Signal transmission in the catfish retina. IV. Transmission to ganglion cells

1987 ◽  
Vol 58 (6) ◽  
pp. 1307-1328 ◽  
Author(s):  
H. M. Sakai ◽  
K. Naka

1. To characterize the temporal dynamic responses of ganglion cells and to define the possible inputs giving rise to their responses in catfish retina, we recorded the ganglion cell responses evoked by 1) a step of light presented in the dark, 2) an incremental and decremental step from a background illumination, and 3) a white-noise modulated light. 2. For comparison, we recorded the responses of preganglionic cells evoked by the same set of stimuli as used for the ganglion cells. Type-C cells produced on-off transient depolarizations to step stimuli, whether presented in the dark or an illuminated background. Type-N amacrine cells produced complex transient responses to incremental and decremental steps, whereas their step-evoked responses in the dark were sustained polarizations. Bipolar cells produced sustained responses to all step stimuli. 3. Ganglion cells were classified into three types, based on their responses evoked by incremental and decremental steps of light. One class of ganglion cells produced responses similar to those of type-C cells, the second class produced responses similar to those of type-N cells, and the third class resembled bipolar cell responses, although spike discharges accompanied the ganglion cell responses. 4. The analysis of the first-order kernels indicates that the temporal properties of linear dynamic responses are established at the level of bipolar cells and encoded into spike trains of ganglion cells without a major transformation. 5. The second-order nonlinearity appeared at the amacrine cell level. Type-C and type-N cells produced a second-order kernel characteristic of each cell type. The second-order kernels produced in ganglion cells were similar to those produced either by type-C or type-N cells. 6. We conclude that bipolar cells are the major source of linear components of ganglion cell responses and that type-C and type-N amacrine cells are the major source of the nonlinear responses. These linear and second-order nonlinear signals were encoded into spike trains by ganglion cells without a major transformation of the temporal response properties.

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.


2010 ◽  
Vol 103 (1) ◽  
pp. 25-37 ◽  
Author(s):  
Erika D. Eggers ◽  
Peter D. Lukasiewicz

While connections between inhibitory interneurons are common circuit elements, it has been difficult to define their signal processing roles because of the inability to activate these circuits using natural stimuli. We overcame this limitation by studying connections between inhibitory amacrine cells in the retina. These interneurons form spatially extensive inhibitory networks that shape signaling between bipolar cell relay neurons to ganglion cell output neurons. We investigated how amacrine cell networks modulate these retinal signals by selectively activating the networks with spatially defined light stimuli. The roles of amacrine cell networks were assessed by recording their inhibitory synaptic outputs in bipolar cells that suppress bipolar cell output to ganglion cells. When the amacrine cell network was activated by large light stimuli, the inhibitory connections between amacrine cells unexpectedly depressed bipolar cell inhibition. Bipolar cell inhibition elicited by smaller light stimuli or electrically activated feedback inhibition was not suppressed because these stimuli did not activate the connections between amacrine cells. Thus the activation of amacrine cell circuits with large light stimuli can shape the spatial sensitivity of the retina by limiting the spatial extent of bipolar cell inhibition. Because inner retinal inhibition contributes to ganglion cell surround inhibition, in part, by controlling input from bipolar cells, these connections may refine the spatial properties of the retinal output. This functional role of interneuron connections may be repeated throughout the CNS.


1987 ◽  
Vol 90 (2) ◽  
pp. 229-259 ◽  
Author(s):  
M Sakuranaga ◽  
Y Ando ◽  
K Naka

