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.
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.
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.
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.
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.
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.
Brian D. Burrell
The medicinal leech (Hirudo verbana) is an annelid (segmented worm) and one of the classic model systems in neuroscience. It has been used in research for over 50 years and was one of the first animals in which intracellular recordings of mechanosensory neurons were carried out. Remarkably, the leech has three main classes of mechanosensory neurons that exhibit many of the same properties found in vertebrates. The most sensitive of these neurons are the touch cells, which are rapidly adapting neurons that detect low-intensity mechanical stimuli. Next are the pressure cells, which are slow-adapting sensory neurons that respond to higher intensity, sustained mechanostimulation. Finally, there are nociceptive neurons, which have the highest threshold and respond to potentially damaging mechanostimuli, such as a pinch. As observed in mammals, the leech has separate mechanosensitive and polymodal nociceptors, the latter responding to mechanical, thermal, and chemical stimuli. The cell bodies for all three types of mechanosensitive neurons are found in the central nervous system where they are arranged as bilateral pairs. Each neuron extends processes to the skin where they form discrete receptive fields. In the touch and pressure cells, these receptive fields are arranged along the dorsal-ventral axis. For the mechano-only and polymodal nociceptive neurons, the peripheral receptive fields overlap with the mechano-only nociceptor, which also innervates the gut. The leech also has a type of mechanosensitive cell located in the periphery that responds to vibrations in the water and is used, in part, to detect potential prey nearby.
In the central nervous system, the touch, pressure, and nociceptive cells all form synaptic connections with a variety of motor neurons, interneurons, and even each other, using glutamate as the neurotransmitter. Synaptic transmission by these cells can be modulated by a variety of activity-dependent processes as well as the influence of neuromodulatory transmitters, such as serotonin. The output of these sensory neurons can also be modulated by conduction block, a process in which action potentials fail to propagate to all the synaptic release sites, decreasing synaptic output. Activity in these sensory neurons leads to the initiation of a number of different motor behaviors involved in locomotion, such as swimming and crawling, as well as behaviors designed to recoil from aversive/noxious stimuli, such as local bending and shortening. In the case of local bending, the leech is able to bend in the appropriate direction away from the offending stimuli. It does so through a combination of which mechanosensory cell receptive fields have been activated and the relative activation of multiple sensory cells decoded by a layer of downstream interneurons.
Thomas F. Mathejczyk and Mathias F. Wernet
Evolution has produced vast morphological and behavioral diversity amongst insects, including very successful adaptations to a diverse range of ecological niches spanning the invasion of the sky by flying insects, the crawling lifestyle on (or below) the earth, and the (semi-)aquatic life on (or below) the water surface. Developing the ability to extract a maximal amount of useful information from their environment was crucial for ensuring the survival of many insect species. Navigating insects rely heavily on a combination of different visual and non-visual cues to reliably orient under a wide spectrum of environmental conditions while avoiding predators. The pattern of linearly polarized skylight that results from scattering of sunlight in the atmosphere is one important navigational cue that many insects can detect. Here we summarize progress made toward understanding how different insect species sense polarized light. First, we present behavioral studies with “true” insect navigators (central-place foragers, like honeybees or desert ants), as well as insects that rely on polarized light to improve more “basic” orientation skills (like dung beetles). Second, we provide an overview over the anatomical basis of the polarized light detection system that these insects use, as well as the underlying neural circuitry. Third, we emphasize the importance of physiological studies (electrophysiology, as well as genetically encoded activity indicators, in Drosophila) for understanding both the structure and function of polarized light circuitry in the insect brain. We also discuss the importance of an alternative source of polarized light that can be detected by many insects: linearly polarized light reflected off shiny surfaces like water represents an important environmental factor, yet the anatomy and physiology of underlying circuits remain incompletely understood.
The crustacean stomatogastric nervous system contains a set of distinct but interacting rhythmic motor circuits that control movements of the foregut. When isolated, these circuits produce activity patterns that are almost perfect replicas of their behavior in vivo. The ease with which distinct circuit neurons are identified, recorded, and manipulated has provided considerable insight into the general principles of how motor circuits operate and are controlled at the cellular level. The small number of relatively large neurons has facilitated several technical advances in neuroscience research and allowed the identification of one of the earliest circuit connectomes. This enabled, for the first time, studies of circuit dynamics using the relationships between all component neurons of a nervous center. A major discovery was that circuits are not dedicated to producing a single neuronal activity pattern, and that the involved neurons are not committed to particular circuits. This flexibility results predominantly from the ability of neuromodulators to change the cellular and synaptic properties of circuit neurons. The relatively unique access to, and detailed documentation of, identified circuit, sensory, and descending pathways has also started new avenues into examining how individual modulatory neurons and transmitters affect their target cells. Groundbreaking experimental and modeling work has further demonstrated that the intrinsic properties of neurons depend on their recent history of activation and that neurons and circuits counterbalance destabilizing influences by compensatory homeostatic regulation of ionic conductances. The stomatogastric microcircuits continue to provide key insight into neural circuit operation in numerically larger and less accessible systems.
Thomas W. Cronin, N. Justin Marshall, and Roy L. Caldwell
The predatory stomatopod crustaceans, or mantis shrimp, are among the most attractive and dynamic creatures living in the sea. Their special features include their powerful raptorial appendages, used to kill, stun, or disable other animals (whether predators, prey, or competitors), and their highly specialized compound eyes. Mantis shrimp vision is unlike that of any other animal and has several unique features. Their compound eyes are optically triple, each having three separate regions that produce overlapping visual fields viewing certain regions of space. They have the most diverse set of spectral classes of receptors ever described in animals, with as many as 16 types in a single compound eye. These receptors are based on a highly duplicated set of opsin molecules paired with strongly absorbing photostable filters in some photoreceptor types. The receptor set includes six ultraviolet types, all spectrally distinct, many themselves tuned by photostable filters. There are as many as eight types of polarization receptors of up to three spectral classes (including an ultraviolet class). In some species, two sets of these receptors analyze circularly polarized light, another unique capability. Stomatopod eyes move independently, each capable of visual field stabilization, image foveation and tracking, or scanning of image features. Stomatopods are known to recognize colors and polarization features and evidently use these in predation and communication. Altogether, mantis shrimps have perhaps the most unusual vision of any animal.
Kerrianne Ryan and Ian A. Meinertzhagen
Urochordates are chordate siblings that comprise the following marine invertebrates: the sessile Ascidiaceae, or sea squirts; planktonic Larvacea; and the pelagic salps, doliolids, and pyrosomes (collectively the Thaliacea), each more beautiful than the next. Tadpole larvae of ascidians and adult larvaceans both have a body plan that is chordate, with a notochord and dorsal, tubular nervous system that forms from a neural plate. Thalaciacea have a ganglion developed from a tubular structure, which has been compared to the vertebrate mes-metencephalic region, and while salps have well developed eyes, other anterior brain components are absent, and the connections within their central nervous system, as well as the neurobiology of other Thaliacea are all little reported. The ascidian tadpole larva is extensively reported, especially in the model species Ciona intestinalis, as is the caudal nerve cord in the larvacean Oikopleura dioica.
Chordate features that share proposed homology with vertebrate features include ciliary photoreceptors that hyperpolarize to light, descending decussating motor pathways that resemble Mauthner cell pathways, coronet cells in the ascidian larva and saccus vasculosus of fishes, the neural canal’s Reissner’s fiber; secondary mechanoreceptors that resemble hair cells; and ascidian bipolar cells that are like dorsal root ganglion cells.