Directed motion in the sea: efficient swimming by reef fish larvae

Directed motion of marine organisms is examined with a focus on efficient behaviour, where efficient swimming minimizes either energetic expenditure or transit time. The swimming behaviour of late pelagic stage reef fish larvae is modelled to illustrate relevant concepts. To swim efficiently in the sea, an organism should exploit current-driven movements of the medium. Favourable currents should be ridden and unfavourable currents avoided. Relatively short movements to control advection can have a greater effect than longer swimming bouts used for independent horizontal locomotion. If larvae exploit the vertical structure of the water column, then the extent to which they can influence their dispersal will be substantially increased.     

Integrative neuroscience: linking levels of analyses

If we are to understand how the brain performs different integrated functions in cellular terms, we need both to understand all relevant levels of analysis from the molecular to the behavioural and cognitive levels and to realize an integration of such levels. This is currently a major challenge for neuroscience. Most research, whether dealing with perception, action or learning, focuses on a few levels of organization, for instance the molecular level and brain imaging, and leaves other crucial areas practically untouched. To reach the level of understanding that we desire, a multi-level approach is required in which the different levels link into each other. It is possible to bridge across the different levels for one system, and this has been demonstrated, for example, in the lamprey in generation of goal-directed locomotion. It can be argued that an integrated analysis of any neural system cannot be performed without the aid of a close interaction between experiments and modelling. The dynamic processing within any neural system is such that an intuitive interpretation is rarely sufficient.     

Better Endurance and Load Capacity: An Improved Design of Manta Ray Robot (RoMan-II)

An improved design of a biomimetic underwater vehicle (RoMan-II) inspired by manta ray is presented in this paper. The design of the prototype and the swimming motion control are discussed. Instead of using rigid multiple degree-of-freedom linkages as fin rays in the first version, six flexible fin rays are adopted to drive two sided fins which generate thrust through flapping motions. Furthermore, in order to save the energy for a long distance cruising, a bio-inspired gliding motion is incorporated onto the motion control of the improved prototype. With a closed-loop buoyancy control system, the vehicle can perform gliding locomotion in water, which reduces the overall energy consumption. The vehicle can also perform pivot turning and backward locomotion without turning its body. It can achieve an average velocity of one body length per second. The vehicle is able to carry various sensors or communication equipments, as the payload capacity is about 4 kg. Initial testing shows that the operation time of the buoyancy body is estimated to about 6 hours for free swimming and 90 hours for a pure gliding. The flapping frequency, flapping amplitude, and the number of waves performed across the fin's chord and wave directions can be independently tuned through the proposed control scheme. In general, the present prototype provides a useful platform to study the ray-like swimming motion in a single or combination mode of flapping, undulation and gliding.     

From cognitive to neural models of working memory

Working memory refers to the temporary retention of information that was just experienced or just retrieved from long-term memory but no longer exists in the external environment. These internal representations are short-lived, but can be stored for longer periods of time through active maintenance or rehearsal strategies, and can be subjected to various operations that manipulate the information in such a way that makes it useful for goal-directed behaviour. Empirical studies of working memory using neuroscientific techniques, such as neuronal recordings in monkeys or functional neuroimaging in humans, have advanced our knowledge of the underlying neural mechanisms of working memory. This rich dataset can be reconciled with behavioural findings derived from investigating the cognitive mechanisms underlying working memory. In this paper, I review the progress that has been made towards this effort by illustrating how investigations of the neural mechanisms underlying working memory can be influenced by cognitive models and, in turn, how cognitive models can be shaped and modified by neuroscientific data. One conclusion that arises from this research is that working memory can be viewed as neither a unitary nor a dedicated system. A network of brain regions, including the prefrontal cortex (PFC), is critical for the active maintenance of internal representations that are necessary for goal-directed behaviour. Thus, working memory is not localized to a single brain region but probably is an emergent property of the functional interactions between the PFC and the rest of the brain.     

The swimming activity of the staggerer mutant mouse

Four experiments investigated the swimming behaviour of staggerer mutant mice. The results partially confirmed previous reports that a mouse's swimming is unaffected by the staggerer mutation. In terms of speed and distance there are indeed no measurable differences between normal and staggerer mice, when first placed in the water. The stagger's resistance was however shown to be much lower than a normal's and the genetic difference was also associated with different styles of swimming. Furthermore, whereas the normal mouse's swimming behaviour evolves with increased time in the water, the staggerer's remains constant.The differences are interpreted on the basis of abnormal novelty reactions by the staggerer mutants. Thus, swimming appears to be a better tool for investigating the higher-level cognitive functions of this mutant than terrestrial locomotion.     

