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Article

Cynthia M. Harley and Mark K. Asplen

Annelid worms are simultaneously an interesting and difficult model system for understanding the evolution of animal vision. On the one hand, a wide variety of photoreceptor cells and eye morphologies are exhibited within a single phylum; on the other, annelid phylogenetics has been substantially re-envisioned within the last decade, suggesting the possibility of considerable convergent evolution. This article reviews the comparative anatomy of annelid visual systems within the context of the specific behaviors exhibited by these animals. Each of the major classes of annelid visual systems is examined, including both simple photoreceptor cells (including leech body eyes) and photoreceptive cells with pigment (trochophore larval eyes, ocellar tubes, complex eyes); meanwhile, behaviors examined include differential mobility and feeding strategies, similarities (or differences) in larval versus adult visual behaviors within a species, visual signaling, and depth sensing. Based on our review, several major trends in the comparative morphology and ethology of annelid vision are highlighted: (1) eye complexity tends to increase with mobility and higher-order predatory behavior; (2) although they have simple sensors these can relay complex information through large numbers or multimodality; (3) polychaete larval and adult eye morphology can differ strongly in many mobile species, but not in many sedentary species; and (4) annelids exhibiting visual signaling possess even more complex visual systems than expected, suggesting the possibility that complex eyes can be simultaneously well adapted to multiple visual tasks.

Article

Nicolas Dallière, Lindy Holden-Dye, James Dillon, Vincent O'Connor, and Robert J. Walker

The microscopic free-living nematode worm Caenorhabditis elegans was the first metazoan to have its genome sequenced and for many decades has served as a genetically tractable model for the investigation of neural mechanisms of behavioral plasticity. Many of its behaviors involve the detection of its food, bacteria, which are ingested and transported to the intestine by a muscular pharynx. The structure of the pharynx and the circuitry of the pharyngeal nervous system that regulates pharyngeal activity have been described in some detail. This has provided a platform for understanding how this simple organism finely tunes its feeding behavior in response to the changing availability and quality of its food, and in the context of its own nutritional status. This resonates with fundamental principles of energy homeostasis that occur throughout the animal kingdom.

Article

James S.H. Wong and Catharine H. Rankin

The nematode, Caenorhabditis elegans (C. elegans), is an organism useful for the study of learning and memory at the molecular, cellular, neural circuitry, and behavioral levels. Its genetic tractability, transparency, connectome, and accessibility for in vivo cellular and molecular analyses are a few of the characteristics that make the organism such a powerful system for investigating mechanisms of learning and memory. It is able to learn and remember across many sensory modalities, including mechanosensation, chemosensation, thermosensation, oxygen sensing, and carbon dioxide sensing. C. elegans habituates to mechanosensory stimuli, and shows short-, intermediate-, and long-term memory, and context conditioning for mechanosensory habituation. The organism also displays chemotaxis to various chemicals, such as diacetyl and sodium chloride. This behavior is associated with several forms of learning, including state-dependent learning, classical conditioning, and aversive learning. C. elegans also shows thermotactic learning in which it learns to associate a particular temperature with the presence or absence of food. In addition, both oxygen preference and carbon dioxide avoidance in C. elegans can be altered by experience, indicating that they have memory for the oxygen or carbon dioxide environment they were reared in. Many of the genes found to underlie learning and memory in C. elegans are homologous to genes involved in learning and memory in mammals; two examples are crh-1, which is the C. elegans homolog of the cAMP response element-binding protein (CREB), and glr-1, which encodes an AMPA glutamate receptor subunit. Both of these genes are involved in long-term memory for tap habituation, context conditioning in tap habituation, and chemosensory classical conditioning. C. elegans offers the advantage of having a very small nervous system (302 neurons), thus it is possible to understand what these conserved genes are doing at the level of single identified neurons. As many mechanisms of learning and memory in C. elegans appear to be similar in more complex organisms including humans, research with C. elegans aids our ever-growing understanding of the fundamental mechanisms of learning and memory across the animal kingdom.

