Largemouth bass (Micropterus salmoides) switch feeding modalities in response to sensory deprivation

Animals use a suite of sensory modalities to precisely locate and capture prey. While numerous studies have examined the effects of sensory deprivation on the behaviors leading to prey capture and while it is generally believed that information in the pre-strike period determines the way fish capture prey, this study is the first to examine the contribution of sensory information to jaw kinematics during capture. Largemouth bass were filmed using high-speed videography while capturing live mosquitofish. Bass were examined intact, with visual deprivation under infrared light, and with lateral line deprivation following treatment with cobalt chloride. Deprived of visual cues, this visual ram-feeding predator switches towards suction-based feeding to successfully capture prey. They approach prey slowly but open their mouths more rapidly, which has been shown to result in greater buccal pressure, causing their prey to move a greater distance at a more rapid velocity as they are being drawn into the predators' mouths. Deprived of lateral line cues, bass have higher forward velocities during capture and capture prey earlier in the gape cycle. This study demonstrates that sensory pre-strike information directly affects the capture modality employed by fishes and that fish can modulate between ram and suction not only by adjusting the amount of ram by increasing or decreasing their movements, but also by actively increasing the amount of suction used. These results suggest that the ability to modulate feeding behavior may allow animals to not only exploit a broader breadth of prey items, but also to be capable of doing so in a wider variety of environments.     

Neural mechanisms underlying the evolvability of behaviour

The complexity of nervous systems alters the evolvability of behaviour. Complex nervous systems are phylogenetically constrained; nevertheless particular species-specific behaviours have repeatedly evolved, suggesting a predisposition towards those behaviours. Independently evolved behaviours in animals that share a common neural architecture are generally produced by homologous neural structures, homologous neural pathways and even in the case of some invertebrates, homologous identified neurons. Such parallel evolution has been documented in the chromatic sensitivity of visual systems, motor behaviours and complex social behaviours such as pair-bonding. The appearance of homoplasious behaviours produced by homologous neural substrates suggests that there might be features of these nervous systems that favoured the repeated evolution of particular behaviours. Neuromodulation may be one such feature because it allows anatomically defined neural circuitry to be re-purposed. The developmental, genetic and physiological mechanisms that contribute to nervous system complexity may also bias the evolution of behaviour, thereby affecting the evolvability of species-specific behaviour.     

Multimodal sensory integration in insects--towards insect brain control architectures

Although a variety of basic insect behaviours have inspired successful robot implementations, more complex capabilities in these 'simple' animals are often overlooked. By reviewing the general architecture of their nervous systems, we gain insight into how they are able to integrate behaviours, perform pattern recognition, context-dependent learning, and combine many sensory inputs in tasks such as navigation. We review in particular what is known about two specific 'higher' areas in the insect brain, the mushroom bodies and the central complex, and how they are involved in controlling an insect's behaviour. While much of the functional interpretation of this information is still speculative, it nevertheless suggests some promising new approaches to obtaining adaptive behaviour in robots.     

Lateral neural borders as precursors of peripheral nervous systems: A comparative view across bilaterians

The nervous systems in most bilaterians are centralized, composed of central nervous systems (CNS) and peripheral nervous systems (PNS). Common molecular and cellular patterns of medial nerve cords have been observed in various distantly related bilaterians, suggesting deep homology of CNS. The development patterns of PNS, however, are more diverse than CNS across different phylogenetic lineages and the evolution of PNS so far has been thought to be polygenic. The molecular and cellular programs during the development of PNS among different bilaterian branches are drastically different. For example, vertebrate PNS is essentially derived from neural crest cells and placodes, which are largely vertebrate innovations and do not exist in invertebrates. On the other hand, the lack of common precursor cell types does not necessarily lead to the conclusion of different evolutionary origins. Homology needs to be examined with a deeper and broader scope. In this review, we examined the molecular, cellular and developmental characteristics of PNS in a broad range of bilaterians to summarize our current understanding of variation and potentially conserved themes. These comparisons demonstrate that there exist both migratory and non-migratory neuroblasts in the lateral border of CNS precursors in most model bilaterian animals. These lateral border neuroblasts are specified by conserved gene regulatory network and give rise to sensory neurons, suggesting that lateral border neuroblasts represent the progenitor of PNS and share deep homology among different branches of Bilateria. Future studies are needed to elucidate the evo-devo mechanisms of the lateral neural borders as PNS progenitors.     

Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish

Sensory systems provide crucial information about an organism's external environment and, thus, are often subject to strong natural selection. Because of the large variation in the intensity and spectral quality of light in aquatic environments, studies of sensory adaptation have focused on the visual systems of fish for over a half a century. Recently, the molecular genetic mechanisms that determine the spectral sensitivity of visual pigments have been characterized in several fishes including zebrafish, guppies, medaka, killifish, bream, and cichlids. The results of these studies suggest that teleost fish have incredibly diverse visual systems. In this paper, we review the role that opsin duplication and differential gene expression have played in the diversification of visual pigments. We compare our findings in cichlids to five other taxonomic groups and highlight the ways that their similarities and differences may provide new insights into the molecular genetic basis of sensory adaptation and diversification.     

Diversification of coordination patterns during feeding behaviour in cheiline wrasses

Successful fish feeding often requires the coordination of several complex motor and sensory systems to ensure that food is accurately detected, approached, acquired, and consumed. In the present study, we address feeding behaviour as a coordinated set of multiple, facultatively independent, anatomical systems. We sought to determine whether the patterns of interaction between trophic, locomotor, and oculomotor systems are associated with changes in morphology and ecology within a closely-related, but trophically divergent, group of fishes. We present a quantitative kinematic analysis of skull motion, locomotor behaviour, and oculomotor responses during feeding to assess coordination in three functional systems directly involved in feeding. We use coordination profiles to depict the feeding behaviours of three carnivorous coral reef fishes of the tribe Cheilinini in the family Labridae (the wrasses): Cheilinus fasciatus (a slow-swimming predator of benthic invertebrates), Epibulus insidiator (a slow-stalking predator with extraordinary jaw protrusion), and Oxycheilinus digrammus (a fast-attack predator). Differences were detected in several variables relating to jaw, body, fin, and eye movements. Overall patterns of coordination were more similar between E. insidiator and O. digrammus , which are capable of capturing elusive prey, than between C. fasciatus and E. insidiator , which are the two most closely-related species among the three. Evidence for the evolution of coordination patterns among cheiline fishes suggests that the sensory-motor systems involved in processing stimuli and coordinating a physical response during feeding have changed considerably, even among closely-related species.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 289–308.     

Electroreception in marine fishes: chondrichthyans

Electroreception in marine fishes occurs across a variety of taxa and is best understood in the chondrichthyans (sharks, skates, rays, and chimaeras). Here, we present an up-to-date review of what is known about the biology of passive electroreception and we consider how electroreceptive fishes might respond to electric and magnetic stimuli in a changing marine environment. We briefly describe the history and discovery of electroreception in marine Chondrichthyes, the current understanding of the passive mode, the morphological adaptations of receptors across phylogeny and habitat, the physiological function of the peripheral and central nervous system components, and the behaviours mediated by electroreception. Additionally, whole genome sequencing, genetic screening and molecular studies promise to yield new insights into the evolution, distribution, and function of electroreceptors across different environments. This review complements that of electroreception in freshwater fishes in this special issue, which provides a comprehensive state of knowledge regarding the evolution of electroreception. We conclude that despite our improved understanding of passive electroreception, several outstanding gaps remain which limits our full comprehension of this sensory modality. Of particular concern is how electroreceptive fishes will respond and adapt to a marine environment that is being increasingly altered by anthropogenic electric and magnetic fields.     

Stabilization of motor asymmetry in the goldfish under the influence of optokinetic stimulation

