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Synaptic Mechanisms of Bipolar Cell Terminals

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Synaptic Mechanisms of Bipolar Cell Terminals View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Vision Research 39 (1999) 2469–2476 Synaptic mechanisms of bipolar cell terminals Gary Matthews * Department of Neurobiology and Beha6ior, State Uni6ersity of New York, Stony Brook, NY 11794-5230, USA Received 8 May 1998; received in revised form 24 August 1998 Abstract Giant synaptic terminals of goldfish bipolar neurons allow direct studies of presynaptic mechanisms underlying neurotransmit- ter release and its modulation. Calcium influx via L-type calcium channels of the terminal triggers synaptic vesicle exocytosis, which can be monitored in isolated terminals by means of the associated changes in membrane capacitance. Information about the kinetics and calcium dependence of synaptic exocytosis has been obtained from capacitance measurements in these ribbon-type synaptic terminals. © 1999 Elsevier Science Ltd. All rights reserved. Keywords: Synaptic mechanisms; Terminals; Bipolar neurons Studies of presynaptic mechanisms in the vertebrate enzymatic digestion of goldfish retina or in single, central nervous system (CNS) are complicated by the isolated terminals. Consistent with their central role in small size of most CNS synaptic terminals. However, neurotransmitter release, voltage-dependent calcium several notable exceptions allow direct electrical mea- channels are located predominantly in the synaptic surements to be made from single terminals, including terminal of the bipolar cell (Tachibana & Okada, 1991; giant caliciform terminals in the brainstem auditory Heidelberger & Matthews, 1992), although there is also system of the rat (Forsythe, 1994) and in the ciliary a low density of channels in the soma. The synaptic ganglion of the chick (Stanley & Atrakchi, 1990; Stan- calcium current is sensitive to dihydropyridine calcium- ley, 1993) and large, bulbous terminals of certain types channel agonists and antagonists, activates at a rela- of bipolar neuron in goldfish retina (Kaneko & tively positive voltage range, and shows sustained Tachibana, 1985; Heidelberger & Matthews, 1992). The activation during prolonged depolarization (Heidel- latter are of interest in retinal neurobiology, and in this berger & Matthews, 1992). All of these characteristics review, I will focus on our current understanding of are typical of L-type calcium channels (Fox, Nowycky presynaptic events that regulate neurotransmitter re- & Tsien, 1987). The dihydropyridine-sensitive channels lease in the giant terminals of goldfish bipolar neurons. have been demonstrated to control glutamate release from the synaptic terminal (Tachibana, Okada, Arimura, Kobayashi & Piccolino, 1993). Thus, in goldfish bipolar cells, neurotransmitter release is con- 1. Calcium current of the synaptic terminal trolled by L-type calcium channels. The large size (diameter:10 mm) of the synaptic terminal of some classes of bipolar cell in carp and goldfish (Stell, 1967; Ishida, Stell & Lightfoot, 1980; 2. Presynaptic inhibition at the bipolar-cell terminal Saito & Kujiraoka, 1982; Sherry & Yazulla, 1993) permits direct patch-clamp recording of synaptic cal- The synaptic terminals of goldfish bipolar neurons cium current, either in intact bipolar cells isolated after receive extensive feedback synapses from amacrine cells (Marc, Stell, Bok & Lam, 1978; Yazulla, Studholme & Wu, 1987), which serve to modulate the synaptic output * Fax: +1-516-632-6661. from the bipolar cells. Several functional effects of the E-mail address: [email protected] (G. Matthews) synaptic feedback have been described, mediated by 0042-6989/99/$ - see front matter © 1999 Elsevier Science Ltd. All rights reserved. PII: S0042-6989(98)00249-1 2470 G. Matthews / Vision Research 39 (1999) 2469–2476 different neurotransmitters and neurotransmitter recep- pamine was mimicked by forskolin and by a permeant tors. Many of the amacrine cells that target bipolar-cell analog of cAMP, suggesting that dopamine acts by terminals are GABAergic (Yazulla et al., 1987), and elevating cAMP in the terminal. Taken together, the GABA acts on two distinct GABA receptors to pro- actions of GABA, dopamine, and neuropeptides duce presynaptic inhibition in the terminal. First, demonstrate that synaptic feedback onto the bipolar GABA activates a GABAA-like receptor and increases cell terminal is capable of modulating transmitter re- chloride conductance (Tachibana & Kaneko, 1987; lease from the bipolar cell and thus the transfer of Heidelberger & Matthews, 1991; Matthews, Ayoub & information from the outer to the inner retina. Heidelberger, 1994). Secondly, GABA produces GTP- dependent inhibition of the calcium current of the bipolar-cell terminal via a GABAB-like