scholarly journals Synchronous inhibitory pathways create both efficiency and diversity in the retina

2017 ◽  
Author(s):  
Mihai Manu ◽  
Lane T. McIntosh ◽  
David B. Kastner ◽  
Benjamin N. Naecker ◽  
Stephen A. Baccus

Visual information is conveyed from the retina to the brain by a diverse set of retinal ganglion cells. Although they have differing nonlinear properties, nearly all ganglion cell receptive fields on average compute a difference in intensity across space and time using a region known as the classical or linear surround1,2, a property that improves information transmission about natural visual scenes3,4. The spatiotemporal visual features that create this fundamental property have not been quantitatively assigned to specific interneurons. Here we describe a generalizable causal approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. Analyzing two inhibitory cell classes, horizontal cells and linear amacrine cells, we find that rather than transmitting different temporal features, the two inhibitory pathways act synchronously to create the salamander ganglion cell surround at different spatial scales. Using these measured visual features and theories of efficient coding, we computed a fitness landscape representing the information transmitted using different weightings of the two inhibitory pathways. This theoretical landscape revealed a ridge that maintains near-optimal information transmission while allowing for receptive field diversity. The ganglion cell population showed a striking match to this prediction, concentrating along this ridge across a wide range of positions using different weightings of amacrine or horizontal cell visual features. These results show how parallel neural pathways synthesize a sensory computation, and why this architecture achieves the potentially competing objectives of high information transmission of individual ganglion cells, and diversity among receptive fields.

1977 ◽  
Vol 40 (1) ◽  
pp. 26-43 ◽  
Author(s):  
K. Naka

1. The basic organization of the biphasic (or concentric) receptive field is established in the bipolar cells as the result of an interaction between two signals, one local representing the activity of a small number of receptors, and the other integrating (19, 20) or global (28) coming from the S space or a lamina formed by the horizontal cells (8, 14, 22, 29). 2. Bipolar-ganglion cell pairs are segregated into two types; A (on center) and B (off center) pairs. A depolarization of a bipolar cell produces spike discharges from ganglion cells of the same type and a hyperpolarization depresses their discharges. I haven't detected any cross talk between the types A and B pairs. Bipolar and ganglion cells must be interfaced by the classical chemical synapses, the only such kind in the catfish retina. 3. Horizontal and type N neurons form two lateral transmission systems, one distal and the other proximal (19, 20). Signals in the lateral systems are shared by the two receptive-field types and are not excitatory or inhibitory in themselves; it is incumbent upon the postsynaptic neurons to decide the polarity of the synaptic transmission. The horizontal cell participates directly in the formation of biphasic receptive fields of bipolar cells by providing their surrounding, whereas type N neuron seems to modify the receptive-field organization established in the bipolar cells. 4. Type N neurons are amacrine cells because they do not produce spike discharges (2, 18, 21) and because they influence the activity of both A and B receptive fields. 5. The function of the type C neuron is as unique as its structure (21) and is not fully clear as yet. It is not a conventional amacrine cell as the type N appears to be, nor is it a classical ganglion cell which forms either a type A or B receptive field (2). 6. Type Y neurons are a class of ganglion cells which forms either a type A or B receptive field.


1996 ◽  
Vol 13 (6) ◽  
pp. 1099-1107 ◽  
Author(s):  
Péter Buzás ◽  
Sára Jeges ◽  
Robert Gábriel

