Ultrastructural and electrophysiological changes associated with K⁺-evoked release of neurotransmitter at the synaptic terminals of skate photoreceptors

Abstract

Bathing the skate retina in a Ringer solution containing a high concentration (100 mM) of potassium ions depolarized the visual cells, depleted the receptor terminals of synaptic vesicles, and suppressed completely the b-wave of the ERG and the intracellularly recorded response of horizontal cells (the S-potential). The depletion of synaptic vesicles was accompanied by a large increase in the extent of the plasma membrane resulting in distortion of the normal terminal profile, i.e. distension of the basal surface and elaborate infolding of protoplasmic extensions. Morphometric analysis showed that despite the changes in vesicle content and terminal structure, the combined linear extent of the vesicular and plasma membranes was unchanged from control (superfusion with normal Ringer solution); the increase in plasma membrane was equivalent to the observed loss of vesicular membrane. When returned to a normal Ringer solution, the terminals rapidly began to reform, and in about 10 min they were morphologically indistinguishable from receptor terminals seen in control preparations. After 30 min in the normal Ringer solution, the amount of membrane associated with the vesicles and the plasma membrane had reverted to control values, and once again the total membrane estimated morphometrically remained essentially the same. Thus, there is an efficient mechanism at the photoreceptor terminal for the recycling of vesicle membrane following exocytosis.The K+-induced depletion of synaptic vesicles was paralleled by a precipitous loss of responsivity in both the b-wave of the ERG and the S-potential of the horizontal cells. However, after 30-min exposure to the high K+ and a return to normal Ringer solution, the recovery of electrophysiological activity followed a much slower time course from that associated with the structural changes; 60 min or longer were required for the potentials to exhibit maximum response amplitudes. It appears that the rate-limiting step in restoring normal synaptic function following massive depletion of vesicular stores is transmitter resynthesis and vesicle loading rather than vesicle recycling.

Light adaptation affects synaptic vesicle density but not the distribution of GABA A receptors in goldfish photoreceptor terminals

“…Since the synaptic vesicles appeared clear and not filled with reaction product, we conclude that GABAr-IR was associated with the cytoplasmic surface of the synaptic vesicle membrane. The plasma membrane of photoreceptor terminals undergoes considerable endocytosis, probably to retrieve membrane added by vesicular exocytosis (Ripps and Chappell, 1991;Ripps et al, 1976;Schacher et al, 1976;Schaeffer and Raviola, 1975). This endocytotic activity could explain the presence of GABAr-IR synaptic vesicles in view of the observation that GABAr-IR occurs on the cytoplasmic surface of both the plasma membrane and synaptic vesicles, which would be expected for vesicles formed by endocytosis.…”

Calcium regulation in photoreceptors

“…ER and its specializations are found in all parts of the inner segment, including the soma and the synaptic terminal (149)(150). Ca 2+ is sequestered into both rough and smooth ER (151)(152)(153).…”

Receptive field properties of rod-driven horizontal cells in the skate retina.

“…A particularly attractive preparation for these purposes is the all-rod retina of the skate (Dowling and Ripps, 1970;Szamier and Ripps, 1983;Ripps and Dowling, 1991). In addition to having only rod photoreceptors, which ensures that any effects that may be observed are not induced by activation of the cone system, the horizontal cells of this elasmobranch have extremely large perikarya (Dowling and Ripps, 1973;Malchow, Qian, Ripps, and Dowling, 1990) that are suitable for obtaining long-term, stable, intracellular recordings even with repeated solution changes during superfusion (Ripps and Chappell, 1991). Another interesting feature of the skate retina relates to the identity of the putative neurotransmitter of its interplexiform cell.…”