Serotonin influences locomotion in the nudibranch mollusc Melibe leonina

Serotonin (5-HT) influences locomotion in many animals, from flatworms to mammals. This study examined the effects of 5-HT on locomotion in the nudibranch mollusc Melibe leonina (Gould, 1852). M. leonina exhibits two modes of locomotion, crawling and swimming. Animals were bath-immersed in a range of concentrations of 5-HT or injected with various 5-HT solutions into the hemolymph and then monitored for locomotor activity. In contrast to other gastropods studied, M. leonina showed no significant effect of 5-HT on the distance crawled or the speed of crawling. However, the highest concentration (10(-3) mol l(-1) for bath immersion and 10(-5) mol l(-1) for injection) significantly increased the time spent swimming and the swimming speed. The 5-HT receptor antagonist methysergide inhibited the influence of 5-HT on the overall amount of swimming but not on swimming speed. These results suggest that 5-HT influences locomotion at the behavioral level in M. leonina. In conjunction with previous studies on the neural basis of locomotion in M. leonina, these results also suggest that this species is an excellent model system for investigating the 5-HT modulation of locomotion.     

Lungfish Axial Muscle Function and the Vertebrate Water to Land Transition

The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates. The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics. Lungfish are an ideal group to study the role of axial function in terrestrial locomotion as they are the sister taxon to tetrapods and regularly move on land. Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty. We compared terrestrial lungfish data to data from lungfish swimming in different viscosities as well as to salamander locomotion. The terrestrial locomotion of lungfish involved substantial activity in the trunk muscles but almost no tail activity. Unlike other elongate vertebrates, lungfish moved on land with a standing wave pattern of axial muscle activity that closely resembled the pattern observed in terrestrially locomoting salamanders. The similarity in axial motor pattern in salamanders and lungfish suggests that some aspects of neuromuscular control for the axial movements involved in terrestrial locomotion were present before derived appendicular structures.     

Triturus newts defy the running-swimming dilemma

Conflicts between structural requirements for carrying out different ecologically relevant functions may result in a compromise phenotype that maximizes neither function. Identifying and evaluating functional trade-offs may therefore aid in understanding the evolution of organismal performance. We examined the possibility of an evolutionary trade-off between aquatic and terrestrial locomotion in females of European species of the newt genus Triturus. Biomechanical models suggest a conflict between the requirements for aquatic and terrestrial locomotion. For instance, having an elongate, slender body, a large tail, and reduced limbs should benefit undulatory swimming, but at the cost of reduced running capacity. To test the prediction of an evolutionary trade-off between swimming and running capacity, we investigated relationships between size-corrected morphology and maximum locomotor performance in females of ten species of newts. Phylogenetic comparative analyses revealed that an evolutionary trend of body elongation (increasing axilla-groin distance) is associated with a reduction in head width and forelimb length. Body elongation resulted in reduced maximum running speed, but, surprisingly, also led to a reduction in swimming speed. The evolution of longer tails was associated with an increase in maximal swimming speed. We found no evidence for an evolutionary trade-off between aquatic and terrestrial locomotor performance, probably because of the unexpected negative effect of body elongation on swimming speed. We conclude that the idea of a design conflict between aquatic and terrestrial locomotion, mediated through antagonistic effects of body elongation, does not apply to our model system.     

Speed/accuracy trade-off between the habitual and the goal-directed processes

Instrumental responses are hypothesized to be of two kinds: habitual and goal-directed, mediated by the sensorimotor and the associative cortico-basal ganglia circuits, respectively. The existence of the two heterogeneous associative learning mechanisms can be hypothesized to arise from the comparative advantages that they have at different stages of learning. In this paper, we assume that the goal-directed system is behaviourally flexible, but slow in choice selection. The habitual system, in contrast, is fast in responding, but inflexible in adapting its behavioural strategy to new conditions. Based on these assumptions and using the computational theory of reinforcement learning, we propose a normative model for arbitration between the two processes that makes an approximately optimal balance between search-time and accuracy in decision making. Behaviourally, the model can explain experimental evidence on behavioural sensitivity to outcome at the early stages of learning, but insensitivity at the later stages. It also explains that when two choices with equal incentive values are available concurrently, the behaviour remains outcome-sensitive, even after extensive training. Moreover, the model can explain choice reaction time variations during the course of learning, as well as the experimental observation that as the number of choices increases, the reaction time also increases. Neurobiologically, by assuming that phasic and tonic activities of midbrain dopamine neurons carry the reward prediction error and the average reward signals used by the model, respectively, the model predicts that whereas phasic dopamine indirectly affects behaviour through reinforcing stimulus-response associations, tonic dopamine can directly affect behaviour through manipulating the competition between the habitual and the goal-directed systems and thus, affect reaction time.     