Responses were evoked from ganglion cells in catfish and frog retinas by a Gaussian modulation of the mean luminance. An algorithm was devised to decompose intracellularly recorded responses into the slow and spike components and to extract the time of occurrence of a spike discharge. The dynamics of both signals were analyzed in terms of a series of first-through third-order kernels obtained by cross-correlating the slow (analog) or spike (discrete or point process) signals against the white-noise input. We found that, in the catfish, (a) the slow signals were composed mostly of postsynaptic potentials, (b) their linear components reflected the dynamics found in bipolar cells or in the linear response component of type-N (sustained) amacrine cells, and (c) their nonlinear components were similar to those found in either type-N or type-C (transient) amacrine cells. A comparison of the dynamics of slow and spike signals showed that the characteristic linear and nonlinear dynamics of slow signals were encoded into a spike train, which could be recovered through the cross-correlation between the white-noise input and the spike (point process signals. In addition, well-defined spike correlates could predict the observed slow potentials. In the spike discharges from frog ganglion cells, the linear (or first-order) kernels were all inhibitory, whereas the second-order kernels had characteristics of on-off transient excitation. The transient and sustained amacrine cells similar to those found in catfish retina were the sources of the nonlinear excitation. We conclude that bipolar cells and possibly the linear part of the type-N cell response are the source of linear, either excitatory or inhibitory, components of the ganglion cell responses, whereas amacrine cells are the source of the cells' static nonlinearity.


2018 ◽  
Author(s):  
Robert E. Marc ◽  
Crystal Sigulinsky ◽  
Rebecca L. Pfeiffer ◽  
Daniel Emrich ◽  
James R. Anderson ◽  
...  

AbstractAll superclasses of retinal neurons display some form of electrical coupling including the key neurons of the inner plexiform layer: bipolar cells (BCs), amacrine or axonal cells (ACs) and ganglion cells (GCs). However, coupling varies extensively by class. For example, mammalian rod bipolar cells form no gap junctions at all, while all cone bipolar cells form class-specific coupling arrays, many of them homocellular in-superclass arrays. Ganglion cells are unique in that classes with coupling predominantly form heterocellular cross-class arrays of ganglion cell::amacrine cell (GC::AC) coupling in the mammalian retina. Ganglion cells are the least frequent superclass in the inner plexiform layer and GC::AC gap junctions are sparsely arrayed amidst massive cohorts of AC::AC, bipolar cell BC::BC, and AC::BC gap junctions. Many of these gap junctions and most ganglion cell gap junctions are suboptical, complicating analysis of specific ganglion cells. High resolution 2 nm TEM analysis of rabbit retinal connectome RC1 allows quantitative GC::AC coupling maps of identified ganglion cells. Ganglion cells classes apparently avoid direct cross-class homocellular coupling altogether even though they have opportunities via direct membrane touches, while transient OFF alpha ganglion cells and transient ON directionally selective (DS) ganglion cells are strongly coupled to distinct amacrine / axonal cell cohorts.A key feature of coupled ganglion cells is intercellular metabolite flux. Most GC::AC coupling involves GABAergic cells (γ+ amacrine cells), which results in significant GABA flux into ganglion cells. Surveying GABA coupling signatures in the ganglion cell layer across species suggests that the majority of vertebrate retinas engage in GC::AC coupling.Multi-hop synaptic queries of the entire RC1 connectome clearly profiles the coupled amacrine and axonal cells. Photic drive polarities and source bipolar cell class selec-tivities are tightly matched across coupled cells. OFF alpha ganglion cells are coupled to OFF γ+ amacrine cells and transient ON DS ganglion cells are coupled to ON γ+ amacrine cells including a large interstitial axonal cell (IAC). Synaptic tabulations show close matches between the classes of bipolar cells sampled by the coupled amacrine and ganglion cells. Further, both ON and OFF coupling ganglion networks show a common theme: synaptic asymmetry whereby the coupled γ+ neurons are also presynaptic to ganglion cell dendrites from different classes of ganglion cells outside the coupled set. In effect, these heterocellular coupling patterns enable an excited ganglion cell to directly inhibit nearby ganglion cells of different classes. Similarly, coupled γ+ amacrine cells engaged in feedback networks can leverage the additional gain of bipolar cell synapses in shaping the signaling of a spectrum of downstream targets based on their own selective coupling with ganglion cells.


