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J Cell Biol. 1975 April 1; 65(1): 192–222.
PMCID: PMC2111162

Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits


Freeze-fracture analysis of the neural connections in the outer plexiform layer of the retina of primates (Macaca mulatta and Macaca arctoides) demonstrates a remarkable diversity in the internal structure of the synaptic membranes. In the invaginating synapses of cone pedicles, the plasma membrane of the photoreceptor ending contains an aggregate of A-face particles, a hexagonal array of synaptic vesicle sites, and rows of coated vesicle sites, which are deployed in sequence from apex to base of the synaptic ridge. The horizontal cell dendrites lack vesicle sites and have two aggregates of intramembrane A-face particles, one at the interface with the apex of the synaptic ridge, the other opposite the tip of the invaginating midget bipolar dendrite. Furthermore, the horizontal cell dendrites are interconnected by a novel type of specialized junction, characterized by: (a) enlarged intercellular cleft, bisected by a dense plate and traversed by uniformly spaced crossbars; (b) symmetrical arrays of B-face particles arranged in parallel rows within the junctional membranes; and (c) a layer of dense material on the cytoplasmic surface of the membranes. The plasmalemma of the invaginating midget bipolar dendrite is unspecialized. At the contact region between the basal surface of cone pedicles and the dendrites of the flat midget and diffuse cone bipolar cells, the pedicle membrane has moderately clustered A-face particles, but no vesicle sites, whereas the adjoining membrane of the bipolar dendrites contains an aggregate of B-face particles. The invaginating synapse of rod spherules differs from that of cone pedicles, because the membrane of the axonal endings of the horizontal cells only has an A-face particle aggregate opposite the apex of the synaptic ridge. Specialized junctions between horizontal cell processes, characterized by symmetrical arrays of intramembrane B-face particles, are also present in the neuropil underlying the photoreceptor endings. Small gap junctions connect the processes of the horizontal cells; other gap junctions probably connect the bipolar cell dendrites which make contact with each cone pedicle. Most of the junctional specializations typical of the primate outer plexiform layer are also found in the rabbit retina. The fact that specialized contacts between different types of neurons interacting in the outer plexiform layer have specific arrangements of intramembrane particles strongly suggests that the internal structure of the synaptic membranes is intimately correlated with synaptic function.

