Opioid pathways in an avian retina. II. Synaptic organization of enkephalin-immunoreactive amacrine cells

Abstract

Peroxidase-antiperoxidase immunocytochemistry was utilized to investigate the synaptic organization of enkephalin-like immunoreactive amacrine (Enk-amacrine) cells in the chicken retina. An initial light microscopic analysis revealed that immunostained cell bodies were situated in either the second or third tier of cells from the border of the inner nuclear and inner plexiform layers. The processes of such cells extended into the inner plexiform layer where they ramified as a fine plexus in sublaminae 1 and 3 to 5. At the ultrastructural level, enkephalin-positive somas exhibited a rather dense and evenly distributed peroxidase reaction product throughout their cytoplasm. Furthermore, the nucleus of Enk-amacrine cells was characterized by a round, unindented nuclear membrane. Immunoreactive processes of such cells were found to receive synaptic input from unstained amacrine and bipolar cells. Immunolabeled varicosities formed conventional synaptic contacts onto other vesicle-filled, nonimmunoreactive profiles tentatively suggested to originate from amacrine cells. Bipolar cell terminals did not receive synaptic input from stained varicosities of enkephalin-immunoreactive amacrine cells. Moreover, each of the above synaptic relationships were identified in each of sublaminae 1, and 3 to 5 of the inner plexiform layer. In addition, labeled varicosities of Enk-amacrine cells synapsed upon unstained processes which lacked synaptic vesicles and possibly arise from ganglion cells. Enkephalin- positive processes were also observed to synapse upon the vitreal pole of unstained somas situated in the innermost cell row of the inner nuclear layer. Lastly, large immunoreactive varicosities of Enk- amacrine cells were often characterized by the presence of large dense- core vesicles in addition to typical, small agranular synaptic vesicles.

Spatial and Temporal Distribution Patterns of Enkephalinergic Neurons in Adult and Developing Retinas of the Preproenkephalin-Green Fluorescent Protein Transgenic Mouse

“…Double immunofluorescent staining results in the present study showed that ENKergic neurons existed in a subpopulation of amacrine cells. This is consistent with previous studies that reported that ENK was localized to a population of amacrine cells in the chicken [Brecha et al, 1979;Tornqvist et al, 1981;Watt et al, 1984;Watt et al, 1985]. The activity of the ENK-immunoreactive amacrine cells of the chicken retina is low in the light and high in the dark, resulting in parallel increases and decreases in the levels of ENK.…”

“…The ENKergic system in the retina has been examined extensively in the chicken, where ENK is localized to a population of amacrine cells [Brecha et al, 1979;Tornqvist et al, 1981;Watt et al, 1984;Watt et al, 1985]. A previous study also showed that the ENK-immunoreactive amacrine cells within the retina appear to be important polyfunctional mediators of the response of the retina, the eye as a whole and the suprachiasmatic nucleus/ pineal system to light and dark .…”

Interaction between enkephalin and γ‐aminobutyric acid in the chicken retina: A double‐label immunoelectron microscopic analysis

“…Approximately 76% of these synaptic arrangements involved the processes of enkephalin amacrine cells, while enkephalin/GABA amacrine cell processes were involved in the remaining 24% of these synaptic relationships (see Discussion). Overall, the basic synaptic organization of enkephalin/GABA amacrine cells was quite similar to that of enkephalin amacrine cells, Moreover, the results of the present study were in agreement with a previous single-label study that defined the basic synaptic relationships of enkephalinergic amacrine cells in the chicken retina (Watt et al, 1985a;see Discussion). Briefly, both enkephalin and enkephaliniGABA processes were found to be pre-and postsynaptic to amacrine cells, postsynaptic to bipolar cells, and presynaptic to possible ganglion cell processes.…”

“…Moreover, this observation extends a previous study of the synaptic organization of enkephalinergic amacrine cells in the chicken retina. In this previous study, both members of a dyad were never observed to express enkephalin immunoreactivity (Watt et al, 1985a). Two ribbon synaptic relationships were observed in which one postsynaptic element was a n enkephalin/GABA process, while the second member of the dyad was either an unlabelled amacrine cell process (example not shown) or a process void of synaptic vesicles (Fig.…”

Diabetic keratopathy and treatment by modulation of the opioid growth factor (OGF)–OGF receptor (OGFr) axis with naltrexone: A review

“…The presence in the eye of endogenous opioids having a role in neurotransmission was initially detected in amacrine cells and cellular processes within the retinal inner plexiform layer [7,96,102,110]. Enkephalins serving as growth factors were identified in the retina by Isayama and coworkers [51], and the precursor for OGF, preproenkephalin A mRNA, were detected in neonatal rat retina [52] and developing brain [114], with the peptide OGF present and functioning as early as the first week of life in rats.…”