Article

Douglas K. Reilly and Jagan Srinivasan

To survive, animals must properly sense their surrounding environment. The types of sensation that allow for detecting these changes can be categorized as tactile, thermal, aural, or olfactory. Olfaction is one of the most primitive senses, involving the detection of environmental chemical cues. Organisms must sense and discriminate between abiotic and biogenic cues, necessitating a system that can react and respond to changes quickly. The nematode, Caenorhabditis elegans, offers a unique set of tools for studying the biology of olfactory sensation. The olfactory system in C. elegans is comprised of 14 pairs of amphid neurons in the head and two pairs of phasmid neurons in the tail. The male nervous system contains an additional 89 neurons, many of which are exposed to the environment and contribute to olfaction. The cues sensed by these olfactory neurons initiate a multitude of responses, ranging from developmental changes to behavioral responses. Environmental cues might initiate entry into or exit from a long-lived alternative larval developmental stage (dauer), or pheromonal stimuli may attract sexually mature mates, or repel conspecifics in crowded environments. C. elegans are also capable of sensing abiotic stimuli, exhibiting attraction and repulsion to diverse classes of chemicals. Unlike canonical mammalian olfactory neurons, C. elegans chemosensory neurons express more than one receptor per cell. This enables detection of hundreds of chemical structures and concentrations by a chemosensory nervous system with few cells. However, each neuron detects certain classes of olfactory cues, and, combined with their synaptic pathways, elicit similar responses (i.e., aversive behaviors). The functional architecture of this chemosensory system is capable of supporting the development and behavior of nematodes in a manner efficient enough to allow for the genus to have a cosmopolitan distribution.

Article

Simona Candiani and Mario Pestarino

The central and peripheral nervous systems of amphioxus adults and larvae are characterized by morphofunctional features relevant to understanding the origins and evolutionary history of the vertebrate CNS. Classical neuroanatomical studies are mainly on adult amphioxus, but there has been a recent focus, both by TEM and molecular methods, on the larval CNS. The latter is small and remarkably simple, and new data on the localization of glutamatergic, GABAergic/glycinergic, cholinergic, dopaminergic, and serotonergic neurons within the larval CNS are now available. In consequence, it has been possible begin the process of identifying specific neuronal circuits, including those involved in controlling larval locomotion. This is especially useful for the insights it provides into the organization of comparable circuits in the midbrain and hindbrain of vertebrates. A much better understanding of basic chordate CNS organization will eventually be possible when further experimental data will emerge.

Article

Z. Yan Wang and Clifton W. Ragsdale

Over 700 species of cephalopods live in the Earth’s waters, occupying almost every marine zone, from the benthic deep to the open ocean to tidal waters. The greatly varied forms and charismatic behaviors of these animals have long fascinated humans. Cephalopods are short-lived, highly mobile predators with sophisticated brains that are the largest among the invertebrates. While cephalopod brains share a similar anatomical organization, the nervous systems of coleoids (octopus, squid, cuttlefish) and nautiloids all display important lineage-specific neural adaptations. The octopus brain, for example, has for its arms a well-developed tactile learning and memory system that is vestigial in, or absent from, that of other cephalopods. The unique anatomy of the squid giant fiber system enables rapid escape in the event of capture. The brain of the nautilus comprises fewer lobes than its coleoid counterparts, but contains olfactory system structures and circuits not yet identified in other cephalopods.

