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The Vertebrate Retina

John E. Dowling, Mark W. Dubin

10.1002/cphy.cp010308

Source: Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes

Originally published: 1984

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Synaptic Organization
1.1 Receptive Fields
2 Intracellular Activity
3 Outer Plexiform Layer Functional Activity
4 Inner Plexiform Layer Functional Activity
5 Pharmacology of Plexiform Layers and the Interplexiform Cell
6 Summary
7 Appendix
7.1 Ganglion Cell Functional Terminology
Figure 1.

A: light micrograph of the mudpuppy retina showing three nuclear layers, two plexiform layers, and prominent Müller (glial) cells, (M). ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer. × 345. B: principal cell types found in vertebrate retina, based on observations of cells in mudpuppy retina impregnated by Golgi method. R, receptors; H, horizontal cells; B, bipolar cells; A, amacrine cells; G, ganglion cells; M, Müller (glial cell)

A: adapted from Miller and Dowling 80; B: adapted from Dowling 23
Figure 2.

Examples of synaptic contacts observed by electron microscopy in vertebrate retinas. A: ribbon synapses (arrows) of cone receptor terminal in rhesus monkey retina. Three processes penetrate into invaginations along terminal base. Lateral processes within invagination are from horizontal cells, H; central elements are bipolar cell dendrites, B. × 38,000. B: ribbon synapse of bipolar teminal B (filled arrow), and conventional synapse of amacrine process (open arrow) in inner plexiform layer of chicken retina. There are usually two postsynaptic processes at ribbon synapses of bipolar terminals and one postsynaptic process at conventional synapses of amacrine cells. Note that amacrine cell process, A, is both a pre‐ and postsynaptic element. × 45,000. C: conventional synapse (open arrow) made by horizontal cell process, H, onto bipolar cell dendrite B, in mudpuppy retina. Note that this horizontal cell process is itself postsynaptic at ribbon synapse of receptor terminal (filled arrow). × 45,000. D: reciprocal synaptic arrangement between bipolar terminal, B, and amacrine cell process, A, in skate retina. Bipolar terminal makes contact with amacrine process at ribbon synapse (filled arrow); amacrine process makes conventional synapse (open arrow) back onto bipolar terminal. × 40,000. E: serial (open arrows) and reciprocal (closed arrow) synaptic arrangments between four amacrine processes (A1-A4) in frog retina. Micrograph illustrates that amacrine processes may be pre‐ and postsynaptic along short portions of their length. × 50,000. F: superficial or basal contact of flat bipolar cell dendrite (FB) on base of receptor terminal (RT) in frog. Note that there is neither synaptic ribbon nor aggregation of synaptic vesicles associated with these junctions. Some membranous specializations, however, are seen along the junction along with filamentous material in junctional cleft. × 75,000. G: an electrical (gap) junction in inner plexiform layer of rat retina between two amacrine cell processes, A. Note that extracellular space between processes making contact is virtually obliterated at the junction. × 100,000. H: gap junction in inner plexiform layer of rat retina demonstrated by freeze‐fracture method. Numerous tightly packed particles, 80-100 Å in diameter, are characteristic of gap junctions seen in variety of tissues, × 100,000.
Figure 3.

Summary diagram of arrangements of synaptic contacts found in vertebrate retinas. In outer plexiform layer, processes from invaginating bipolar, IB, and horizontal, H, cells penetrate into invaginations in receptor terminals, R, and terminate near synaptic ribbons of receptors. Processes of flat bipolar cells, FB, make superficial (basal) contacts on bases of some receptor terminals. Horizontal cells make conventional synaptic contacts onto bipolar dendrites. In inner plexiform layer, bipolar terminals most commonly contact one ganglion cell, G, dendrite and one amacrine cell, A, process at the ribbon synapse (left), or two amacrine cell processes (right). When the latter arrangement predominates in a retina, numerous conventional synapses between amacrine cell processes (serial synapses) are observed. Amacrine cell synapses in all retinas make synapses back onto bipolar teminals (reciprocal synapses). Input to ganglion cells may differ in terms of proportion of bipolar and amacrine synapses. Ganglion cells may receive mainly bipolar input, G1, an even mix of bipolar and amacrine input, G2, or exclusively amacrine input, G3.
Figure 4.