Adaptation as a memory model appears, at the cellular level, as an increase in the resistivity of neurons to fatigue under the influence of repetitive natural training stimulation. Selective induction of adaptational changes in separate compartments of one and the same neuron can also serve as an important instrument for identification of the roles of these compartments in the integrative function of the individual neuron. Mauthner neurons (MNs) of fishes (the goldfish in particular) possess a clearly differentiated soma and two dendrites, lateral and ventral ones. The soma and lateral dendrite of each MN receive afferentation from the ipsilateral vestibular apparatus; at present, the functional and morphological aspects of selective adaptational modifications induced in these compartments by adequate vestibular stimulation have been examined in detail. As to the ventral MN dendrite receiving visual afferentation from the contralateral eye via the ipsilateral tectum, it remained impossible until now to realize the respective approach. We found that training sessions of visual optokinetic stimulation performed in certain modes provide selective activation of one MN through its ventral dendrite and increase the resistivity of this cell to fatiguing stimulation. Therefore, we first demonstrated the possibility of adaptational changes in an individual ventral dendrite of the MN. If fishes were preliminarily adapted with respect to vestibular stimulation, and the resistivity of the soma and lateral dendrite was selectively increased, the resistivity to fatiguing visual test stimulation also increased. On the other hand, if fishes were preliminarily adapted with respect to visual stimulation, the resistivity to fatiguing vestibular stimulation also increased. The observed increase in the resistivity of MNs of fishes adapted due to sensory stimulation of one afferent input with respect to sensory stimulation of other sensory input, as well as an increase in the resistivity to sensory stimulation of one modality, probably show that the mechanism of increase in the resistivity is the same in both cases. Neirofiziologiya/Neurophysiology, Vol. 40, No. 3, pp. 211–220, May–June, 2008.     

Coherence in nervous system design: the visual system of Pantodon buchholzi

One of the more unusual visual systems of the Actinopterygii is that of Pantodon buchholzi (Osteoglossomorpha: Osteoglossidae). Its adaptations associate neuroanatomy at different levels of the visual system with ecological and behavioural correlates and demonstrate that the visual system of this fish has adapted for simultaneous vision in air and water. The visual field is divided into three distinct areas: for viewing into the water column, into air, and for viewing the aquatic reflection from the underside of the water surface. Cone diameters in different retinal areas correlate with the differing physical constraints in the respective visual field. Retinal differentiation between the aquatic and aerial views is paralleled at different levels of the central nervous system. A diencephalic nucleus receives both direct and indirect (tectal) afferent input from only the aerial visual system and a specific type of cell in the optic tectum is preferentially distributed in the tectum processing aerial inputs. Distinctions within a single sensory system suggest that some behaviours may be organized according to visual field. For Pantodon, feeding is initiated by stimuli seen by the ventral hemiretina so the anatomical specializations may well play an important role as elements in a feeding circuit.     

The cytokine macrophage migration inhibitory factor (MIF) acts as a neurotrophin in the developing inner ear of the zebrafish, Danio rerio

Macrophage migration inhibitory factor (MIF) plays versatile roles in the immune system. MIF is also widely expressed during embryonic development, particularly in the nervous system, although its roles in neural development are only beginning to be understood. Evidence from frogs, mice and zebrafish suggests that MIF has a major role as a neurotrophin in the early development of sensory systems, including the auditory system. Here we show that the zebrafish mif pathway is required for both sensory hair cell (HC) and sensory neuronal cell survival in the ear, for HC differentiation, semicircular canal formation, statoacoustic ganglion (SAG) development, and lateral line HC differentiation. This is consistent with our findings that MIF is expressed in the developing mammalian and avian auditory systems and promotes mouse and chick SAG neurite outgrowth and neuronal survival, demonstrating key instructional roles for MIF in vertebrate otic development.     

Molluscan neurons in culture: shedding light on synapse formation and plasticity

From genes to behaviour, the simple model system approach has played many pivotal roles in deciphering nervous system function in both invertebrates and vertebrates. However, with the advent of sophisticated imaging and recording techniques enabling the direct investigation of single vertebrate neurons, the utility of simple invertebrate organisms as model systems has been put to question. To address this subject meaningfully and comprehensively, we first review the contributions made by invertebrates in the field of neuroscience over the years, paving the way for similar breakthroughs in higher animals. In particular, we focus on molluscan (Lymnaea, Aplysia, and Helisoma) and leech (Hirudo) models and the pivotal roles they have played in elucidating mechanisms of synapse formation and plasticity. While the ultimate goal in neuroscience is to understand the workings of the human brain in both its normal and diseased states, the sheer complexity of most vertebrate models still makes it difficult to define the underlying principles of nervous system function. Investigators have thus turned to invertebrate models, which are unique with respect to their simple nervous systems that are endowed with a finite number of large, individually identifiable neurons of known function. We start off by discussing in vivo and semi-intact preparations, regarding their amenability to simple circuit analysis. Despite the 'simplicity' of invertebrate nervous systems however, it is still difficult to study individual synaptic connections in detail. We therefore emphasize in the next section, the utility of studying identified invertebrate neurons in vitro, to directly examine the development, specificity, and plasticity of synaptic connections in a well-defined environment, at a resolution that it is still unapproachable in the intact brain. We conclude with a discussion of the future of invertebrates in neuroscience in elucidating mechanisms of neurological disease and developing neuron-silicon interfaces.     