Article

Anna Di Cosmo and Gianluca Polese

Within the Phylum Mollusca, cephalopods encompass a small and complex group of exclusively marine animals that live in all the oceans of the world with the exception of the Black and Caspian seas. They are distributed from shallow waters down into the deep sea, occupying a wide range of ecological niches. They are dominant predators and themselves prey with high visual capability and well-developed vestibular, auditory, and tactile systems. Nevertheless, their perceptions are chemically facilitated, so that water-soluble and volatile odorants are the key mediators of many physiological and behavioral events. For cephalopods as well as the other aquatic animals, chemical cues convey a remarkable amount of information critical to social interaction, habitat selection, defense, prey localization, courtship and mating, affecting not only individual behavior and population-level processes, but also community organization and ecosystem function. Cephalopods possess chemosensory systems that have anatomical similarities to the olfactory systems of land-based animals, but the molecules perceived from distance are different because their water solubility is of importance. Many insoluble molecules that are detected from distance on land must, in an aquatic system, be perceived by direct contact with the odour source. Most of the studies regarding olfaction in cephalopods have been performed considering only waterborne molecules detected by the “olfactory organs.” However cephalopods are also equipped with “gustatory systems” consisting of receptors distributed on the arm suckers in octopods, buccal lips in decapods, and tentacles in nautiluses. To date, what is known about the olfactory organ in cephalopods comes from studies on nautiloids and coleoids (decapods and octopods). In the nautiloid’s olfactory system, there is a pair of rhinophores located below each eye and open to the environment with a tiny pore, whereas in coleoids a small pit of ciliated cells is present on either side of the head below the eyes close to the mantle edge.

Article

Donald Edwards

Crayfish are decapod crustaceans that use different forms of escape to flee from different types of predatory attacks. Lateral and Medial Giant escapes are released by giant interneurons of the same name in response to sudden, sharp attacks from the rear and front of the animal, respectively. A Lateral Giant (LG) escape uses a fast rostral abdominal flexion to pitch the animal up and forward at very short latency. It is succeeded by guided swimming movements powered by a series of rapid abdominal flexions and extensions. A Medial Giant (MG) escape uses a fast, full abdominal flexion to thrust the animal directly backward, and is also followed by swimming that moves the animal rapidly away from the attacker. More slowly developing attacks evoke Non-Giant (NG) escapes, which have a longer latency, are varied in the form of abdominal flexion, and are directed initially away from the attacker. They, too, are followed by swimming away from the attacker. The neural circuitry for LG escape has been extensively studied and has provided insights into the neural control of behavior, synaptic integration, coincidence detection, electrical synapses, behavioral and synaptic plasticity, neuroeconomical decision-making, and the modulatory effects of monoamines and of changes in the animal’s social status.

Article

Charles Derby and Manfred Schmidt

Olfaction is a chemical sense present not only in mammals, insects, and other terrestrial animals, but also in crustaceans, most of which are aquatic. Crustaceans use olfaction for detecting and responding in appropriate ways to chemicals relevant to most ecological contexts, including: environmental cues indicating quality of food, habitat, and location; interspecies cues indicating presence of predators and competitors; and intraspecific signals indicating social status of conspecifics and presence of possible mating partners. Olfaction is only one of the chemical senses of crustaceans, being distinguished based on anatomical and functional features of the sensory neurons detecting the chemicals and the pathways within the central nervous system that processes this information.

Article

Daniel Tomsic and Julieta Sztarker

Decapod crustaceans, in particular semiterrestrial crabs, are highly visual animals that greatly rely on visual information. Their responsiveness to visual moving stimuli, with behavioral displays that can be easily and reliably elicited in the laboratory, together with their sturdiness for experimental manipulation and the accessibility of their nervous system for intracellular electrophysiological recordings in the intact animal, make decapod crustaceans excellent experimental subjects for investigating the neurobiology of visually guided behaviors. Investigations of crustaceans have elucidated the general structure of their eyes and some of their specializations, the anatomical organization of the main brain areas involved in visual processing and their retinotopic mapping of visual space, and the morphology, physiology, and stimulus feature preferences of a number of well-identified classes of neurons, with emphasis on motion-sensitive elements. This anatomical and physiological knowledge, in connection with results of behavioral experiments in the laboratory and the field, are revealing the neural circuits and computations involved in important visual behaviors, as well as the substrate and mechanisms underlying visual memories in decapod crustaceans.