1994 ◽  
Vol 11 (6) ◽  
pp. 1193-1203 ◽  
Author(s):  
Chen-Yu Yang ◽  
Stephen Yazulla

AbstractThe presence of inhibitory bipolar cells in salamander retina was investigated by a comparative analysis of the distribution of glutamate- and GABA-immunoreactivities (GLU-IR; GABA-IR) using a postembedding immunocytochemical method. GLU-IR was found in virtually all photoreceptors, bipolar cells and ganglion cells, neuronal elements that transfer information vertically through the retina. GLU-IR also was found in numerous amacrine cells in the mid and proximal inner nuclear layer as well as in the cytoplasm of horizontal cells, while the nucleus of horizontal cells was either lightly labeled or not labeled at all. GLU-IR was found in the outer plexiform layer and intensely in the inner plexiform layer, in which there was no apparent sublamination. Forty-seven percent of Type IB bipolar cells in the distal inner nuclear layer and 13% of the displaced bipolar cells were GABA-IR. All bipolar cells were also GLU-IR, indicating that GABA-IR bipolar cells were a subset of GLU-IR bipolar cells rather than a separate population. About 12% of the Type IB bipolar cells were moderately GABA-IR and likely comprised a GABAergic subtype. GLU-IR levels in the presumed GABAergic bipolar cells were higher than in other purely GLU-IR bipolar cells suggesting that these GABA-IR bipolar cells are glutamatergic as well. All of the displaced bipolar cells were only lightly GABA-IR, indicating that displaced bipolar cells comprise a more homogeneous class of glutamatergic cell than orthotopic bipolar cells. GAD-IR co-localized with GABA-IR in orthotopic but not displaced bipolar cells, further supporting the idea that some orthotopic bipolar cells are GABAergic. A small proportion of bipolar cells in salamander retina contain relatively high levels of both GABA and glutamate. Co-release of these substances by bipolar cells could contribute to the “push-pull” modulation of ganglion cell responses.


2019 ◽  
Vol 36 ◽  
Author(s):  
Ashleigh J. Chandra ◽  
Sammy C.S. Lee ◽  
Ulrike Grünert

Abstract In primate retina, the calcium-binding protein calbindin is expressed by a variety of neurons including cones, bipolar cells, and amacrine cells but it is not known which type(s) of cell express calbindin in the ganglion cell layer. The present study aimed to identify calbindin-positive cell type(s) in the amacrine and ganglion cell layer of human and marmoset retina using immunohistochemical markers for ganglion cells (RBPMS and melanopsin) and cholinergic amacrine (ChAT) cells. Intracellular injections following immunolabeling was used to reveal the morphology of calbindin-positive cells. In human retina, calbindin-labeled cells in the ganglion cell layer were identified as inner and outer stratifying melanopsin-expressing ganglion cells, and ON ChAT (starburst amacrine) cells. In marmoset, calbindin immunoreactivity in the ganglion cell layer was absent from ganglion cells but present in ON ChAT cells. In the inner nuclear layer of human retina, calbindin was found in melanopsin-expressing displaced ganglion cells and in at least two populations of amacrine cells including about a quarter of the OFF ChAT cells. In marmoset, a very low proportion of OFF ChAT cells was calbindin-positive. These results suggest that in both species there may be two types of OFF ChAT cells. Consistent with previous studies, the ratio of ON to OFF ChAT cells was about 70 to 30 in human and 30 to 70 in marmoset. Our results show that there are species-related differences between different primates with respect to the expression of calbindin.


1987 ◽  
Vol 58 (6) ◽  
pp. 1329-1350 ◽  
Author(s):  
H. M. Sakai ◽  
K. Naka

1. We analyzed the light-evoked responses of retinal neurons by means of a white-noise technique. Horizontal and bipolar cells produced a modulation response that was linearly related to a modulation of the mean luminance of a large field of light. The first-order kernels were capable of reproducing the cells' modulation response with a fair degree of accuracy. The amplitude as well as the waveform of the kernels changed with the change in the mean luminance. This is a parametric change and is a form of field adaptation. As the time constant of the parametric change was much longer than that of the modulation response (memory), neurons were assumed to be at a dynamic steady state at a given mean luminance. 2. With the presence of a steady annular illumination, the first-order kernel derived from stimulation with a small spot of light became faster in peak response time and larger in amplitude. For horizontal-cell somas and bipolar cells, the surround also linearized their modulation response. This surround enhancement has been seen in all the cone-driven retinal cells except the receptor and horizontal cell axon, in which a steady surround decreased the amplitude of the spot-evoked kernel but shortened the peak response time. 3. A change in the modulation depth did not affect either the amplitude or the wave-form of the first-order kernels from the horizontal and bipolar cells. In the amacrine and ganglion cells, on the other hand, the amplitude of kernels was related inversely to the depth of modulation. These cells were more sensitive to the modulation of a small modulation depth. 4. A static nonlinearity appeared when signals were transmitted to the amacrine cells. The nonlinearity was first produced in the type-C amacrine cells by a process, which could be modeled by squaring the bipolar cell response. A gamut of more complex second-order nonlinearities found in type-N amacrine cells could be modeled by a band-pass filtering of the type-C cell response. Linear components in the bipolar cells and nonlinear components in the amacrine cells are encoded into spike trains in the ganglion cells. Thus, under our simple stimulus regimen, the ganglion cells transformed the results of the preganglionic signal processing into a spike train without much modification. 5. We propose a tentative diagram of the signal flow in the cone-driven catfish retinal neurons based on this and previous studies.(ABSTRACT TRUNCATED AT 400 WORDS)


