats prioritize horizontal versus vertical components differently when they remember three-dimensional space.     

Sensory pathways and their modulation in the control of locomotion

Recent experiments have extended our understanding of how sensory information in premotor networks controlling motor output is processed during locomotion, and at what level the efficacy of specific sensory—motor pathways is determined. Phasic presynaptic inhibition of sensory transmission combined with postsynaptic alterations of excitatory and inhibitory synaptic transmission from interneurons of the premotor networks contribute to the modulation of reflex pathways and to the generation of reflex reversal. These mechanisms play an important role in adapting the operation of central networks to external demands and thus help optimize sensory—motor integration.     

Object localization with whiskers

Rats use their large facial hairs (whiskers) to detect, localize and identify objects in their proximal three-dimensional (3D) space. Here, we focus on recent evidence of how object location is encoded in the neural sensory pathways of the rat whisker system. Behavioral and neuronal observations have recently converged to the point where object location in 3D appears to be encoded by an efficient orthogonal scheme supported by primary sensory-afferents: each primary-afferent can signal object location by a spatial (labeled-line) code for the vertical axis (along whisker arcs), a temporal code for the horizontal axis (along whisker rows), and an intensity code for the radial axis (from the face out). Neuronal evidence shows that (i) the identities of activated sensory neurons convey information about the vertical coordinate of an object, (ii) the timing of their firing, in relation to other reference signals, conveys information about the horizontal object coordinate, and (iii) the intensity of firing conveys information about the radial object coordinate. Such a triple-coding scheme allows for efficient multiplexing of 3D object location information in the activity of single neurons. Also, this scheme provides redundancy since the same information may be represented in the activity of many neurons. These features of orthogonal coding increase accuracy and reliability. We propose that the multiplexed information is conveyed in parallel to different readout circuits, each decoding a specific spatial variable. Such decoding reduces ambiguity, and simplifies the required decoding algorithms, since different readout circuits can be optimized for a particular variable.     

Evidence for implication of primate area V1 in neural 3-D spatial localization processing.

We investigated the neural mechanisms underlying visual localization in 3-D space in area V1 of behaving monkeys. Three different sources of information, retinal disparity, viewing distance and gaze direction, that participate in these neural mechanisms are being reviewed. The way they interact with each other is studied by combining retinal and extraretinal signals. Interactions between retinal disparity and viewing distance have been shown in foveal V1; we have observed a strong modulation of the spontaneous activity and of the visual response of most V1 cells that was highly correlated with the vergence angle. As a consequence of these gain effects, neural horizontal disparity coding is favoured or refined for particular distances of fixation. Changing the gaze direction in the fronto-parallel plane also produces strong gains in the visual response of half of the cells in foveal V1. Cells tested for horizontal disparity and orientation selectivities show gain effects that occur coherently for the same spatial coordinates of the eyes. Shifts in preferred disparity also occurred in several neurons. Cells tested in calcarine V1 at retinal eccentricities larger than 10 degrees , show that horizontal disparity is encoded at least up to 20 degrees around both the horizontal and vertical meridians. At these large retinal eccentricities we found that vertical disparity is also encoded with tuning profiles similar to those of horizontal disparity coding. Combinations of horizontal and vertical disparity signals show that most cells encode both properties. In fact the expression of horizontal disparity coding depends on the vertical disparity signals that produce strong gain effects and frequent changes in peak selectivities. We conclude that the vertical disparity signal and the eye position signal serve to disambiguate the horizontal disparity signal to provide information on 3-D spatial coordinates in terms of distance, gaze direction and retinal eccentricity. We suggest that the relative weight among these different signals is the determining factor involved in the neural processing that gives information on 3-D spatial localization.     

Bands against stripes on the backs of mackerel,Scomber scombrus L.