The Roles of the Dystrophin-Associated Glycoprotein Complex at the Synapse

Duchenne muscular dystrophy is caused by mutations in the dystrophin gene and is characterized by progressive muscle wasting. A number of Duchenne patients also present with mental retardation. The dystrophin protein is part of the highly conserved dystrophin-associated glycoprotein complex (DGC) which accumulates at the neuromuscular junction (NMJ) and at a variety of synapses in the peripheral and central nervous systems. Many years of research into the roles of the DGC in muscle have revealed its structural function in stabilizing the sarcolemma. In addition, the DGC also acts as a scaffold for various signaling pathways. Here, we discuss recent advances in understanding DGC roles in the nervous system, gained from studies in both vertebrate and invertebrate model systems. From these studies, it has become clear that the DGC is important for the maturation of neurotransmitter receptor complexes and for the regulation of neurotransmitter release at the NMJ and central synapses. Furthermore, roles for the DGC have been established in consolidation of long-term spatial and recognition memory. The challenges ahead include the integration of the behavioral and mechanistic studies and the use of this information to identify therapeutic targets.     

Information-processing demands in electrosensory and mechanosensory lateral line systems.

The electrosensory and mechanosensory lateral line systems of fish exhibit many common features in their structural and functional organization, both at the sensory periphery as well as in central processing pathways. These two sensory systems also appear to play similar roles in many behavioral tasks such as prey capture, orientation with respect to external environmental cues, navigation in low-light conditions, and mediation of interactions with nearby animals. In this paper, we briefly review key morphological, physiological, and behavioral aspects of these two closely related sensory systems. We present arguments that the information processing demands associated with spatial processing are likely to be quite similar, due largely to the spatial organization of both systems and the predominantly dipolar nature of many electrosensory and mechanosensory stimulus fields. Demands associated with temporal processing may be quite different, however, due primarily to differences in the physical bases of electrosensory and mechanosensory stimuli (e.g. speed of transmission). With a better sense of the information processing requirements, we turn our attention to an analysis of the functional organization of the associated first-order sensory nuclei in the hindbrain, including the medial octavolateral nucleus (MON), dorsal octavolateral nucleus (DON), and electrosensory lateral line lobe (ELL). One common feature of these systems is a set of neural mechanisms for improving signal-to-noise ratios, including mechanisms for adaptive suppression of reafferent signals. This comparative analysis provides new insights into how the nervous system extracts biologically significant information from dipolar stimulus fields in order to solve a variety of behaviorally relevant problems faced by aquatic animals.     

Rhythmic behaviour and pattern-generating circuits in the locust: Key concepts and recent updates

There is growing recognition that rhythmic activity patterns are widespread in our brain and play an important role in all aspects of the functioning of our nervous system, from sensory integration to central processing and motor control. The study of the unique properties that enable central circuits to generate their rhythmic output in the absence of any patterned, sensory or descending, inputs, has been very rewarding in the relatively simple invertebrate preparations. The locust, specifically, is a remarkable example of an organism in which central pattern generator (CPG) networks have been suggested and studied in practically all aspects of their behaviour. Here we present an updated overview of the various rhythmic behaviours in the locust and aspects of their neural control. We focus on the fundamental concepts of multifunctional neuronal circuits, neural centre interactions and neuromodulation of CPG networks. We are certain that the very broad and solid knowledge base of locust rhythmic behaviour and pattern-generating circuits will continue to expand and further contribute to our understanding of the principles behind the functioning of the nervous system and, indeed, the brain.     

SEROTONERGIC MODULATION OF BEHAVIOUR: A PHYLOGENETIC OVERVIEW

Serotonergic neurons are present in all phyla that possess nervous systems. In most of these phyla, serotonin modulates important behaviours, including feeding, sexual and aggressive behaviour. Serotonin exerts its effects by acting in three basic modes: as a classical neurotransmitter, as a neuromodulator, or as a neurohormone. In a number of invertebrate species, the neural circuitry underlying the effects of serotonin has been well characterized, whereas in vertebrates, the mechanisms by which serotonin affects behaviour are currently less fully understood. The following review examines the role played by serotonin in the generation and modulation of behaviour in successively more complex species, ranging from coelenterates to humans.     