AbstractThe main route of information flow through the vertebrate retina is from the photoreceptors towards the ganglion cells whose axons form the optic nerve. Bipolar cells of the frog have been so far reported to contact mostly amacrine cells and the majority of input to ganglion cells comes from the amacrines. In this study, ganglion cells of frogs from two species (Bufo marinus, Xenopus laevis) were filled retrogradely with horseradish peroxidase. After visualization of the tracer, light-microscopic cross sections showed massive labeling of the somata in the ganglion cell layer as well as their dendrites in the inner plexiform layer. In cross sections, bipolar output and ganglion cell input synapses were counted in the electron microscope. Each synapse was assigned to one of the five equal sublayers (SLs) of the inner plexiform layer. In both species, bipolar cells were most often seen to form their characteristic synaptic dyads with two amacrine cells. In some cases, however, the dyads were directed to one amacrine and one ganglion cell dendrite. This type of synapse was unevenly distributed within the inner plexiform layer with the highest occurrence in SL2 both in Bufo and Xenopus. In addition, SL4 contained also a high number of this type of synapse in Xenopus. In both species, we found no or few bipolar to ganglion cell synapses in the marginal sublayers (SLs 1 and 5). In Xenopus, 22% of the bipolar cell output synapses went onto ganglion cells, whereas in Bufo this was only 10%. We conclude that direct bipolar to ganglion cell information transfer exists also in frogs although its occurrence is not as obvious and regular as in mammals. The characteristic distribution of these synapses, however, suggests that specific type of the bipolar and ganglion cells participate in this process. These contacts may play a role in the formation of simple ganglion cell receptive fields.


2016 ◽  
Vol 115 (6) ◽  
pp. 2761-2778 ◽  
Author(s):  
Reece E. Mazade ◽  
Erika D. Eggers

The retina adjusts its signaling gain over a wide range of light levels. A functional result of this is increased visual acuity at brighter luminance levels (light adaptation) due to shifts in the excitatory center-inhibitory surround receptive field parameters of ganglion cells that increases their sensitivity to smaller light stimuli. Recent work supports the idea that changes in ganglion cell spatial sensitivity with background luminance are due in part to inner retinal mechanisms, possibly including modulation of inhibition onto bipolar cells. To determine how the receptive fields of OFF cone bipolar cells may contribute to changes in ganglion cell resolution, the spatial extent and magnitude of inhibitory and excitatory inputs were measured from OFF bipolar cells under dark- and light-adapted conditions. There was no change in the OFF bipolar cell excitatory input with light adaptation; however, the spatial distributions of inhibitory inputs, including both glycinergic and GABAergic sources, became significantly narrower, smaller, and more transient. The magnitude and size of the OFF bipolar cell center-surround receptive fields as well as light-adapted changes in resting membrane potential were incorporated into a spatial model of OFF bipolar cell output to the downstream ganglion cells, which predicted an increase in signal output strength with light adaptation. We show a prominent role for inner retinal spatial signals in modulating the modeled strength of bipolar cell output to potentially play a role in ganglion cell visual sensitivity and acuity.


1991 ◽  
Vol 7 (1-2) ◽  
pp. 155-169 ◽  
Author(s):  
Leo Peichl

AbstractA specific morphological class of ganglion cell, the alpha cell, was first defined in cat retina. Alpha cells have since been found in a wide range of mammalian retinae, including several orders of placental and marsupial mammals. Characteristically, they have the largest somata and a large dendritic field with a typical branching pattern. They occur as inner and outer stratifying subpopulations, presumably corresponding to ON-center and OFF-center receptive fields. In all species, alpha cells account for less than 10% of the ganglion cells, their somata are regularly spaced, and their dendritic fields evenly and economically cover the retina in a mosaic-like fashion. The morphology of alpha cells and many features, both of single cells and of the population, are conserved across species with different habitats and life-styles. This suggests that alpha cells are a consistent obligatory ganglion cell type in every mammalian retina and probably subserve some fundamental task(s) in visual performance.Some general rules about the construction principles of ganglion cell classes are inferred from the alpha cells, stressing the importance of population parameters for the definition of a class. The principle, that a functionally and morphologically homogeneous population should have a regular arrangement and a complete and even coverage of the retina to perform its part in image processing at each retinal location, is especially evident across species and across ganglion cell types.