Intracellular recordings from neurons in mudpuppy retina. Responses elicited with a spot of light (diam approx. 100 μm) focused over electrode (left column of records) or with a centered annulus (radius, 500 μm; width, 100 μm).
Figure 5.

Summary figure correlating synaptic organization of outer plexiform layer of retina with intracellularly recorded responses from mudpuppy retina. R, receptors; H, horizontal cell; B, bipolar cells.
Figure 6.

Experiment showing effects of magnesium on skate horizontal cell. Ringer's solution containing magnesium was applied to retina (arrow); within 15-25 s the cell began to hyperpolarize. During next few minutes, cell hyperpolarized to approximately −60 mV, and light‐evoked activity was lost. At end of experiment, pipette was withdrawn from cell (break in record). Rapid positive shift of potential of 55 to 60 mV confirmed increase in membrane potential in presence of high levels of magnesium. Test flash intensity and duration (0.2 s) were constant throughout both experiments. Markers along lower trace of each record indicate flash presentations

From Dowling and Ripps 33
Figure 7.

Intensity‐response curve of typical cone photoreceptor. Increasing numbers on log intensity scale indicate brighter stimuli. Receptor potential values are measured peak amplitudes of responses to flashed spot stimuli of approximately 2 s duration. Photoreceptor hyperpolarizes in response to light. Note that entire range of curve spans about 4 log units of illumination and that most of variation in response spans only about 3 log units of illumination

Adapted from Werblin 129
Figure 8.

Intensity‐response curves for depolarizing bipolar cell in mudpuppy retina taken at three different background levels. Background levels indicated by numbers labeled Surround Intensity; 1.2 is brightest background. For each curve, steady stimulus of noted intensity (log scale) is presented in surround portion of receptive field of cell. Then, spots in center of receptive field were flashed. Intensities of those spots are shown on abscissa, and peak responses they elicited are indicated in mV on ordinate. Note that antagonistic interaction of center and surround shift operating curve of bipolar cell to the right as function of increased surround illumination. This results in midpoint of operating range falling at an intensity approximately equal to value of background illumination itself

Adapted from Werblin 130
Figure 9.

Idealized response characteristics of typical center‐surround type of ganglion cells. Cell at left is an on‐center, off‐surround unit; cell at right is an off‐center, on‐surround cell. For each cell, response is to various stimuli of 1 s duration. Upper row is response to a spot of light presented in receptive‐field center. On‐center cell responds with a burst of spikes at light onset and continues to fire above its unstimulated (maintained) firing rate for duration of stimulus. This cell decreases its firing rate below maintained level to a very low rate for a brief time after stimulus is turned off. This increased response at light onset is indicated by symbols (pluses) filling region of receptive field center (upper left). Response of this cell to an annular ring of light that covers surround region of receptive field is shown in second row. Cell responds with extra firing at light offset in this case; at light onset firing is decreased. This firing pattern is indicated by symbols (minuses) in region of the receptive‐field surround. Bottom row shows that, when both center and surround regions are stimulated simultaneously by a large stimulus that covers entire receptive field, there is a weak burst of spikes both at light onset and light offset. This occurs because illumination of surround region decreases response to stimulation of receptive‐field center in same way in which it brought about a decrease in maintained firing rate (center row). The off‐center cell (right) has a similar response to whole‐field stimulation but has a reversal of center and surround responses when compared with on‐center type of cell.
Figure 10.

Diagram showing way in which photoreceptors, horizontal cells, and depolarizing bipolar cells interact to generate center‐surround responses of some types of on‐center ganglion cells. Basic retinal circuitry (upper left) and basic (The Rules) or initial conditions (upper right) apply throughout. Box (center) describes states of various cells unstimulated in darkness. Two boxes (left, read in order shown by large arrows) indicate way in which a centered spot of light stimulates ganglion cell. Two boxes (right, read in order indicated by large arrows) indicate way in which stimulation confined to receptive‐field surround of ganglion cell will affect it. Response of ganglion cell to whole‐field stimulation can be approximated by appropriate conjunction of relevant parts in descriptions.
Figure 11.

