Synaptic microcircuitry of bipolar and amacrine cells with serotonin-like immunoreactivity in the retina of the turtle, Pseudemys scripta elegans

Abstract

Although serotonin is thought to be a neurotransmitter in a number of retinal systems, much of the precise synaptic connectivity of serotonergic neurons is unknown. To address this issue, we used an antiserum directed against serotonin to label serotonergic bipolar and amacrine cells in the turtle retina. Light-microscopic analysis of labeled amacrine and bipolar cells indicated that both had bistratified dendritic arborizations primarily in stratum 1 and in strata 4/5 of the inner plexiform layer.Ultrastructural analysis of the neurocircuitry of these cells indicated that the processes of labeled bipolar cells in the outer plexiform layer made basal junction contacts with photoreceptor terminals. Only in rare instances did labeled bipolar cells processes invaginate near photoreceptor ribbon synapses. Processes of labeled bipolar cells received both conventional and small ribbon synaptic contacts in the outer plexiform layer. Bipolar cell processes in stratum 1 of the inner plexiform layer synapsed onto either amacrine/amacrine or amacrine/ganglion cell dyads, and made rare ribbon synaptic contacts onto labeled amacrine cell processes. Synaptic inputs to serotonergic bipolar cells in stratum 1 were from unlabeled bipolar and amacrine cells. Bipolar cell contacts in strata 4/5 were similar to those in stratum 1, but were fewer in number and no bipolar cell inputs were seen.Labeled amacrine cell output in both strata was onto other unlabeled amacrine cells and ganglion cells; but synaptic outputs to unlabeled bipolar cells were only seen in strata 4/5. In both strata 1 and 4/5, synaptic inputs to labeled amacrine cells were from both unlabeled amacrine cells and labeled bipolar cells. The serotonergic amacrine cells had many more synaptic interactions in stratum 1 than in strata 4/5 which supports the role of serotonergic bipolar cells in the OFF pathway of retinal processing. Interactions between serotonergic bipolar and amacrine cells may play an important role in visual processing.

Tryptophan Hydroxylase and Serotonin Receptors 5-HT1A, 5-HT2A, 5-HT3A, 5-HT4, 5-HT5A, 5-HT6 and 5-HT7 in Frog and Turtle Retina: an Immunofluorescence Study

“…It is known that the different subtypes of amacrine cells form the so called "serial synapses" between each other. Our observation about the presence of a great number of serial synapses between the serotoninergic amacrine cells and other amacrine cells is in good agreement with the observations of other authors [13,16,17]. We also showed in our study that the 5-HT1A, 5-HT3A and 5-HT5A receptors mediate the serotoninergic transmission to the ganglion cells.…”

“…As concerns the synapses between the serotoninergic amacrine cells and bipolar cells, called "feedback synapses", our results show that the transmission here is most probably mediated by the serotonin receptors 5-HT3A and 5-HT5A. The presence of such type of serotoninergic synapse (without identification of the receptors) is pointed out by Hurd and Eldred as well [13].…”

“…Most often, antibodies directed to serotonin (anti 5-HT antibodies) are used, and by means of this technique the retinal serotonin is proved to be expressed predominantly in the amacrine and bipolar cells [13,14,46,47]. To a lesser extent, serotonin is found in some ganglion cells as well [48].…”

Synaptic circuitry of serotonin-synthesizing and serotonin-accumulating amacrine cells in the retina of the cane toad, Bufo marinus

“…The synaptic connections of SLI amacrine cells have been investigated in the retinas of chick (Millar & Morgan, 1989); turtle (Hurd & Eldred, 1993); tiger salamander (Watt & Wilson 1990); and Xenopus laevis and Bufo marinus (Gdbriel et al, 1993). Labeled amacrine cells frequently form synapses with unlabeled amacrine cells.…”

Two classes of bipolar cell in the retina of the skateRaja erinacea

“…Schaper, 1899;Retzius, 1905;Witkovsky & Stell, 1973). Bipolar cells which accumulate serotonin have been identified by immunocytochemical, autoradiographic or histofluorescent techniques in a variety of non-mammalian retinas (Ehinger & Floren, 1978;Marc, 1982;Bruun et al, 1984;Osborne, 1984;Witkovsky et al, 1984;Weiler andCHAPPELL & Sch6tte, 1985a,b;Sch/itte & Weiler, 1987;Tauchi, 1989Tauchi, , 1990Negishi & Teranishi, 1990;Sch/itte & Witkovsky, 1990;Zhu et al, 1992;Hurd & Eldred, 1993;Schiitte, 1994). Kainic acid has been found to release serotonin from serotonin-accumulating cells (Weiler & Sch/itte, 1985b;Schfitte & Witkovsky, 1990) and this release was blocked in the presence of the ionotropic glutamate receptor antagonist 2,3-piperidine dicarboxylic acid (PDA) (Weiler & Sch/itte, 1985b).…”