We have examined the various classes of cells that can be innervated by the giant cerebral neuron (GCN), an identified serotonergic cell that functions in arousal and maintenance of feeding behavior. We have found that this single neuron innervates a remarkable variety of postsynaptic targets by means of varicosities bearing active zones. The neuron's presynaptic terminals were identified by electron microscopic radioautography after intrasomatic injection of a tritiated amino sugar precursor of membrane glycoproteins; these are moved to nerve endings by fast axonal transport. In addition to endings on buccal muscle, we have found that GCN forms appositions with the morphological characteristics of synapses on axonal processes and cell bodies of neurons in the buccal ganglion and, unexpectedly, it forms appositions most often with glial cells which form the lining of intraganglionic hemal sinuses. Thus, GCN, through contacts on a variety of postsynaptic targets, has the potential of mediating several different functions, each of which is usually associated with a specific specialized type of neuron. In random electron micrographs, approximately 14% of GCN's varicosities had membrane specializations presumed to be the sites where transmitter is released. In these sections, GCN's active zones were quite small, 0.25 micrometer or approximately five vesicle diameters long. One of GCN's terminals was reconstructed completely from a series of thin sections. It had a single, flat ovoid active zone with an area of 17 micrometers2. We suggest that active zones often are overlooked in random sections of monoaminergic terminals because they are small.
Injection of [3Hjserotonin directly into the cell body of the giant metacerebral neuron (GCN), an identified serotonergic cell in the Aplysia cerebral ganglion, revealed a striking association of the labeled transmitter with large lysosomes. Most of the [3H] Recycled synaptic membrane, packaged in lysosomes, is thought to return to the perikaryon by retrograde axonal transport. Ultimately these worn constituents are incorporated into the lipofuscin granules, which are plentiful in many nerve cell bodies, both vertebrate and invertebrate (1, 2). Cytological and histochemical studies have provided convincing'evidence that these organelles are lysosomes that are approaching their last developmental stage, and are morphologically similar to terminal lysosomes (residual bodies) found in many other cell types. With age, the number of these bodies increases, as does their content of pigment, lipid, and other materials thought to derive from degraded cellular organelles and from exogenous constituents engulfed by the cell (3). In gastropod molluscs, somatic lysosomes are slightly larger than the lipofuscin granules of vertebrate neurons, reaching 10 gm in diameter (4-8). In pigmented Aplysia neurons they are characteristically situated in a juxtanuclear ring and contain the pigment originally used to classify neurons of the abdominal ganglion'into pigmented and white cells (9).There have been previous indications that somatic lysosomes can retain the ability to carry out activities normally attributed to other cellular organelles. Attention has recently been drawn to Aplysia pigment granules because in some neurons they serve as an intracellular Ca2+ sink (a property assigned to mitochondria) and can release Ca2+ in response to light. Thus Henkart (10) and Brown et al. (11) MATERIALS AND METHODS Animals and Intracellular Injections. Aplysia californica weighing 40-70 g were supplied by Pacific Bio-Marine Supply, Venice, CA. The cerebral ganglion with the lateral lip nerves, cerebrobuccal connectives, and buccal ganglia attached, or the abdominal ganglion, was removed by opening the animal through the foot; nervous tissue was pinned in a chamber filled with an artificial sea water containing amino acids, glucose, and vitamins (18).Before injection, the overlying connective tissue sheath of the cerebral ganglion was removed by dissection. The giant metacerebral neuron (GCN) was injected with [G-3H]serotonin (13.8-14.7 Ci/mmol), [G-3H]
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