Diagram (left) shows test spot centered in receptive field of ganglion cell and windmill vanes in surround of that cell; retinal neurons driven by these stimuli are diagrammed (below). Response (spikes per flash) of ganglion cell to flashes of test spot of increasing intensity is graphed at right. Intensity of flash (logarithmic units) is on abscissa. If test flashes are presented when windmill is spinning, ganglion cell responds less strongly than when spots are presented with windmill stationary (see two curves). This is taken as evidence that amacrine cells cause response of ganglion cell to be diminished

Adapted from Werblin 129
Figure 12.

Summary of amacrine cell circuitry in inner plexiform layer with attention to synaptic transmitter used by amacrine cells. Dopaminergic amacrine cells, DA, make pre‐ and postsynaptic contacts only with other amacrine cells. Amacrine cells that use indoleamines, IA, are pre‐ and postsynaptic mainly with bipolar terminals, B, although they also make some connections with amacrine cells. Connections of other amacrine cells, A, that use γ‐amino butyric acid (GABA), glycine (Gly), or acetylcholine (Ach) have yet to be specifically determined, although at least some of these subclasses must provide synaptic output directly onto ganglion cells, G.
Figure 13.

Schematic diagram of synaptic connections of interplexiform cells of goldfish retina. Input to these neurons is in inner plexiform layer from amacrine cells, A. Interplexiform cell processes make synapses onto amacrine cell processes in inner plexiform layer, but never contact ganglion cells, G, or their dendrites. In outer plexiform layer, processes of interplexiform cells surround external horizontal cells, EH, making synapses on external horizontal cell perikarya and onto bipolar cell, B, dendrites. Interplexiform cell processes have never been observed as postsynaptic elements in outer plexiform layer at either rod, R, or cone, C, receptor terminals or at occasional external horizontal synapse. Also, no synapses are observed between interplexiform cell processes and elements of intermediate and internal horizontal cell layers. Intermediate (rod) horizontal cell (IH) and external horizontal cell axon process (EHA) are indicated

From Dowling and Ehinger 28
Figure 14.

Summary scheme of synaptic interactions that occur in retina and that underlie receptive‐field properties of on, off, and on‐off ganglion cells. Excitatory synapses (open circles), inhibitory junctions (filled circles), and reciprocal synapses (triangles) are indicated.


Figure 1.

A: light micrograph of the mudpuppy retina showing three nuclear layers, two plexiform layers, and prominent Müller (glial) cells, (M). ONL, outer nuclear layer; OPL, outer plexiform layer; INL, inner nuclear layer; IPL, inner plexiform layer; GCL, ganglion cell layer. × 345. B: principal cell types found in vertebrate retina, based on observations of cells in mudpuppy retina impregnated by Golgi method. R, receptors; H, horizontal cells; B, bipolar cells; A, amacrine cells; G, ganglion cells; M, Müller (glial cell)

A: adapted from Miller and Dowling 80; B: adapted from Dowling 23


Figure 2.

Examples of synaptic contacts observed by electron microscopy in vertebrate retinas. A: ribbon synapses (arrows) of cone receptor terminal in rhesus monkey retina. Three processes penetrate into invaginations along terminal base. Lateral processes within invagination are from horizontal cells, H; central elements are bipolar cell dendrites, B. × 38,000. B: ribbon synapse of bipolar teminal B (filled arrow), and conventional synapse of amacrine process (open arrow) in inner plexiform layer of chicken retina. There are usually two postsynaptic processes at ribbon synapses of bipolar terminals and one postsynaptic process at conventional synapses of amacrine cells. Note that amacrine cell process, A, is both a pre‐ and postsynaptic element. × 45,000. C: conventional synapse (open arrow) made by horizontal cell process, H, onto bipolar cell dendrite B, in mudpuppy retina. Note that this horizontal cell process is itself postsynaptic at ribbon synapse of receptor terminal (filled arrow). × 45,000. D: reciprocal synaptic arrangement between bipolar terminal, B, and amacrine cell process, A, in skate retina. Bipolar terminal makes contact with amacrine process at ribbon synapse (filled arrow); amacrine process makes conventional synapse (open arrow) back onto bipolar terminal. × 40,000. E: serial (open arrows) and reciprocal (closed arrow) synaptic arrangments between four amacrine processes (A1-A4) in frog retina. Micrograph illustrates that amacrine processes may be pre‐ and postsynaptic along short portions of their length. × 50,000. F: superficial or basal contact of flat bipolar cell dendrite (FB) on base of receptor terminal (RT) in frog. Note that there is neither synaptic ribbon nor aggregation of synaptic vesicles associated with these junctions. Some membranous specializations, however, are seen along the junction along with filamentous material in junctional cleft. × 75,000. G: an electrical (gap) junction in inner plexiform layer of rat retina between two amacrine cell processes, A. Note that extracellular space between processes making contact is virtually obliterated at the junction. × 100,000. H: gap junction in inner plexiform layer of rat retina demonstrated by freeze‐fracture method. Numerous tightly packed particles, 80-100 Å in diameter, are characteristic of gap junctions seen in variety of tissues, × 100,000.