Goal-direction and top-down control

We review the neural mechanisms that support top-down control of behaviour and suggest that goal-directed behaviour uses two systems that work in concert. A basal ganglia-centred system quickly learns simple, fixed goal-directed behaviours while a prefrontal cortex-centred system gradually learns more complex (abstract or long-term) goal-directed behaviours. Interactions between these two systems allow top-down control mechanisms to learn how to direct behaviour towards a goal but also how to guide behaviour when faced with a novel situation.     

Locomotion and phenotypic transformation of the amoeboflagellate Naegleria gruberi at the water-air interface

The protozoon Naegleria gruberi is able to carry out amoeboid locomotion at the water-air interface in a manner indistinguishable from that exhibited on solid substrata with the production of focal contacts and associated filopodia. The speed of locomotion at this interface can be modulated by changes in electrolyte concentrations; these speed changes are identical to those observed at a water-glass interface. The nature of the water-air interface is discussed leading to the hypothesis that surface tension alone could provide suitable properties for the adhesion and translocation of amoebae at this interface without necessitating specific, absorbed molecules. The temporary swimming flagellate stage of Naegleria is able to dock at the interface, make stable adhesions to it, and revert to the amoeboid phenotype. Conversely, amoebae resident at the water-air interface can transform to swimming flagellates and escape into the bulk liquid phase. We report the presence of Naegleria amoebae in the surface microlayers of natural ponds; thus, in freshwater bodies there may be active shuttling of Naegleria amoebae from the benthos to the surface microlayers by means of the non-feeding, swimming flagellate phenotype. The public health implication of this behaviour in the case of the pathogenic relative, Naegleria fowleri, is discussed.     

Decoding the mechanisms of gait generation in salamanders by combining neurobiology, modeling and robotics

Vertebrate animals exhibit impressive locomotor skills. These locomotor skills are due to the complex interactions between the environment, the musculo-skeletal system and the central nervous system, in particular the spinal locomotor circuits. We are interested in decoding these interactions in the salamander, a key animal from an evolutionary point of view. It exhibits both swimming and stepping gaits and is faced with the problem of producing efficient propulsive forces using the same musculo-skeletal system in two environments with significant physical differences in density, viscosity and gravitational load. Yet its nervous system remains comparatively simple. Our approach is based on a combination of neurophysiological experiments, numerical modeling at different levels of abstraction, and robotic validation using an amphibious salamander-like robot. This article reviews the current state of our knowledge on salamander locomotion control, and presents how our approach has allowed us to obtain a first conceptual model of the salamander spinal locomotor networks. The model suggests that the salamander locomotor circuit can be seen as a lamprey-like circuit controlling axial movements of the trunk and tail, extended by specialized oscillatory centers controlling limb movements. The interplay between the two types of circuits determines the mode of locomotion under the influence of sensory feedback and descending drive, with stepping gaits at low drive, and swimming at high drive.     

Experiments on the central pattern generator for swimming in amphibian embryos

The central nervous system of paralysed Xenopus laevis embryos can generate a motor output pattern suitable for swimming locomotion. By recording motor root activity in paralysed embryos with transected nervous systems we have shown that: (a) the spinal cord is capable of swimming pattern generation; (b) swimming pattern generator capability in the hindbrain and spinal cord is distributed; (c) caudal hindbrain is necessary for sustained swimming output after discrete stimulation. By recording similarly from embryos whose central nervous system was divided longitudinally into left and right sides, we have shown that: (a) each side can generate rhythmic motor output with cycle periods like those in swimming; (b) during this activity cycle period increases within an episode, and there is the usual rostrocaudal delay found in swimming; (c) this activity is influenced by sensory stimuli in the same way as swimming activity; (d) normal phase coupling of the left and right sides can be established by the ventral commissure in the spinal cord. We conclude that interactions between the antagonistic (left and right) motor systems are not necessary for swimming rhythm generation and present a model for swimming pattern generation where autonomous rhythm generators on each side of the nervous system drive the motoneurons. Alternation is achieved by reciprocal inhibition, and activity is initiated and maintained by tonic excitation from the hindbrain.     

Behaviour of fish by-catch in the mouth of a crustacean trawl

The behaviour of fish by-catch was recorded and characterized by in situ observations in the mouth of a crustacean trawl using an underwater camera system with artificial light, at depths between 106 and 461 m, along the central coast of Chile. The groups or species studied were rattails (family Macrouridae), Chilean hake Merluccius gayi gayi, sharks (orders Carcharhiniformes and Squaliformes), skates (family Rajidae), flatfishes (genus Hippoglossina) and small benthopelagic and demersal fishes (orders Osmeriformes, Stomiiformes, Gadiformes, Ophidiiformes and Perciformes). The fish behaviour was categorized in terms of (1) position in the water column, (2) initial orientation with respect to the trawl, (3) locomotion and (4) swimming speed with respect to the trawl. Rattails, sharks, skates and flatfishes were passive in response to the trawl and showed similar behavioural patterns, with most fishes observed sitting or touching the bottom with no swimming or other activity. Merluccius gayi gayi was the most active species, displaying a wide combination of behavioural responses when the trawl approached. This species showed several behavioural patterns, mainly characterized by swimming forward at variable speed. A fraction of small bentho-pelagic and demersal fishes also showed an active behaviour but always at lower speed than the trawl. The species-specific differences in behaviour in the mouth of the trawl suggest that improvements at the level of the footrope can be made to reduce by-catch, especially of passive species.     

