How does morphology relate to function in sensory arbors?

Abstract

Sensory dendrites fall into many different morphological and functional classes. Polymodal nociceptors are one subclass of sensory neurons, which are of particular note owing to their elaborate dendritic arbors. Complex developmental programs are required to form these arbors and there is striking conservation of morphology, function and molecular determinants between vertebrate and invertebrate polymodal nociceptors. Based on these studies, we argue that arbor morphology plays an important role in the function of polymodal nociceptors. Similar associations between form and function might explain the plethora of dendrite morphologies seen among all sensory neurons.

Figure 1. Organization and development of PVD and FLP arbors in C.elegans

Schematic diagrams of PVD (blue) and FLP (red) processes as they are seen at 5 different stages of development [late larval stage 2 (late L2) to late L4/ young adult]. Dashed lines (in black) indicate processes that appeared earlier in development but have retracted by this stage. All views are from the left aspect showing only the left side cells of each cell pair; anterior is to the left. For convenience, all stages are shown at constant size. A single axon emerges ventralward from the cell body (colored ball) before going rostrally within the ventral cord. The process(es) emerging laterally from the cell body elaborate into highly branched dendrites. Note that knowledge of FLP development is meager compared to that of PVD, but available data suggest that FLP dendrites undergo the same sequence of events, and are likely obey the same rules.

Figure 2. Proposed mechanism linking organization of PVD branches to mechanosensation in C.elegans

A. Schematic of an adult C. elegans midbody showing three ventral and three dorsal menorah-like structures growing out of the PVD primary dendrite (dark blue). Movement of a single menorah upon pressure application by a sharp needle is indicated (white lines indicate position of the central dorsal menorah before pressure application). Transverse cross-section on the left edge of the diagram indicates positions of the four muscle quadrants (green) and hypodermis (beige) in the bodywall. The cuticle and thin layer of hypodermis are peeled back in part of the diagram to reveal the PVD quaternary dendrites (but quaternary dendrites are really within the hypodermis). One dorsal menorah on the left has been numbered, to indicate the temporal stage of branch development [ie. primary branches appeared first (1), followed by secondary (2) etc.]. On the right of the diagram, the overlying structures are shown: the outer cuticle layer (grey) and cuticle annuli (grey lines). B. PVD quaternary dendrite enmeshed within the thin hypodermal layer (beige) in a transmission electron microscopic (TEM) image [colors have been superimposed on the image for clarity: PVD, blue; M (bodywall muscle), green; H (hypodermis), yellow]. Adapted, with permission, from [10]. C. Enlarged schematic showing how stretching of affected processes may lead to local DEG/ENaC channel opening. Both the position and likely activation state of these channels are indicated (filled circle indicates fully open, filled ellipse partly open, and thin line is closed).

Figure 3. Multi-dendritic polymodal nociceptors and mechanosensors from different organisms

A. Drosophila DA-IV neurons. The skin of the fly third instar larva is tiled with dendritic arbors that cover large receptive fields; the many free endings of each cell show self-avoidance. Redrawn with permission, based on immunohistochemical images from [25]. B. Leech P-cell. Pressure receptors in leech skin have distinctive multi-branched arbors with very fine endings that show self-avoidance (adapted, with permission, based on dye-filling images in [37]). Their receptive fields cover large portions of the leech skin and are known to substantially overlap circumferentially (i.e. no tiling). C. Penicillate neuron of human skin. Nociceptors form highly branched dendrites ensheathed by a Schwann cell and its processes, except for short free endings at their termini (gray process shown in inset) that insert themselves at the borders between epidermal cells (wiggly line extending from the ending) or by invagination into a subepidermal cell. Short terminal branches of the neuron run within peripheral branches of the Schwann cell, and anchor to the epidermal basal lamina (arrows). These neurons are unmeylinated and belong to the C-fiber neuron class. N, Schwann cell nucleus. Based on schematic diagram in [30]. D. Palisade neuron of mammalian fur. Mechanosensitive dendrites end in candelabra-like arbors. These arbors show self-avoidance, and perhaps tiling, and wrap around the base of a vibrissal hair follicle (indicated by *). A single protruding hair is indicated by an arrow. Adapted, with permission, from [60].