Figure 3.

Summary diagram of arrangements of synaptic contacts found in vertebrate retinas. In outer plexiform layer, processes from invaginating bipolar, IB, and horizontal, H, cells penetrate into invaginations in receptor terminals, R, and terminate near synaptic ribbons of receptors. Processes of flat bipolar cells, FB, make superficial (basal) contacts on bases of some receptor terminals. Horizontal cells make conventional synaptic contacts onto bipolar dendrites. In inner plexiform layer, bipolar terminals most commonly contact one ganglion cell, G, dendrite and one amacrine cell, A, process at the ribbon synapse (left), or two amacrine cell processes (right). When the latter arrangement predominates in a retina, numerous conventional synapses between amacrine cell processes (serial synapses) are observed. Amacrine cell synapses in all retinas make synapses back onto bipolar teminals (reciprocal synapses). Input to ganglion cells may differ in terms of proportion of bipolar and amacrine synapses. Ganglion cells may receive mainly bipolar input, G1, an even mix of bipolar and amacrine input, G2, or exclusively amacrine input, G3.



Figure 4.

Intracellular recordings from neurons in mudpuppy retina. Responses elicited with a spot of light (diam approx. 100 μm) focused over electrode (left column of records) or with a centered annulus (radius, 500 μm; width, 100 μm).



Figure 5.

Summary figure correlating synaptic organization of outer plexiform layer of retina with intracellularly recorded responses from mudpuppy retina. R, receptors; H, horizontal cell; B, bipolar cells.



Figure 6.

Experiment showing effects of magnesium on skate horizontal cell. Ringer's solution containing magnesium was applied to retina (arrow); within 15-25 s the cell began to hyperpolarize. During next few minutes, cell hyperpolarized to approximately −60 mV, and light‐evoked activity was lost. At end of experiment, pipette was withdrawn from cell (break in record). Rapid positive shift of potential of 55 to 60 mV confirmed increase in membrane potential in presence of high levels of magnesium. Test flash intensity and duration (0.2 s) were constant throughout both experiments. Markers along lower trace of each record indicate flash presentations

From Dowling and Ripps 33


Figure 7.

Intensity‐response curve of typical cone photoreceptor. Increasing numbers on log intensity scale indicate brighter stimuli. Receptor potential values are measured peak amplitudes of responses to flashed spot stimuli of approximately 2 s duration. Photoreceptor hyperpolarizes in response to light. Note that entire range of curve spans about 4 log units of illumination and that most of variation in response spans only about 3 log units of illumination

Adapted from Werblin 129


Figure 8.

Intensity‐response curves for depolarizing bipolar cell in mudpuppy retina taken at three different background levels. Background levels indicated by numbers labeled Surround Intensity; 1.2 is brightest background. For each curve, steady stimulus of noted intensity (log scale) is presented in surround portion of receptive field of cell. Then, spots in center of receptive field were flashed. Intensities of those spots are shown on abscissa, and peak responses they elicited are indicated in mV on ordinate. Note that antagonistic interaction of center and surround shift operating curve of bipolar cell to the right as function of increased surround illumination. This results in midpoint of operating range falling at an intensity approximately equal to value of background illumination itself

Adapted from Werblin 130


Figure 9.

