Large-Scale Convergence of Receptor Cell Arrays Onto Afferent Terminal Arbors in the Lorenzinian Electroreceptors of Polyodon.

Abstract

Certain sensory receptors contain many transducers, converging onto few afferents. Convergence creates star-topology neural networks, of iterative parallel organization, that may yield special functional properties. We quantitated large-scale convergence in electroreceptors on the rostrum of preadult paddlefish, Polyodon spathula (Acipenseriforme vertebrates), and analyzed the afferent terminal branching underlying the convergence. From neurophysiological mapping, a recorded afferent innervated 23.3 ± 9.1 (range 6–45) ampullary organs, and innervated every ampullary organ within the receptive field’s sharp boundary. Ampullary organs each contained ∼665 Lorenzinian receptor cells, from imaging and modeling. We imaged three serial types of afferent branching at electroreceptors, after immunofluorescent labeling for neurite filaments, glial sheaths, or nodal ion channels, or by DiI tracing. (i) Myelinated tree: Each of 3.08 ± 0.51 (2–4) parallel afferents from a cranial nerve (ALLn) entered a receptive field from deeper tissue, then branched into a laminar tree of large myelinated dendrites, parallel to the skin, that branched radially until ∼9 extremities with heminodes, which were candidate sites of spike encoders. (ii) Inline transition: Each myelinated extremity led distally into local unmyelinated arbors originating at inline branching structures covered by terminal (satellite) glia. The unmyelinated transition zones included globular afferent modules, 4–6 microns wide, from which erupted fine fascicles of parallel submicron neurites, a possibly novel type of neuronal branching. The neurite fascicles formed loose bundles projecting ∼105 microns distally to innervate local groups of ∼3 adjacent ampullary organs. (iii) Radial arbors: Receptor cells in an electrosensory neuroepithelium covering the basal pole of each ampullary organ were innervated by bouton endings of radial neurites, unmyelinated and submicron, forming a thin curviplanar lamina distal to the lectin+ basal lamina. The profuse radial neurites diverged from thicker (∼2 micron) basolateral trunks. Overall, an average Polyodon electroreceptor formed a star topology array of ∼9 sensor groups. Total convergence ratios were 15,495 ± 6,052 parallel receptor cells per afferent per mean receptive field, assuming 100% innervation. Large-scale convergence likely increases the signal-to-noise ratio (SNR) of stimulus encoding into spiking afferent output, increasing receiver sensitivity. Unmyelinated arbors may also regenerate and repair the afferent innervation of ampullary organs.LSID: urn:lsid:zoobank.org:act:09BCF04C-3C3C-4B6C-9DC9-A2BF43087369