The connectome of the Caenorhabditis elegans pharynx

Detailed anatomical maps of individual organs and entire animals have served as invaluable entry points for ensuing dissection of their evolution, development, and function. The pharynx of the nematode Caenorhabditis elegans is a simple neuromuscular organ with a self-contained, autonomously acting nervous system, composed of 20 neurons that fall into 14 anatomically distinct types. Using serial EM reconstruction, we re-evaluate here the connectome of the pharyngeal nervous system, providing a novel and more detailed view of its structure and predicted function. Contrasting the previous classification of pharyngeal neurons into distinct inter- and motorneuron classes, we provide evidence that most pharyngeal neurons are also likely sensory neurons and most, if not all, pharyngeal neurons also classify as motorneurons. Together with the extensive cross-connectivity among pharyngeal neurons, which is more widespread than previously realized, the sensory-motor characteristics of most neurons define a shallow network architecture of the pharyngeal connectome. Network analysis reveals that the patterns of neuronal connections are organized into putative computational modules that reflect the known functional domains of the pharynx. Compared to the somatic nervous system, pharyngeal neurons both physically associate with a larger fraction of their neighbors and create synapses with a greater proportion of their neighbors. We speculate that the overall architecture of the pharyngeal nervous system may be reminiscent of the architecture of ancestral, primitive nervous systems.

Neuropeptides in cnidarians

Cnidarians are the lowest animal group having a nervous system. In the primitive nervous systems of cnidarians, peptides play important roles as neurotransmitters or neurohormones. So far, we have isolated and sequenced about 35 neuropeptides from different cnidarian classes (Hydrozoa, Scyphozoa, Anthozoa). All these neuropeptides have a C-terminal amide group, which protects against C-terminal degradation, but which also is important for receptor recognition. Also the N-termini of the cnidarian neuropeptides often contain different kinds of protecting groups (such as <Glu residues, L-3-phenyllactyl groups, and X-Pro or X-Pro-Pro sequences). Cnidarian neuropeptides are located in neuronal dense-core vesicles and are synthesized as preprohormones, which can contain up to 41 copies of a neuro peptide sequence. From Hydra, six different neuropeptide genes have been cloned so far. Each gene is expressed by a specific population of neurons, but in two instances coexpression of neuropeptide genes has been found. We have also cloned some of the cnidarian prohormone processing enzymes, among them the enzymes necessary for C-terminal amidation. These enzymes are closely related to their mammalian counterparts. All these data show that the primitive nervous systems of cnidarians have already acquired some of the sophisticated principles that we know from higher animals.

Primitive nervous systems: electrophysiology of the pharynx of the polyclad flatworm, Enchiridium punctatum

1. Electrical activity accompanying motor activity can be recorded from the excised pharynx of Enchiridium punctatum. Multiple stimuli elicit behaviour which consists of an initial aperture closure followed by extension and then peristalsis. If the stimulus parameters are increased the preparation bends from side to side instead of proceeding through the behavioural sequence. Bending appears to inhibit other movements differentially. 2. The conduction involved with peristalsis is polarized and proceeds in a proximal direction. 3. With stimulus intensities greater than those needed to produce the behavioural response an initial muscle potential (IMP) is evoked. The IMP is frequency sensitive. Maximum facilitation occurs within 100 ms and drops to 50% of maximum within 250 ms. 4. Conduction velocities of the IMP range from 0–05 m s-1 to 1-9 m s-1. Conduction velocities appear to increase with facilitation.