Idealized response characteristics of typical center‐surround type of ganglion cells. Cell at left is an on‐center, off‐surround unit; cell at right is an off‐center, on‐surround cell. For each cell, response is to various stimuli of 1 s duration. Upper row is response to a spot of light presented in receptive‐field center. On‐center cell responds with a burst of spikes at light onset and continues to fire above its unstimulated (maintained) firing rate for duration of stimulus. This cell decreases its firing rate below maintained level to a very low rate for a brief time after stimulus is turned off. This increased response at light onset is indicated by symbols (pluses) filling region of receptive field center (upper left). Response of this cell to an annular ring of light that covers surround region of receptive field is shown in second row. Cell responds with extra firing at light offset in this case; at light onset firing is decreased. This firing pattern is indicated by symbols (minuses) in region of the receptive‐field surround. Bottom row shows that, when both center and surround regions are stimulated simultaneously by a large stimulus that covers entire receptive field, there is a weak burst of spikes both at light onset and light offset. This occurs because illumination of surround region decreases response to stimulation of receptive‐field center in same way in which it brought about a decrease in maintained firing rate (center row). The off‐center cell (right) has a similar response to whole‐field stimulation but has a reversal of center and surround responses when compared with on‐center type of cell.



Figure 10.

Diagram showing way in which photoreceptors, horizontal cells, and depolarizing bipolar cells interact to generate center‐surround responses of some types of on‐center ganglion cells. Basic retinal circuitry (upper left) and basic (The Rules) or initial conditions (upper right) apply throughout. Box (center) describes states of various cells unstimulated in darkness. Two boxes (left, read in order shown by large arrows) indicate way in which a centered spot of light stimulates ganglion cell. Two boxes (right, read in order indicated by large arrows) indicate way in which stimulation confined to receptive‐field surround of ganglion cell will affect it. Response of ganglion cell to whole‐field stimulation can be approximated by appropriate conjunction of relevant parts in descriptions.



Figure 11.

Diagram (left) shows test spot centered in receptive field of ganglion cell and windmill vanes in surround of that cell; retinal neurons driven by these stimuli are diagrammed (below). Response (spikes per flash) of ganglion cell to flashes of test spot of increasing intensity is graphed at right. Intensity of flash (logarithmic units) is on abscissa. If test flashes are presented when windmill is spinning, ganglion cell responds less strongly than when spots are presented with windmill stationary (see two curves). This is taken as evidence that amacrine cells cause response of ganglion cell to be diminished

Adapted from Werblin 129


Figure 12.

Summary of amacrine cell circuitry in inner plexiform layer with attention to synaptic transmitter used by amacrine cells. Dopaminergic amacrine cells, DA, make pre‐ and postsynaptic contacts only with other amacrine cells. Amacrine cells that use indoleamines, IA, are pre‐ and postsynaptic mainly with bipolar terminals, B, although they also make some connections with amacrine cells. Connections of other amacrine cells, A, that use γ‐amino butyric acid (GABA), glycine (Gly), or acetylcholine (Ach) have yet to be specifically determined, although at least some of these subclasses must provide synaptic output directly onto ganglion cells, G.



Figure 13.

Schematic diagram of synaptic connections of interplexiform cells of goldfish retina. Input to these neurons is in inner plexiform layer from amacrine cells, A. Interplexiform cell processes make synapses onto amacrine cell processes in inner plexiform layer, but never contact ganglion cells, G, or their dendrites. In outer plexiform layer, processes of interplexiform cells surround external horizontal cells, EH, making synapses on external horizontal cell perikarya and onto bipolar cell, B, dendrites. Interplexiform cell processes have never been observed as postsynaptic elements in outer plexiform layer at either rod, R, or cone, C, receptor terminals or at occasional external horizontal synapse. Also, no synapses are observed between interplexiform cell processes and elements of intermediate and internal horizontal cell layers. Intermediate (rod) horizontal cell (IH) and external horizontal cell axon process (EHA) are indicated

From Dowling and Ehinger 28


Figure 14.

Summary scheme of synaptic interactions that occur in retina and that underlie receptive‐field properties of on, off, and on‐off ganglion cells. Excitatory synapses (open circles), inhibitory junctions (filled circles), and reciprocal synapses (triangles) are indicated.

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Article Title: The Vertebrate Retina
 

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John E. Dowling, Mark W. Dubin. The Vertebrate Retina. Compr Physiol 2011, Supplement 3: Handbook of Physiology, The Nervous System, Sensory Processes: 317-339. First published in print 1984. doi: 10.1002/cphy.cp010308