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,
The branching of vertebrate neuronal processes, axons or dendrites, is predominantly binary, where a proximal neuronal process bifurcates into two distal progeny. Here, we illustrate counterexamples where neuronal processes branched into more than 2, up to 6, progeny branches, in one step. These were branch points of myelinated dendrites in the peripheral terminals of ALLn cranial nerve afferents innervating the Lorenziniantype ampullary electroreceptors on the rostrum of paddlefish, Polyodon spathula. We imaged afferent terminals fluorescently (in widefield stacks, with deconvolution) after immunolabling of afferent terminals for neuronal cytoplasmic neurofilament-H (NEFH), myelin markers (MBP, P0), or nodal ion channels (Nav1.x, Kv1.1), or after migration of DiI in dendrite membranes. Branched afferent terminals formed a laminar radial radiation beneath a receptive field, parallel to the skin surface, with two serial stages: (1) Starting at each afferent's centric first branchpoint, each of a small group of 2-4 (most often 3) afferents branched radially into 2-4 (usually 3) generations of myelinated dendrites, whose internodes were covered by sheaths immunoreactive for antigenic markers of myelin (MBP+/P0+), ending distally at~15 heminode presumed spike initiation zones. (2) From the latter, bundles of unmyelinated (MBP-/P0-) sensory neuron (NEFH+) processes projected distally to innervate electrosensory neuroepithelia of adjacent ampullary organs. The nonbinary branch points that we imaged were in stage-1, on myelinated dendrites. Branch points always coincided with composite systems of nodes, in which each progeny dendrite started at a narrowed nodal segment expressing voltage gated sodium ion channels at high density. These narrowed nodal segments of multiple progeny branched in parallel from a parent's blunt distal end. Hence the branch point nodal complexes formed multisite excitable systems, likely strongly coupled due to proximity. 1 + 2 where N varies from 1.5 to 2 corresponding to symmetrical d/D ratios of 0.63-0.71 [2].
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