The structure of the human, but mainly of the rhesus monkey, retina as examined by Golgi-staining techniques is described and interpreted on evidence from both light and electron microscopy. One type of rod bipolar cell and two types of cone bipolar cell are recognized. The rod bipolar is exclusively connected to rods. The midget bipolar is postsynaptic to only one cone but each cone is also presynaptic to a diffuse cone (flat) bipolar. Such flat bipolar cells are in synaptic relationship with about seven cones. No other bipolar cell types have been found. The brush bipolar of Polyak is interpreted as probably a distorted rod bipolar, while Polyak’s centrifugal bipolar is a misinterpretation of the morphology of diffuse amacrine cells. When presumptive centrifugal bipolars were observed they appeared to be a developmental stage of amacrine cells. In the outer plexiform layer two types of horizontal cell have been defined. Each type of horizontal cell has a single axon and two kinds of horizontal cell axon terminals are recognized. In the inner plexiform layer there are two main classes of amacrine cells: the stratified amacrines and the diffuse amacrines. Each class of amacrine has a wide variety of shapes. Polyak’s midget ganglion cell is confirmed and his five other kinds of ganglion cell are classified into diffuse and stratified ganglion cells according to the level at which their dendrites branch within the inner plexiform layer. A fuller summary is given by the diagram and in the legend of figure 98, p. 174. A new type of midget bipolar is described in the Appendix (p. 177).


2018 ◽  
Author(s):  
Neda Nategh ◽  
Mihai Manu ◽  
Stephen A. Baccus

SUMMARYInhibitory interneurons are diverse in the nervous system, though most have unknown functions. In sensory systems, two broad classes of computation have been considered – linear effects that generate the classical receptive field and nonlinear modulation that mediates non-classical contextual effects. Here we analyze salamander retinal amacrine cells using a general approach to directly measure and model how an interneuron pathway influences computation. Using simultaneous intracellular and multielectrode recording, we measure the linear feature contributed by an amacrine pathway and nonlinear modulatory effects on other visual features. We find great diversity in the functional effects of amacrine cells, with even apparently simple, linear amacrine cells creating both linear and diverse modulatory effects such as divisive gain control, polarity reversal and shifting threshold on distinct visual features conveyed to single target ganglion cells. The functional effects of amacrine cells parallel the previously noted anatomical and molecular heterogeneity of this interneuron population.HighlightsSome amacrine cells contribute a linear feature to ganglion cells but others do notThe visual feature conveyed by an amacrine pathway improves a ganglion cell modelOne amacrine-ganglion cell pair has different modulatory effects on different featuresAmacrine cells with linear responses have highly diverse nonlinear modulary effects


1993 ◽  
Vol 10 (5) ◽  
pp. 887-897 ◽  
Author(s):  
L. C. L. Silveira ◽  
V. H. Perry ◽  
E. S. Yamada

AbstractThe distribution of ganglion cells and displaced amacrine cells was determined in whole-mounted Aotus retinae. In contrast to diurnal simians, Aotus has only a rudimentary fovea. Ganglion cell density decreases towards the periphery at approximately the same rate along all meridians, but is 1.2–1.8 times higher in the nasal periphery when compared to temporal region at the same eccentricities. The total number of ganglion cells varied from 421,500 to 508,700. Ganglion cell density peaked at 15,000/mm2 at 0.25 mm dorsal to the fovea. The displaced amacrine cells have a shallow density gradient, their peak density in the central region is about 1500–2000/mm2 and their total number varied from 315,900 to 482,800. Comparison between ganglion cell density and areal cortical magnification factor for the primary visual cortex, area 17, shows that there is not a simple proportional representation of the ganglion cell distribution. There is an overrepresentation of the central 10 deg of the visual field in the visual cortex. The present results for Aotus and the results of a similar analysis of data from other primates indicate that the overrepresentation of the central visual field is a general feature of the visual system of primates.