A thin band of reflecting platelets overlies the central parts of the light and dark stripes found on each side of the dorsal surfaces of the body of the mackerel (Scomber scombrus L.). When this fish has its antero-posterior axis horizontal and its mid-dorsal and mid-ventral lines in the same vertical plane, V, the surfaces of the reflecting platelets in these bands are within a few degrees of being vertical. These surfaces are, however, tipped about 17 degrees from plane V towards the tail. In the angular distributions of radiance commonly found in the sea, the reflections from these bands can mask parts of the pattern of light and dark stripes seen by neighbours in ways that depend on the orientation of the fish in the external light field and the position of the fish relative to its neighbours. With this arrangement, when the fish changes its orientation and/or its velocity with respect to neighbouring fish, this is signalled to the neighbours as changes in the patterns of brightness of its dorsal surfaces. Relatively small changes in roll, pitch and yaw can produce large changes in appearance and, as vision is a most important sense in the mackerel, it seems likely that these changes are important for signalling.     

The halteres of the blowfly Calliphora

The movement of the halteres during fixed flight was video recorded under stroboscopic illumination phase coupled to the wing beat. The halteres swing in a rounded triangular manner through an angle of almost 80° in vertical planes tilted backwards from the transverse plane by ca. 30° (Figs. 1, 2).The physics of the halteres are described in terms of a general formula for the force acting onto the endknob of the moving haltere during rotations and linear accelerations of the fly (Eq. 1). On the basis of the experimentally determined kinematics of the haltere, the primary forces and the forces dependent on angular velocity and on angular acceleration are calculated (Figs. 3, 4).Three distinct types of angular velocity dependent (Coriolis) forces are generated by rotations about 3 orthogonal axes. Thus, in principle one haltere could detect all rotations in space (Fig. 6).The angular acceleration dependent forces have the same direction and frequency as the Coriolis forces, but they are shifted in phase by 90°. Thus, they could be evaluated in parallel and independently from the Coriolis forces. They are, however, much smaller than the Coriolis forces for oscillation frequencies of the fly up to 20 Hz (Fig. 5). From these considerations it is concluded that Coriolis forces play the major role in detecting body rotations.     

Comparison of various motion stimuli on motion sickness and acquisition of adaptation in Suncus Murinus

Effects of various types of motion stimuli were compared to investigate optimum method to elicit motion sickness and adaptation in Suncus murinus (suncus). Three different direction of shaking in the horizontal plane, back and forth, right and left and revolving, induced emetic response to the similar extent. However, vertical shaking was far less effective in inducing motion sickness. Mild and severe horizontal shaking (15 min per day) was continued for 14 days and emetic response to standard motion stimulus was compared before and after the training. The severe daily acceleration strongly depressed the susceptibility to motion stimulus. The mild acceleration which was not emetic stimulus in itself also remarkably attenuated the vomiting response to standard motion stimulus. These results indicate that 1) the emetic responsiveness of the suncus does not depend on the modes of shaking as long as the direction is in the horizontal plane, 2) the suncus is relatively refractory to the vertical linear acceleration and 3) the adaptation to motion stimulus does not develop on the latest peripheral steps of the vomiting reflex pathways.     

Some characteristics of the visual perception of the ant Myrmica sabuleti

Abstract. Using classical conditioning techniques, this study aims to determine what the ant Myrmica sabuleti can see and discriminate. It appears that workers see distinctly vertical as well as horizontal segments 1, 2, 3, 5, 10 and 15 mm wide and 1, 2, 3, 5, 10 and 15 cm long. They can also see distinctly horizontal segments (0.5 × 3 cm) located at 1, 2, 3, 5 and 10 cm height, but do not see such a segment situated at 15 cm height. This allowed the assessment of their maximum distance of vision. Myrmica sabuleti workers also see distinctly vertical segments (0.5 × 3 cm) sloping backwards towards the horizontal at different angles (90, 60, 45, 30, 15 and 0 °). Consequently, M. sabuleti workers see cues lying horizontally on the ground and have a stereovision of a portion of their environment. The species also see distinctly black circles of different sizes located horizontally above them. Thus, they are able to see distinctly slightly modified patterns located aside, below, above as well as before them, and have a small area of binocular vision that both eyes can look at. Myrmica sabuleti workers' maximum distance of vision is directly proportional to the square root of the surface of the object observed. Consequently, the smallest vision angular subtense of an object needed to elicit a reaction in M. sabuleti workers is evaluated as being approximately 5 angular degrees.     