Aggressive biases towards similarly coloured males in Lake Malawi cichlid fishes

In haplochromine cichlids, female mate choice based on male nuptial coloration has played an important role in speciation. Recent studies suggest that male coloration strongly influences the distribution of these fishes based on male-male aggression; males direct more aggression towards similarly coloured opponents while tolerating differently coloured individuals. We explored the role of male nuptial colour in aggression among the mbuna of Lake Malawi, examining aggression by male Metriaclima mbenjii, the red top cobalt zebra, towards conspecific opponents, similarly coloured heterospecific opponents and differently coloured heterospecifics. In trials in which focal males were offered a single opponent, while the total number of aggressive behaviours did not vary among opponent species, the types of behaviours did; focal males directed more lateral displays towards conspecifics than towards the other opponent species. When focal males were offered two opponents simultaneously, M. mbenjii directed more aggressive behaviours and more lateral displays towards similarly coloured opponents, regardless of species. Furthermore, when offered a conspecific and a similarly coloured opponent simultaneously, there were no differences in behaviour towards either opponent. Thus, nuptial coloration is used by males to identify competitors, and it suggests that male-male aggression may have also been an important diversifying force in speciation in rock-dwelling Lake Malawi cichlids.     

From fish to fashion: experimental and theoretical insights into the evolution of culture

Recent years have witnessed a re-evaluation of the cognitive capabilities of fishes, including with respect to social learning. Indeed, some of the best experimental evidence for animal traditions can be found in fishes. Laboratory experimental studies reveal that many fishes acquire dietary, food site and mating preferences, predator recognition and avoidance behaviour, and learn pathways, through copying other fishes. Concentrating on foraging behaviour, we will present the findings of laboratory experiments that reveal social learning, behavioural innovation, the diffusion of novel behaviour through populations and traditional use of food sites. Further studies reveal surprisingly complex social learning strategies deployed by sticklebacks. We will go on to place these observations of fish in a phylogenetic context, describing in which respects the learning and traditionality of fish are similar to, and differ from, that observed in other animals. We end by drawing on theoretical insights to suggest processes that may have played important roles in the evolution of the human cultural capability.     

Similarities in feeding behaviour between some marine and freshwater fishes in two tropical communities

The feeding behaviour and diets of fishes in two tropical habitats, a marine reef and a freshwater pond, were studied comparatively in Brazil. Similarities were found in the tactics employed to obtain food, the social patterns during foraging, and the general diet, notwithstanding lower-level taxonomic differences between the food items. The feeding behaviours of about one-third of the fish fauna from each community were approximately equivalent. The feeding categories of these fishes are briefly described. The similarities in the feeding modes probably reflect structural and functional properties shared by the two communities. Additional behavioural similarities of fishes in both habitats are presented and the lack of some particular foraging modes in each community is noted. The picture emerged that different, unrelated fish assemblages have the ability to evolve towards a similar behavioural and structural organization in response to comparable situations and constraints. The value of underwater observations and naturalistic studies on tropical freshwater fish assemblages is indicated.     

NMDA receptors in sensory information processing.

During the past year electrophysiological studies, particularly in the visual and somatosensory systems, have begun to uncover the specific roles played by NMDA receptors in the processing of sensory information. Many of the features of NMDA-receptor-mediated sensory responses reflect known properties of the receptor.     

Peripheral and central processing of lateral line information

The lateral line is a hydrodynamic sensory system that allows fishes and aquatic amphibians to detect the water motions caused, for instance, by conspecifics, predators or prey. Typically the peripheral lateral line of fishes consists of several hundred neuromasts spread over the head, trunk, and tail fin. Lateral line neuromasts are mechanical low-pass filters that have an operating range from <1 Hz up to about 150 Hz. Within this frequency range, neuromasts encode the duration, local direction, amplitude, frequency, and phase of a hydrodynamic stimulus. This paper reviews the peripheral and central processing of lateral line information in fishes. Special attention is given to the coding of simple and complex hydrodynamic stimuli, to parallel processing, the roles of the various brain areas that process hydrodynamic information and the centrifugal (efferent) control of lateral line information. The review argues that in order to fully comprehend peripheral and central lateral line information processing, it is imperative to do comparative studies that take into account the ecology of fishes, meaning that natural stimulus and noise conditions have to be considered.