The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (gymnotidae): Dendritic differentiation and synaptic specificity in a simple cortex

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Abstract

The posterior lateral line lobe of two high-frequency weakly electric fish, Apteronotus albifrons and Eingenmannia viriscens, was studied at the electron microscopic level. The various cell types previously described by light microscopy (Maler, ′79) were identified on the basis of their unique position or by combined Golgi-EM. Afferent input to the posterior lobe was identified either by its location and generally accepted characteristics, e.g., parallel fibers in the molecular layer, or by making appropriate lesions and noting the degenerating terminals, e.g., primary electroreceptive afferents.

The major cell types of the posterior lobe are as follows: (1) spherical cells—an electron-dense cytoplasm crowded with ribosomes and other organelles; (2) granule cells—a small pale soma; fairly electron-dense dendrites, and pale axon terminals with clustered pleomorphic vesicles; (3) pyramidal cells—a large pale soma with a well-developed golgi apparatus; pale dendrites with evenly distributed microtubules; the somatic dendrites of pyramidal cells have an exceptional quantity of coated vesicles, multivesicular bodies, and smooth endoplasmic reticulum; (4) polymorphic cells—a medium-sized electron-dense soma; the dendrites are easily recognized by their content of neurofilaments, while their axon terminals are distinguished by their increased electron density and tightly packed ovoid vesicles.

Two types of primary electroreceptive afferents were identified: (1) Latency coder terminals were slightly electron-dense, with a small number of vesicles but large numbers of mitochondria; (2) Probability coder terminals were electron-lucent, with a large number of round synaptic vesicles; the diameters of these vesicles were always bimodally distributed. Afferent fibers to the molecular layer of the posterior lobe are organized as parallel fibers at the light microscopic level; ultrastructurally they are similar to parallel fibers of the cerebellum and make appropriate asymetric synapses on all apical dendritic trees within the molecular layer.

The circuitry of the posterior lobe is summarized in Figure 17. Latency coders make gap junction contact only with spherical cells, which in turn receive strictly latency coder input. Probability coders make mostly asymmetric chemical synapses onto granule cell and pyramidal cell basilar dendrites. The granule cell axons make symmetric synaptic contacts with the somata and somatic dendrites of both basilar and non-basilar pyramids; they also synapse on the ascending apical and basilar dendritic processes of granule cells. These ascending processes of granule cells make gap junction contacts with the somata and somatic dendrites of only the non-basilar pyramids. The consequence of this basic circuit appears to be that the posterior lobe can detect and enhance the contrast of objects with either high conductivity (basilar pyramids) or low conductivity (non-basilar pyramids).

The somatic dendrites of pyramidal cells were found to have extraordinary numbers of coated vesicles, and these were often associated with the postsynaptic densities of granule cell axons. The possible role of these coated vesicles in receptor recycling is discussed.

All afferents of the posterior lobe end in specific laminae, and in a given lamina they usually terminate on all potential postsynaptic sites; this was defined as laminar specificity of synaptic connections. The latency coder to spherical cells contacts, and the granule cell ascending process to non-basilar pyramid contacts are both specific to particular cells within a lamina; this was defined as cellular specificity of synaptic connections. Other examples of both sorts of synaptic specificity are presented and discussed in relation to current concepts of neuronal development.

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