Sensory Systems/Nematodes

Caenorhabditis elegans
C.elegans (Caenorhabditis elegans) is a transparent non-parasitic nematode (or roundworm) that is used as a eukaryotic model organism especially to study developmental biology. Its small size (~1.5 mm long), rapid life cycle (3 days) and easy laboratory cultivation make it a very suitable animal to work with in research.

Anatomy
The genome of C.elegans comprises six chromosomes, five autosomes and one sex chromosome, with a total size of ~100 million base pairs. Although being 20 times smaller than the human genome, it contains a similar amount of genes (~20'000) with 35% being human homologs. The tissues present in this worm are much like the ones found in higher order animals and humans but in a simplified form: nervous system, gastrointestinal tract, epidermis, muscles, and gonads are present but not a respiratory or a circulatory tract.

There are two forms of sex in the nematode: a male form with only one sex chromosome (indicated by XO) and a hermaphrodite form with two sex chromosomes (XX). The hermaphrodite is a self-fertile organism which is able to create self-progeny by internal fertilization. In case of harsh conditions, larvae enter into a type of stasis called Dauer, which allows them to survive. The decision to enter into this state is influenced by temperature, food supply, levels of dauer-inducing pheromone, and population density.

Many species of nematodes are eutelic, which means that they reach maturity with a fixed amount of genetically predetermined somatic cells. For instance, C.elegans hermaphrodites consist of 959 cells and males of 1'031 cells. These cells are generated through an invariant cell lineage. Today, the developmental fate of every single somatic cell has been mapped, such that it is possible to predict the differentiation pattern of each cell during embryogenesis.

Nervous System
C.elegans is one of the simplest organisms with a nervous system. The nervous system is reproducible at a cellular level since neurons have simple branching structures and both the disposition of cell processes, and the connections they make, appear to be largely invariant between animals.

The adult hermaphrodite has 302 neurons that belong to two distinct nervous systems: a somatic nervous system (282 neurons) and a pharyngeal nervous system (20 neurons). The adult male has 83 neurons more than the hermaphrodite, but most of them are involved in mating behavior. Neurons have been assigned to 118 classes according to their topology and synaptic connection patterns and fall into four categories defined by their circuitry: motor neurons, sensory neurons, interneurons, and plolymodal neurons; most of the cell bodies are located either in the head or the tail and communicate through approximately 6'400 synapses, 900 gap junctions, and 1'500 neuromuscular junctions.

Every C.elegans neuron has been named, each name consists of either two or three uppercase letters indicating the class and, in some cases, a number indicating the neuron number within one class. If the neurons are radially symmetrical, each cell has a three-letter name followed by L (left), R (right), D (dorsal), or V (ventral) ; for example, ALML and ALMR are the left and right anterior lateral microtubule neurons.

Sensory System
C.elegans moves and explores its environment by chemotaxis (movement in response to a chemical stimulus), aerotaxis (movement in response to molecular oxygen), and thermotaxis (movement in response to temperature). Other sensory information is taken up by mechanical stimuli. Behavior is adapted to the nature of the stimuli: moving towards favorable and escaping from harmful environments. The perception of environmental cues is accomplished through 24 sensillar organs and various isolated sensory neurons. Sensillar neurons perform all the sensory functions except for oxygen sensing and some types of mechanosensation, which are performed by non-sensillar neurons.

Sensilla
Sensilla are simple epithelial sense organ composed of one or a few cells with a nerve connection and usually taking the form of a spine, plate, rod, cone or peg .Sensillar organs are divided into 7 groups: amphid, cephalic, inner labial, outer labial, anterior deirid, posterior deirid, and phasmid sensilla. Each type of sensillum has a different structure, although the cell types that compose them are the same. Sheath and socket cells enclose and protect the sensillar endings and are considered glia cells. In one individual organism, there are 24 sheath cells and 26 socket cells in total. Unlike in higher organisms, glia cells do not form myelin in C.elegans.

The amphids are the two largest chemosensory organs, they are innervated invaginations of cuticle located in the head, open to the outside at the sides of the lips. Each amphid includes 12 sensory neurons.

Each cephalic sensillum is positioned to a counterpart outer labial quadrant (OLQ) sensillum in the lips and contains the dendrites of one of the four cephalic neurons (CEP). CEP neurons are dopaminergic and are suggested to be texture sensing (mechanosensation).

Inner labial sensilla are six symmetrically arranged sensilla placed at the apex of each lip. They are innervated by mechanosensory neurons in order to perform head withdrawal in response to nose touching and by chemosensory neurons.

Outer labial sensilla are also six and are placed posterior to the inner labial sensilla. They are innervated by mechanosensory neurons.

Anterior and posterior deirid are innervated by dopaminergic neurons. They are bilaterally paired and are involved in mechanical texture sensation. Anterior deirid sensilla are located at the posterior of the head, whereas posterior deirid sensilla are located halfway between the vulva and the tail.

Phasmids are similar to amphids and are located at the lateral sides of the tail, behind the rectum. Phasmids are mostly involved in avoidance behavior.

(A list of neuronal support cells and a list of sensory receptors, along with the associated neurons and corresponding activity is placed at the end of the chapter)

Mechanosensation
Mechanical stimuli sensed by C.elegans can be divided into different types of stimuli: gentle body touch, harsh body touch, gentle nose touch, harsh nose touch, texture sensation, and proprioception. Receptors are classified according to their cytoskeletal specialization: mechanoceptors with ciliated sensory endings, touch receptor neurons containing large-diameter, 15-protofilament microtubules (also called MT cells), and neurons with processes containing synapse-free stretches and undifferentiated cytoskeletons.

Mechanosensory neurons detect force through mechanically-gated ion channels which produce touch- or stretch-evoked currents.

Thermosensation
C.elegans can detect temperatures which are favorable to its survival, that is in the range of ~12-27°C. Individual organisms can associate a determined temperature with a favorable environment (e.g. food abundance) and preferably move towards environments with similar temperatures. Thermosensors are placed in the head amphids and are composed by three types of neurons (AFD, AWC, ASI), with AFD being the most important ones (organisms without these neurons are athermotactic). Thermosensory neurons are not exposed to the outside and their signaling is dependent, among others, by cation channels.

Aerosensation
Lacking a respiratory system, C.elegans relies on diffusion through its pseudocoelomic fluid, which reaches all tissues of an individual. Metabolism can be sustained into an environment composed of 2-21% oxygen. As in thermosensation, oxygen sensation can be associated to favorable, food rich environments and set a preferred oxygen concentration for the individual. Aerosensation is not performed by the sensilla but from neurons distributed in the whole body.

Chemosensation
Different chemical compounds can be sensed by the organism, these can be water-soluble such as anions/cations or amino acids (gustatory sensation) or volatile such as alcohols (olfactory sensation). 32 neurons, assigned to 14 different classes, are involved in chemosensation, 22 of which are located in the amphid sensilla. Different neurons sense different compounds and depending on the type of stimulus they get (noxious or favorable) they lead to different types of movements associated with avoidance or attraction

Links
WormAtlas - Online database of all aspects of C.elegans.

WormBook - Online review of C.elegans biology.

C.elegans II - Free online textbook.

OpenWorm - Open source 3D model of C.elegans.