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Article

Nir Nesher, Guy Levy, Letizia Zullo, and Benyamin Hochner

The octopus, with its eight long and flexible arms, is an excellent example of the independent evolution of highly efficient motor behavior in a soft-bodied animal. Studies will be summarized to show that the amazing behavioral motor abilities of the octopus are achieved through a special embodied organization of its flexible body, unusual morphology, and a unique central and peripheral distribution of its extremely large nervous system. This special embodied organization of brain–body–environment reciprocal interactions makes it possible to overcome the difficulties involved in generation and control of movement in an animal, which unlike vertebrates and arthropods lacks rigid skeletal appendages.

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

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

Chuan-Chin Chiao and Roger T. Hanlon

Visual camouflage change is a hallmark of octopus, squid, and cuttlefish and serves as their primary defense against predators. They can change their total body appearance in less than a second due to one principal feature: every aspect of this sensorimotor system is neurally refined for speed. Cephalopods live in visually complex environments such as coral reefs and kelp forests and use their visual perception of backgrounds to rapidly decide which camouflage pattern to deploy. Counterintuitively, cuttlefish have evolved a small number of pattern designs to achieve camouflage: Uniform, Mottle, and Disruptive, each with variation. The expression of these body patterns is based on several fundamental scene features. In cuttlefish, there appear to be several “visual assessment shortcuts” that enable camouflage patterning change in as little as 125 milliseconds. Neural control of the dynamic body patterning of cephalopods appears to be organized hierarchically via a set of lobes within the brain, including the optic lobes, the lateral basal lobes, and the anterior/posterior chromatophore lobes. The motor output of the central nervous system (CNS) in terms of the skin patterns that are produced is under sophisticated neural control of chromatophores, iridophores, and three-dimensional skin papillae. Moreover, arm postures and skin papillae are also regulated visually for additional aspects of concealment. This coloration system, often referred to as rapid neural polyphenism, is unique in the animal kingdom and can be explained and interpreted in the context of sensory and behavioral ecology.

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

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

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

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

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

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.