2001 ◽  
Vol 18 (4) ◽  
pp. 559-570 ◽  
Author(s):  
B.E. REESE ◽  
M.A. RAVEN ◽  
K.A. GIANNOTTI ◽  
P.T. JOHNSON

The present study has examined the emergence of cholinergic stratification within the developing inner plexiform layer (IPL), and the effect of ablating the cholinergic amacrine cells on the formation of other stratifications within the IPL. The population of cholinergic amacrine cells in the ferret's retina was identified as early as the day of birth, but their processes did not form discrete strata until the end of the first postnatal week. As development proceeded over the next five postnatal weeks, so the positioning of the cholinergic strata shifted within the IPL toward the outer border, indicative of the greater ingrowth and elaboration of processes within the innermost parts of the IPL. To examine whether these cholinergic strata play an instructive role upon the development of other stratifications which form within the IPL, one-week-old ferrets were treated with l-glutamate in an attempt to ablate the population of cholinergic amacrine cells. Such treatment was shown to be successful, eliminating all of the cholinergic amacrine cells as well as the alpha retinal ganglion cells in the central retina. The remaining ganglion cell classes as well as a few other retinal cell types were partially reduced, while other cell types were not affected, and neither retinal histology nor areal growth was compromised in these ferrets. Despite this early loss of the cholinergic amacrine cells, which are eliminated within 24 h, other stratifications within the IPL formed normally, as they do following early elimination of the entire ganglion cell population. While these cholinergic amacrine cells are present well before other cell types have differentiated, apparently neither they, nor the ganglion cells, play a role in determining the depth of stratification for other retinal cell types.


2011 ◽  
Vol 28 (3) ◽  
pp. 205-220 ◽  
Author(s):  
MARTIN WILSON ◽  
NICK NACSA ◽  
NATHAN S. HART ◽  
CYNTHIA WELLER ◽  
DAVID I. VANEY

AbstractUsing both NADPH diaphorase and anti-nNOS antibodies, we have identified—from retinal flatmounts—neuronal types in the inner retina of the chicken that are likely to be nitrergic. The two methods gave similar results and yielded a total of 15 types of neurons, comprising 9 amacrine cells, 5 ganglion cells, and 1 centrifugal midbrain neuron. Six of these 15 cell types are ubiquitously distributed, comprising 3 amacrine cells, 2 displaced ganglion cells, and a presumed orthotopic ganglion cell. The remaining nine cell types are regionally restricted within the retina. As previously reported, efferent fibers of midbrain neurons and their postsynaptic partners, the unusual axon-bearing target amacrine cells, are entirely confined to the ventral retina. Also confined to the ventral retina, though with somewhat different distributions, are the “bullwhip” amacrine cells thought to be involved in eye growth, an orthotopic ganglion cell, and two types of large axon-bearing amacrine cells whose dendrites and axons lie in stratum 1 of the inner plexiform layer (IPL). Intracellular fills of these two cell types showed that only a minority of otherwise morphologically indistinguishable neurons are nitrergic. Two amacrine cells that branch throughout the IPL are confined to an equatorial band, and one small-field orthotopic ganglion cell that branches in the proximal IPL is entirely dorsal. These findings suggest that the retina uses different processing on different regions of the visual image, though the benefit of this is presently obscure.


1979 ◽  
Vol 73 (3) ◽  
pp. 265-286 ◽  
Author(s):  
D F Wunk ◽  
F S Werblin

The postsynaptic potentials (PSPs) that form the ganglion cell light response were isolated by polarizing the cell membrane with extrinsic currents while stimulating at either the center or surround of the cell's receptive field. The time-course and receptive field properties of the PSPs were correlated with those of the bipolar and amacrine cells. The tiger salamander retina contains four main types of ganglion cell: "on" center, "off" center, "on-off", and a "hybrid" cell that responds transiently to center, but sustainedly, to surround illumination. The results lead to these inferences. The on-ganglion cell receives excitatory synpatic input from the on bipolars and that synapse is "silent" in the dark. The off-ganglion cell receives excitatory synaptic input from the off bipolars with this synapse tonically active in the dark. The on-off and hybrid ganglion cells receive a transient excitatory input with narrow receptive field, not simply correlated with the activity of any presynaptic cell. All cell types receive a broad field transient inhibitory input, which apparently originates in the transient amacrine cells. Thus, most, but not all, ganglion cell responses can be explained in terms of synaptic inputs from bipolar and amacrine cells, integrated at the ganglion cell membrane.


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