Effects of the trematode Microphallus turgidus on locomotion and prey capture in the grass shrimp Palaemonetes pugio

The grass shrimp, Palaemonetes pugio, is common in estuaries and marshes along the east coast of the USA and is frequently infected with metacercariae of the trematode, Microphallus turgidus. To test whether or not M. turgidus has an effect on intermediate host behaviour, the length of time spent swimming and walking over 1 min and 3 min intervals and prey (Artemia) capture rates of uninfected grass shrimp and those infected with 1-10, 11-20 or 21-30 metacercarial cysts were compared. Uninfected shrimps spent significantly more time swimming than infected shrimps during the first minute of observation. There were no differences between the control and infected groups in terms of swimming at 3 min, walking at 1 and 3 min, or in numbers of prey captured. These results indicate that M. turgidus may induce little or no change in grass shrimp locomotion nor in prey capture behaviour. This is in contrast to other parasites that modify intermediate host behaviour to enhance their transmission to definitive hosts. Furthermore, these data support earlier studies indicating that M. turgidus does not affect the growth and survival of P. pugio.     

Different modes of swimming of the carp, Cyprinus carpio L.

An electromyographical study has been made of carp swimming muscles at various points along the body length during sustained and burst locomotion. During sustained swimming, red muscles show a constant time lag between activation of anterior and posterior segments which is practically independent of the speed of locomotion. In contrast, anterior and posterior homolateral segments are activated simultaneously during bursts of rapid movement. This pattern of co-ordination between body segments differs from that reported for other species.     

Swimming speed performance in coral reef fishes: field validations reveal distinct functional groups

Central to our understanding of locomotion in fishes are the performance implications of using different modes of swimming. Employing a unique combination of laboratory performance trials and field observations of swimming speed, this study investigated the comparative performance of pectoral and body-caudal fin swimming within an entire assemblage of coral reef fishes (117 species 10 families). Field observations of swimming behaviour identified three primary modes: labriform (pectoral 70 spp.), subcarangiform (body-caudal 29 spp.) and chaetodontiform (augmented body-caudal 18 spp.). While representative taxa from all three modes were capable of speeds exceeding 50 cm s⁻¹ during laboratory trials, only pectoral-swimmers maintained such high speeds under field conditions. Direct comparisons revealed that pectoral-swimming species maintained field speeds at a remarkable 70% of their maximum (lab-tested) recorded speed; species using body-caudal fin propulsion maintained field speeds at around 50% of maximum. These findings highlight a profound influence of swimming mode on performance, with the relative mechanical and energetic efficiency of each swimming mode being of major importance. Combining attributes of efficiency, maneuverability and speed in one mode of propulsion, pectoral swimming appears to be a particularly versatile form of locomotion, well suited to a demersal lifestyle on coral reefs.     

Development of motor behaviour

The development of motor behaviour depends on the differentiation of underlying circuitry. Recent work with the zebrafish brings the simple swimming behaviour of lower vertebrates and their embryos into focus as a suitable model to study the development of motor circuitry and its genetic control. Changes in connectivity and excitability contribute to the development of swimming in this simple system. In the chick embryo, limb motor circuitry is spontaneously active before motor axons reach their muscle targets, and it has properties in common with the spontaneously active networks in the retina. The early rhythmic activity responsible for embryonic movement is probably a generalised property of developing spinal networks that precedes, and may be required for, the completion of functional locomotor circuitry.     

Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease

Progressive loss of the ascending dopaminergic projection in the basal ganglia is a fundamental pathological feature of Parkinson's disease. Studies in animals and humans have identified spatially segregated functional territories in the basal ganglia for the control of goal-directed and habitual actions. In patients with Parkinson's disease the loss of dopamine is predominantly in the posterior putamen, a region of the basal ganglia associated with the control of habitual behaviour. These patients may therefore be forced into a progressive reliance on the goal-directed mode of action control that is mediated by comparatively preserved processing in the rostromedial striatum. Thus, many of their behavioural difficulties may reflect a loss of normal automatic control owing to distorting output signals from habitual control circuits, which impede the expression of goal-directed action.