Article

Quentin Gaudry and Jonathan Schenk

Olfactory systems are tasked with converting the chemical environment into electrical signals that the brain can use to optimize behaviors such as navigating towards resources, finding mates, or avoiding danger. Drosophila melanogaster has long served as a model system for several attributes of olfaction. Such features include sensory coding, development, and the attempt to link sensory perception to behavior. The strength of Drosophila as a model system for neurobiology lies in the myriad of genetic tools made available to the experimentalist, and equally importantly, the numerical reduction in cell numbers within the olfactory circuit. Modern techniques have recently made it possible to target nearly all cell types in the antennal lobe to directly monitor their physiological activity or to alter their expression of endogenous proteins or transgenes.

Article

Carlos A. Díaz-Balzac and José E. García-Arrarás

The nervous system of echinoderms has been studied for well over a century. Nonetheless, the information available is disparate, with in-depth descriptions for the nervous component of some groups or of particular organs while scant data is available for others. The best studied representatives to date are the nervous system of echinoid embryos and larva, and the adult holothurian nervous system. Although described sometimes inaccurately as a neural net, the echinoderm nervous system consists of well-defined neural structures. This is observed since early embryogenesis when activation of the anterior neuroectoderm gene regulatory networks initiate the formation of the embryonic nervous system. This system then undergoes expansion and differentiation to form the larval nervous system, which is centered on the ciliary bands. This “simpler” nervous system is then metamorphosed into the adult echinoderm nervous system. The adult echinoderm nervous system is composed of a central nervous system made up of a nerve ring connected to a series of radial nerve cords. Peripheral nerves extending from the radial nerve cords or nerve ring connect with the peripheral nervous system, located in other organs or effectors including the viscera, podia, body wall muscles, and connective tissue. Both the central and peripheral nervous systems are composed of complex and diverse subdivisions. These are mainly characterized by the expression of neurotransmitters, namely acetylcholine, catecholamines, histamine, amino acids, GABA, and neuropeptides. Other areas of interest include the amazing regenerative capabilities of echinoderms that have been shown to be able to regenerate their nervous system components; and the analysis of the echinoderm genome that has provided essential insights into the molecular basis of how echinoderms develop an adult pentaradial symmetry from bilaterally symmetric larvae and the role of the nervous system in this process.

Article

Although the Cnidaria have evolved a wide range of body forms matched with an equally varied neural anatomy, individual species exhibit common patterns of behavior. For example, in all species a key challenge for the nervous system is to transfer food from the peripherally mounted tentacles to the centrally located stomach. Foraging movements, necessary to maintain the food supply, must be accomplished in such a way as to avoid interference with the primary objective of getting prey into the mouth. Furthermore, the hunt for prey must be balanced by a measured response to “threat.” Different species respond to threat in markedly different ways, but in each case foraging is inhibited, just as it is during transmission of food. One hundred years ago, G. H. Parker questioned whether a centralized or a locally organized nervous system could best account for sea anemone behavior. Anatomical and electrophysiological studies now suggest that in most Cnidaria there is a degree of hierarchical control, with local reflexes coordinated by more condensed systems of neurons. This organization is highly developed in the nerve rings of hydrozoan medusae and takes the form of ganglion-like rhopalia in the Cubozoa. Even in hydrozoan polyps such as Hydra there are at least four separate neuronal systems. It is likely that the underlying mechanisms (containing both homologous and analogous elements) will be best revealed by a comparative approach that directly relates behavior with its molecular basis. Useful examples include comparisons between sea anemones with and without through-conducting systems; between hydra with and without oral rings; between medusae with and without coordinated escape swimming. Recent advances in transgenomic labeling have shown the way forward.

Article

It is conceptually reasonable to explore how the evolution of behavior involves changes in neural circuitry. Progress in determining this evolutionary relationship has been limited in neuroscience because of difficulties in identifying individual neurons that contribute to the evolutionary development of behaviors across species. However, the results from the feeding systems of gastropod mollusks provide evidence for this concept of co-evolution because the evolution of different types of feeding behaviors in this diverse group of mollusks is mirrored by species-specific changes in neural circuitry. The evolution of feeding behaviors involves changes in the motor actions that allow diverse food items to be acquired and ingested. The evolution in neural control accompanies this variation in food and the associated changes in flexibility of feeding behaviors. This is present in components of the feeding network that are involved in decision making, rhythm generation, and behavioral switching but is absent in background mechanisms that are conserved across species, such as those controlling arousal state. These findings show how evolutionary changes, even at the single neuron level, closely reflect the details of behavioral evolution.

