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.
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.
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.
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.
Z. Yan Wang and Clifton W. Ragsdale
This is an advance summary of a forthcoming article in the Oxford Research Encyclopedia of Neuroscience. Please check back later for the full article.
Cephalopod molluscs have the largest invertebrate nervous systems and demonstrate a commensurate repertoire of behaviors, including a sophisticated and extremely rapid adaptive coloration system, extraordinary facility in problem solving, and dramatic visually guided predation capabilities. These complex behaviors have long fascinated humans, and have spurred over a century of research on cephalopod nervous systems.
Extant cephalopods are morphologically diverse and can be divided into the nautiloids, which retain an external shell; and the coleoids, which include octopus, squid, and cuttlefish. Despite their divergence ~400 mya, nautiloids and coleoids share some underlying organizational principles and anatomical features in their nervous systems, including central brain masses situated around the esophagus flanked by a pair of optic lobes. The soft-bodied coleoid cephalopods have, however, developed many striking innovations, such as chemosensory suckers that line the arms, dozens of sharply distinguished lobes within the central brain, and a pair of neuroendocrine organs called the optic gland. Recent developments in cephalopod biology, including the availability of the octopus genome, have led to new insights into cephalopod nervous system organization, including the striking finding that the functional convergence of the cephalopod nervous system with that of vertebrates is paralleled by convergence at the molecular level.
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.
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.
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.
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.
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.