receptor 3. Capacitance measurements of exocytosis (Heidelberger & Matthews, 1991; Matthews et al., 1994). The GABA-activated chloride current hyperpo- When a secretory granule fuses with the plasma larizes the bipolar cell and thus inhibits calcium influx membrane during exocytosis, the surface area of the into the terminal via voltage-gated calcium channels secreting cell increases. The increased surface area can (Heidelberger & Matthews, 1991; Matthews et al., be estimated by monitoring the associated change in 1994). GABA inhibits the calcium current by shifting electrical capacitance of the cell, as shown schematically its voltage dependence toward more positive potentials, in Fig. 1. Sensitive techniques for monitoring capaci- thus tending to prevent activation of the current upon tance in real time in single cells are well-established depolarization. (Lindau & Neher, 1988; Gillis, 1995) and have been Both actions of GABA in the terminal are mediated used to gather information about exocytosis in various by receptors with unusual pharmacology. The receptor types of secretory cell, including adrenal chromaffin coupled to chloride conductance is insensitive to bicu- cells (Neher & Marty, 1982), mast cells (Fernandez, culline and SR95531, which typically block GABAA Neher & Gomperts, 1984), pituitary cells (Thomas, receptors, while the action of GABA on calcium cur- Suprenant & Almers, 1990), and neuroendocrine nerve rent is neither mimicked by the GABAB agonist ba- terminals (Fidler Lim, Nowycky & Bookman, 1990; clofen nor blocked by the GABAB antagonist saclofen. Lindau, Stuenkel & Nordmann, 1992). Because of the bicuculline resistance of the GABAA-like Neurotransmitter is released at synapses by a process receptors, they are commonly referred to in retinal of exocytosis, during which transmitter-containing research as GABAC receptors (Feigenspan, Wa¨ssle & synaptic vesicles fuse with the membrane of the presy- Bormann, 1993; Qian & Dowling, 1993) to distinguish naptic terminal in response to calcium influx via them from bicuculline-sensitive isoforms of the GABAA voltage-gated calcium channels. Therefore, capacitance receptor. The bicuculline-resistant GABAA-like recep- measurements are potentially useful at synapses as an tor probably corresponds to the retina-specific GABA index of neurotransmitter release. However, a difficulty r receptor subunit, 1 (Cutting, Lu, O’Hara, Kasch, for capacitance measurements from synaptic terminals Montrose-Rafizader, Donovan, Shimada, Antonarakis, is the small size—and hence the small capacitance—of Guggino, Uhl & Kazazian, 1991; Shimada, Cutting & the synaptic vesicles at most synapses. A synaptic vesi- Uhl, 1992), which produces bicuculline-resistant cle with a diameter of about 30 nm, which would be GABA-activated chloride channels when expressed in typical for glutamatergic synapses in the CNS, would Xenopus oocytes. Studies using conformationally locked have an expected capacitance of about 3×10−17 F analogs of GABA show that the bipolar-cell GABAA- (assuming that capacitance of biological membranes is like receptor prefers the trans (extended) isomer of approximately 10−14 F/mm2). The addition of such a GABA to the cis (folded) conformation (Ayoub & small amount of capacitance is below the level of Matthews, 1991). resolution presently attainable in whole-cell recordings, In addition to GABA, other neurotransmitters affect and so capacitance measurements are limited to special- the bipolar-cell terminal. Neuropeptides that are found ized synapses at which the number of synaptic vesicles in amacrine cells, including substance P and met- fusing with the plasma membrane during a stimulus is enkephalin, produce GTP-dependent inhibition of cal- sufficiently large to allow detection of the correspond- cium current by shifting the voltage dependence, similar ing increase in capacitance. In neurons, capacitance to the action produced by GABA (Ayoub & Matthews, measurements have been used to study synaptic release 1992). Goldfish bipolar-cell terminals also receive do- in the giant synaptic terminals of goldfish bipolar cells paminergic inputs (Dowling & Ehinger, 1978; Yazulla (von Gersdorff & Matthews, 1994), in retinal photore- & Zucker, 1988), and dopamine was found to enhance ceptors (Rieke & Schwartz, 1994), and in saccular hair the increase in intracellular calcium evoked in the ter- cells (Parsons, Lenzi, Almers & Roberts, 1994). All of minal by activation of voltage-gated calcium channels these cells have distinctive presynaptic structures (Heidelberger & Matthews, 1994). This action of do- (synaptic ribbons or synaptic bodies), which are G. Matthews / Vision Research 39 (1999) 2469–2476 2471 Fig. 1. Schematic diagram of the changes in membrane capacitance that accompany exocytosis and endocytosis. Electrical
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