Article

Euopisthobranchia (Aplysia), Nudipleura (Tritonia, Hermissenda, Pleurobranchaea), and Panpulmonata (Lymnaea, Helix, Limax) gastropod mollusks exhibit a variety of reflex, rhythmic, and motivated behaviors that can be modified by elementary forms of learning and memory. The relative simplicity of their nervous systems and behavioral repertoires has allowed the uncovering of processes of neuronal and synaptic plasticity underlying non-associative learning, such as habituation, sensitization, and different forms of associative learning, such as classical and operant conditioning. Decades of work on these simpler and accessible animal systems have almost uniquely yielded an understanding into the mechanistic basis of learning and memory spanning behavior, neuronal circuitry, and molecules. Given the conservative nature of evolutionary processes, the mechanisms deciphered have also provided valuable insights into the neural basis of learning and memory in other metazoans, including higher vertebrates.

Article

Norio Miyamoto and Hiroshi Wada

Hemichordates are marine invertebrates consisting of two distinct groups: the solitary enteropneusts and the colonial pterobranchs. Hemichordates are phylogenetically a sister group to echinoderm composing Ambulacraria. The adult morphology of hemichordates shares some features with chordates. For that reason, hemichordates have been considered key organisms to understand the evolution of deuterostomes and the origin of the chordate body plan. The nervous system of hemichordates is also important in the discussion of the origin of centralized nervous systems. However, unlike other deuterostomes, such as echinoderms and chordates, information on the nervous system of hemichordates is limited. Recent improvements in the accessibility of embryos, development of functional tools, and genomic resources from several model organisms have provided essential information on the nervous system organization and neurogenesis in hemichordates. The comparison of the nervous system between hemichordates and other bilaterians helps to elucidate the origin of the chordate central nervous system. Extant hemichordates are divided into two groups: enteropneusts and pterobranchs. The nervous system of adult enteropneusts consists of nerve cords and the basiepidermal nerve net. The two nerve cords run along the dorsal and ventral midlines. The dorsal nerve cord forms a tubular structure in the collar region. The two nerve cords are connected through the prebranchial nerve ring. The larval nervous system of enteropneusts develops along the ciliary band and there is a ganglion at the anterior end of the body called the apical ganglion. A pair of pigmented eyespots is situated at the lateral side of the apical ganglion. The adult nervous system of pterobranchs is basiepidermal and there are several condensations of plexuses. The most prominent one is the brain, located at the base of the tentaculated arms. From the brain, small fibers radiate and enter tentaculated arms to form a tentacle nerve in each. There is a basiepidermal nerve cord in the ventral midline of the trunk.

Article

Navigation is the ability of animals to move through their environment in a planned manner. Different from directed but reflex-driven movements, it involves the comparison of the animal’s current heading with its intended heading (i.e., the goal direction). When the two angles don’t match, a compensatory steering movement must be initiated. This basic scenario can be described as an elementary navigational decision. Many elementary decisions chained together in specific ways form a coherent navigational strategy. With respect to navigational goals, there are four main forms of navigation: explorative navigation (exploring the environment for food, mates, shelter, etc.); homing (returning to a nest); straight-line orientation (getting away from a central place in a straight line); and long-distance migration (seasonal long-range movements to a location such as an overwintering place). The homing behavior of ants and bees has been examined in the most detail. These insects use several strategies to return to their nest after foraging, including path integration, route following, and, potentially, even exploit internal maps. Independent of the strategy used, insects can use global sensory information (e.g., skylight cues), local cues (e.g., visual panorama), and idiothetic (i.e., internal, self-generated) cues to obtain information about their current and intended headings. How are these processes controlled by the insect brain? While many unanswered questions remain, much progress has been made in recent years in understanding the neural basis of insect navigation. Neural pathways encoding polarized light information (a global navigational cue) target a brain region called the central complex, which is also involved in movement control and steering. Being thus placed at the interface of sensory information processing and motor control, this region has received much attention recently and emerged as the navigational “heart” of the insect brain. It houses an ordered array of head-direction cells that use a wide range of sensory information to encode the current heading of the animal. At the same time, it receives information about the movement speed of the animal and thus is suited to compute the home vector for path integration. With the help of neurons following highly stereotypical projection patterns, the central complex theoretically can perform the comparison of current and intended heading that underlies most navigation processes. Examining the detailed neural circuits responsible for head-direction coding, intended heading representation, and steering initiation in this brain area will likely lead to a solid understanding of the neural basis of insect navigation in the years to come.