Graviresponses of gliding and swimming Loxodes using step transition to weightlessness

Cells of Loxodes striatus were adjusted to defined culturing, experimental solution O2-supply, temperature, and state of equilibration to be subjected to step type transition of acceleration from normal gravity, (1 g) to the weightless condition (microgravity) during free fall in a 500 m drop shaft. Cellular locomotion inside a vertical experimental chamber was recorded preceding transition and during 10 s of microgravity. Cell tracks from video records were used to separate cells gliding along a solid surface from free swimmers, and to determine gravitaxis and gravikenesis of gliding and swimming cells. With O2 concentrations > or = 40% air saturation gliders and swimmers showed a positive gravitaxis. In microgravity gravitaxis of gliders relaxed within 5 s whereas gravitaxis relaxation of swimmers was not completed even after 10 s. Rates of horizontal gliders (319 micrometers/s) exceeded those, of horizontal swimmers (275 micrometers/s). Relaxation of gravikinesis was incomplete after 10 s of microgravity. Analysis of the locomotion rates during the g-step transition revealed that gliders sediment more slowly, than swimmers (14 versus 45 micrometers/s). The gravikinesis of gliders cancelled sedimentation effects during upward and downward locomotion tending to maintain cells at a predetermined level inside sediments of a freshwater habitat. At > or = 40% air saturation, gravikinesis of swimmers augmented the speed of the majority of cells during gravitaxis, which favours fast vertical migrations of Loxodes.     

An inter-segmental network model and its use in elucidating gait-switches in the stick insect

Animal locomotion requires highly coordinated working of the segmental neuronal networks that control the limb movements. Experiments have shown that sensory signals originating from the extremities play a pivotal role in controlling locomotion patterns by acting on central networks. Based on the results from stick insect locomotion, we constructed an inter-segmental model comprising local networks for all three legs, i.e. for the pro-, meso- and meta-thorax, their inter-connections and the main sensory inputs modifying their activities. In the model, the local networks are uniform, and each of them consists of a central pattern generator (CPG) providing the rhythmic oscillation for the protractor-retractor motor systems, the corresponding motoneurons (MNs), and local inhibitory interneurons (IINs) between the CPGs and the MNs. Between segments, the CPGs are connected cyclically by both excitatory and inhibitory pathways that are modulated by the aforementioned sensory inputs. Simulations done with our network model showed that it was capable of reproducing basic patterns of locomotion such as those occurring during tri- and tetrapod gaits. The model further revealed a number of elementary neuronal processes (e.g. synaptic inhibition, or changing the synaptic drive at specific neurons) that in the simulations were necessary, and in their entirety sufficient, to bring about a transition from one type of gait to another. The main result of this simulation study is that exactly the same mechanism underlies the transition between the two types of gait irrespective of the direction of the change. Moreover, the model suggests that the majority of these processes can be attributed to direct sensory influences, and changes are required only in centrally controlled synaptic drives to the CPGs.     

The Effect of Locomotion on the Mobilization of Minerals from the Maternal Skeleton

Bone is a dynamic tissue from which minerals are deposited or withdrawn according to the body’s demand. During late pregnancy and lactation, female mammals mobilize mineral from bone to support the ossification of offspring skeleton(s). Conversely, in response to mechanical loading, minerals are deposited in bone enabling it to develop a stronger architecture. Despite their central importance to reproductive performance and skeletal integrity, the interactions between these potentially opposing forces remains poorly understood. It is possible that inter-individual differences in the loading imposed by different forms of locomotion may alter the amount of mineral mobilized during reproduction. Here, the impact of vertical versus horizontal locomotion on bone mobilization was examined during reproduction in the laboratory mouse. The vertical, or climbing, group had access to a 60-cm tower, increasing strain on their appendicular skeleton. The horizontal, or tunnel, group had access to a 100-cm tunnel, which encouraged movements within the horizontal plane. Form of locomotion did not impact the amount of bone females mobilized during reproduction or the amount of mineral females deposited in the litter, but maternal bone architecture differed between groups. The climbing group displayed more trabeculae than the tunnel group, whereas the tunnel group displayed greater cortical bone mineral density mid-shaft. Interestingly, pups born to mothers in the climbing group had a higher concentration of total body calcium at 16 days than pups of mothers in the tunnel group. As maternal total body calcium composition and the amount of calcium invested in the full litter were not different between groups, the difference in the relative calcium content of pups between groups is not suspected to reflect difference in mineral allocation. Future research should consider the impact of maternal activity on the efficiency of offspring skeletal ossification via hormones and other bioactive factors transferred in utero and in milk.     