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Selected References

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  • Baylor DA, Fuortes MG, O'Bryan PM. Receptive fields of cones in the retina of the turtle. J Physiol. 1971 Apr;214(2):265–294. [PubMed]
  • BIRKS R, HUXLEY HE, KATZ B. The fine structure of the neuromuscular junction of the frog. J Physiol. 1960 Jan;150:134–144. [PubMed]
  • Boycott BB, Kolb H. The horizontal cells of the rhesus monkey retina. J Comp Neurol. 1973 Mar 1;148(1):115–139. [PubMed]
  • Branton D. Fracture faces of frozen membranes. Proc Natl Acad Sci U S A. 1966 May;55(5):1048–1056. [PubMed]
  • Bunt AH. Enzymatic digestion of synaptic ribbons in amphibian retinal photoreceptors. Brain Res. 1971 Feb 5;25(3):571–577. [PubMed]
  • Cartaud J, Benedetti EL, Cohen JB, Meunier JC, Changeux JP. Presence of a lattice structure in membrane fragments rich in nicotinic receptor protein from the electric organ of Torpedo marmorata. FEBS Lett. 1973 Jun 15;33(1):109–113. [PubMed]
  • Couteaux R, Pécot-Dechavassine M. Vésicules synaptiques et poches au niveau des "zones actives" de la jonction neuromusculaire. C R Acad Sci Hebd Seances Acad Sci D. 1970 Dec 21;271(25):2346–2349. [PubMed]
  • Dowling JE, Boycott BB. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci. 1966 Nov 15;166(1002):80–111. [PubMed]
  • Dreyer F, Peper K, Akert K, Sandri C, Moor H. Ultrastructure of the "active zone" in the frog neuromuscular junction. Brain Res. 1973 Nov 23;62(2):373–380. [PubMed]
  • Fuortes MG, Schwartz EA, Simon EJ. Colour-dependence of cone responses in the turtle retina. J Physiol. 1973 Oct;234(1):199–216. [PubMed]
  • Gray EG, Pease HL. On understanding the organisation of the retinal receptor synapses. Brain Res. 1971 Dec 10;35(1):1–15. [PubMed]
  • Heuser JE, Reese TS. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol. 1973 May;57(2):315–344. [PMC free article] [PubMed]
  • Heuser JE, Reese TS, Landis DM. Functional changes in frog neuromuscular junctions studied with freeze-fracture. J Neurocytol. 1974 Mar;3(1):109–131. [PubMed]
  • Kaneko A. Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J Physiol. 1970 May;207(3):623–633. [PubMed]
  • Kaneko A. Electrical connexions between horizontal cells in the dogfish retina. J Physiol. 1971 Feb;213(1):95–105. [PubMed]
  • Kaneko A. Receptive field organization of bipolar and amacrine cells in the goldfish retina. J Physiol. 1973 Nov;235(1):133–153. [PubMed]
  • Karnovsky MJ. The ultrastructural basis of capillary permeability studied with peroxidase as a tracer. J Cell Biol. 1967 Oct;35(1):213–236. [PMC free article] [PubMed]
  • LADMAN AJ. The fine structure of the rod-bipolar cell synapse in the retina of the albino rat. J Biophys Biochem Cytol. 1958 Jul 25;4(4):459–466. [PMC free article] [PubMed]
  • Landis DM, Reese TS. Differences in membrane structure between excitatory and inhibitory synapses in the cerebellar cortex. J Comp Neurol. 1974 May 1;155(1):93–125. [PubMed]
  • McNutt NS, Weinstein RS. Membrane ultrastructure at mammalian intercellular junctions. Prog Biophys Mol Biol. 1973;26:45–101. [PubMed]
  • Naka KI, Rushton WA. The generation and spread of S-potentials in fish (Cyprinidae). J Physiol. 1967 Sep;192(2):437–461. [PubMed]
  • Nelson R. A comparison of electrical properties of neurons in Necturus retina. J Neurophysiol. 1973 May;36(3):519–535. [PubMed]
  • Nickel E, Potter LT. Ultrastructure of isolated membranes of Torpedo electric tissue. Brain Res. 1973 Jul 27;57(2):508–517. [PubMed]
  • O'Bryan PM. Properties of the depolarizing synaptic potential evoked by peripheral illumination in cones of the turtle retina. J Physiol. 1973 Nov;235(1):207–223. [PubMed]
  • Perri V, Sacchi O, Raviola E, Raviola G. Evaluation of the number and distribution of synaptic vesicles at cholinergic nerve-endings after sustained stimulation. Brain Res. 1972 Apr 28;39(2):526–529. [PubMed]
  • Pfenninger K, Akert K, Moor H, Sandri C. The fine structure of freeze-fractured presynaptic membranes. J Neurocytol. 1972 Sep;1(2):129–149. [PubMed]
  • Pfenninger KH, Rovainen CM. Stimulation- and calcium-dependence of vesicle attachment sites in the presynaptic membrane: a freeze-cleave study on the lamprey spinal cord. Brain Res. 1974 May 31;72(1):1–23. [PubMed]
  • Pinto da Silva P, Branton D. Membrane splitting in freeze-ethching. Covalently bound ferritin as a membrane marker. J Cell Biol. 1970 Jun;45(3):598–605. [PMC free article] [PubMed]
  • Raviola E, Gilula NB. Gap junctions between photoreceptor cells in the vertebrate retina. Proc Natl Acad Sci U S A. 1973 Jun;70(6):1677–1681. [PubMed]
  • Sandri C, Akert K, Livingston RB, Moor H. Particle aggregations at specialized sites in freeze-etched postsynaptic membranes. Brain Res. 1972 Jun 8;41(1):1–16. [PubMed]
  • Satir B, Schooley C, Satir P. Membrane fusion in a model system. Mucocyst secretion in Tetrahymena. J Cell Biol. 1973 Jan;56(1):153–176. [PMC free article] [PubMed]
  • Schwartz EA. Responses of bipolar cells in the retina of the turtle. J Physiol. 1974 Jan;236(1):211–224. [PubMed]
  • Simon EJ. Two types of luminosity horizontal cells in the retina of the turtle. J Physiol. 1973 Apr;230(1):199–211. [PubMed]
  • Sjöstrand FS. A search for the circuitry of directional selectivity and neural adaptation through three-dimensional analysis of the outer plexiform layer of the rabbit retina. J Ultrastruct Res. 1974 Oct;49(1):60–156. [PubMed]
  • Streit P, Akert K, Sandri C, Livingston RB, Moor H. Dynamic ultrastructure of presynaptic membranes at nerve terminals in the spinal cord of rats. Anesthetized and unanesthetized preparations compared. Brain Res. 1972 Dec 24;48:11–26. [PubMed]
  • Tillack TW, Marchesi VT. Demonstration of the outer surface of freeze-etched red blood cell membranes. J Cell Biol. 1970 Jun;45(3):649–653. [PMC free article] [PubMed]
  • Werblin FS, Dowling JE. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969 May;32(3):339–355. [PubMed]

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