Article

Nathaniel J. Himmel, Atit A. Patel, and Daniel N. Cox

Nociception is a protective mechanism that mediates behavioral responses to a range of potentially damaging stimuli, including noxious temperature, chemicals, and mechanical stimulation. Nociceptive mechanisms are found throughout metazoans. Noxious stimuli are transduced by specialized, high-threshold peripheral nociceptors, which fire action potentials to elicit adaptive behavioral responses. Nociception is essential for survival and provides a mechanism for sensory perception of noxious stimuli, which alerts the organism to potential environmental dangers. When coupled with pain sensation and complex behavioral responses, this mechanism protects the organism from incipient damage. Moreover, acute and chronic pain may manifest as altered nociception in neuropathic pain states. Elucidating the neural bases of nociception is therefore important for identifying and implementing novel strategies for the treatment of neuropathic pain, as well as uncovering the mechanistic bases by which the nervous system integrates information to produce specific behaviors in response to a range of noxious stimuli. Invertebrate organisms, such as Drosophila melanogaster and Caenorhabditis elegans, have emerged as powerful, genetically tractable platforms for exploring these questions. Here, we concisely review the current state of knowledge regarding the cells, molecules, neural circuits, and behaviors associated with invertebrate nociception in the fruit fly and nematode worm.

Article

Richard Satterlie

Two dichotomies exist within the swim systems of jellyfish—one centered on the mechanics of locomotion and the other on phylogenetic differences in nervous system organization. For example, medusae with prolate body forms use a jet propulsion mechanism, whereas medusae with oblate body forms use a drag-based marginal rowing mechanism. Independent of this dichotomy, the nervous systems of hydromedusae are very different from those of scyphomedusae and cubomedusae. In hydromedusae, marginal nerve rings contain parallel networks of neurons that include the pacemaker network for the control of swim contractions. Sensory structures are similarly distributed around the margin. In scyphomedusae and cubomedusae, the swim pacemakers are restricted to marginal integration centers called rhopalia. These ganglionlike structures house specialized sensory organs. The swim system adaptations of these three classes (Hydrozoa, Scyphozoa, and Cubozoa), which are constrained by phylogenetics, still adhere to the biomechanical efficiencies of the prolate/oblate dichotomy. This speaks to the adaptational abilities of the cnidarian nervous system as specialized in the medusoid forms.

Article

William B. Kristan Jr.

New techniques for recording the activity of many neurons simultaneously have given insights into how neuronal circuits make the decision to perform one of many possible behaviors. A long-standing hypothesis for how behavioral choices are made in any animal is that “command neurons” are responsible for selecting individual behaviors, and that these same neurons inhibit the command neurons that elicit other behaviors. In fact, this mechanism has turned out to be just one of several ways that such decision-making is accomplished. In particular, for some behavioral choices, the circuits appear to overlap, sometimes extensively, to perform two or more behaviors. Making decisions using such “multifunctional neurons” has been proposed for large neural networks, but this strategy appears to be used in relatively small nervous systems, too. These simpler nervous systems can serve as useful test systems to test hypotheses about how the dynamics of networks of neurons can be used to select among different behaviors, similar to the mechanisms used by leeches deciding to swim, shorten, crawl, or feed.