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.
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.
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.
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.
Pedro Martínez, Volker Hartenstein, and Simon G. Sprecher
The emergence and diversification of bilateral animals are among the most important transitions in the history of life on our planet. A proper understanding of the evolutionary process will derive from answering such key questions as, how did complex body plans arise in evolutionary time, and how are complex body plans “encoded” in the genome? the first step is focusing on the earliest stages in bilaterian evolution, probing the most elusive organization of the genomes and microscopic anatomy in basally branching taxa, which are currently assembled in a clade named Xenacoelomorpha. This enigmatic phylum is composed of three major taxa: acoel flatworms, nemertodermatids, and xenoturbellids. Interestingly, the constituent species of this clade have an enormously varied set of morphologies; not just the obvious external features but also their tissues present a high degree of constructional variation. This interesting diversity of morphologies (a clear example being the nervous system, with animals showing different degrees of compaction) provides a unique system in which to address outstanding questions regarding the parallel evolution of genomes and the many morphological characters encoded by them. A systematic exploration of the anatomy of members of these three taxa, employing immunohistochemistry, in situ hybridization, and high-throughput transmission electron microscopy, will provide the reference framework necessary to understand the changing roles of genes and gene networks during the evolution of xenacoelomorph morphologies and, in particular, of their nervous systems.
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.
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.
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.
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.
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.