Gait and posture discrimination in sheep using a tri-axial accelerometer

Temporo-spatial observation of the leg could provide important information about the general condition of an animal, especially for those such as sheep and other free-ranging farm animals that can be difficult to access. Tri-axial accelerometers are capable of collecting vast amounts of data for locomotion and posture observations; however, interpretation and optimization of these data records remain a challenge. The aim of the present study was to introduce an optimized method for gait (walking, trotting and galloping) and posture (standing and lying) discrimination, using the acceleration values recorded by a tri-axial accelerometer mounted on the hind leg of sheep. The acceleration values recorded on the vertical and horizontal axes, as well as the total acceleration values were categorized. The relative frequencies of the acceleration categories (RFACs) were calculated in 3-s epochs. Reliable RFACs for gait and posture discrimination were identified with discriminant function and canonical analyses. Post hoc predictions for the two axes and total acceleration were conducted, using classification functions and classification scores for each epoch. Mahalanobis distances were used to determine the level of accuracy of the method. The highest discriminatory power for gait discrimination yielded four RFACs on the vertical axis, and five RFACs each on the horizontal axis and total acceleration vector. Classification functions showed the highest accuracy for walking and galloping. The highest total accuracy on the vertical and horizontal axes were 90% and 91%, respectively. Regarding posture discrimination, the vertical axis exhibited the highest discriminatory power, with values of RFAC (0, 1]=99.95% for standing; and RFAC (−1, 0]=99.50% for lying. The horizontal axis showed strong discrimination for the lying side of the animal, as values were in the acceleration category of (0, 1] for lying on the left side and (−1, 0] on the right side. The algorithm developed by the method employed in the present study facilitates differentiation of the various types of gait and posture in animals from fewer data records, and produces the most reliable acceleration values from only one axis within a short time frame. The present study introduces an optimized method by which the tri-axial accelerometer can be used in gait and posture discrimination in sheep as an animal model.     

Functions of mammalian spinal interneurons during movement

The major recent advances in understanding the role of spinal neurons in generating movement include new information about the modulation of classic reflex pathways during fictive locomotion and in response to pharmacological probes. The possibility of understanding movements in terms of spinal representations of a basic set of movement primitives has been extended by the analysis of normal reflexes. Recordings of the activity of cervical interneurons in behaving monkeys has elucidated their contribution to generating voluntary movement and revealed their involvement in movement preparation.     

Optimization of the mechanical performance of a two-duct semicircular duct system--part 3: the positioning of the ducts in the head

In the majority of vertebrates, the horizontal duct of the vestibular system lies approximately in the yawing plane of the head. The positioning of the vertical ducts, however, is not in the pitch- and roll planes but the vertical ducts generally lie under an angle of about 30-45 degrees relative to the medial plane. Using the equations for a hydrodynamically interconnected two-duct system, optimal positions of the vertical and horizontal ducts in different vertebrate groups can be derived. It was stated that the mean response of the vertical ducts should be optimized. This leads to a symmetrical positioning of the vertical ducts with respect to the medial plane. In all observed vertebrate groups, a solution of mu =(pi-alpha)/2 is found (mu is the angle of the vertical ducts relative to the medial plane, alpha is the angle between the vertical duct planes). For alpha=90 degrees, this provides an equal sensitivity for pitch- and roll- movements. For alpha>90 degrees, a larger sensitivity for pitch movements is obtained, at the expense of a lower sensitivity for roll movements. It is argued that the angle alpha between the vertical ducts may vary from 90 to 120 degrees. In most vertebrates, the centre of mass is stabilized by e.g. fins, tri- or quadrupedal stability, a crawling body or upside-down resting positions (e.g. bats). Birds are generally biped, so in walking they are also rather sensitive to roll. These features are related to labyrinth positioning in the head.