2019 ◽  
Vol 36 ◽  
Author(s):  
Andrea S. Bordt ◽  
Diego Perez ◽  
Luke Tseng ◽  
Weiley Sunny Liu ◽  
Jay Neitz ◽  
...  

AbstractThere are more than 30 distinct types of mammalian retinal ganglion cells, each sensitive to different features of the visual environment. In rabbit retina, they can be grouped into four classes according to their morphology and stratification of their dendrites in the inner plexiform layer (IPL). The goal of this study was to describe the synaptic inputs to one type of Class IV ganglion cell, the third member of the sparsely branched Class IV cells (SB3). One cell of this type was partially reconstructed in a retinal connectome developed using automated transmission electron microscopy (ATEM). It had slender, relatively straight dendrites that ramify in the sublamina a of the IPL. The dendrites of the SB3 cell were always postsynaptic in the IPL, supporting its identity as a ganglion cell. It received 29% of its input from bipolar cells, a value in the middle of the range for rabbit retinal ganglion cells studied previously. The SB3 cell typically received only one synapse per bipolar cell from multiple types of presumed OFF bipolar cells; reciprocal synapses from amacrine cells at the dyad synapses were infrequent. In a few instances, the bipolar cells presynaptic to the SB3 ganglion cell also provided input to an amacrine cell presynaptic to the ganglion cell. There was apparently no crossover inhibition from narrow-field ON amacrine cells. Most of the amacrine cell inputs were from axons and dendrites of GABAergic amacrine cells, likely providing inhibitory input from outside the classical receptive field.


1992 ◽  
Vol 9 (3-4) ◽  
pp. 313-323 ◽  
Author(s):  
David M. Sherry ◽  
Robert J. Ulshafer

AbstractImmunocytochemical and autoradiographic methods were used to identify neurons in the pure cone retina of the lizard (Anolis carolinensis) that are likely to employ glutamate (GLU) or aspartate (ASP) as a neurotransmitter.GLU immunocytochemistry demonstrated high levels of endogenous GLU in all cone types and numerous bipolar cells. Moderate GLU levels were found in horizontal and ganglion cells. Müller cells and most amacrine cells had very low GLU levels. GLU immunoreactivity (GLU-IR) in the cones was present from the inner segment to the synaptic pedicle. A large spherical cell type with moderate GLU-IR was identified in the proximal inner plexiform layer (IPL). These cells also contain ASP and have been tentatively identified as amacrine cells. Uptake of [3H]-L-GLU labeled all retinal layers. All cone types and Müller cells sequestered [3H]-D-ASP, a substrate specific for the GLU transporter.Anti-ASP labeling was observed in cones, horizontal cells, amacrine cells, and cells in the ganglion cell layer. ASP immunoreactivity (ASP-IR) in the cones was confined to the inner segment. One ASP-containing pyriform amacrine cell subtype ramifying in IPL sublamina b was identified.Analysis of GLU-IR, ASP-IR, and GABA-IR on serial sections indicated that there were two distinct populations of horizontal cells in the Anolis retina: one containing GABA-IR, GLU-IR, and ASP-IR; and another type containing only GLU-IR and ASP-IR. Light GLU-IR was frequently found in GABA-containing amacrine cells but ASP-IR was not.The distinct distributions of GLU and ASP may indicate distinctly different roles for these amino acids. GLU, not ASP, is probably the major neurotransmitter in the cone-biploar-ganglion cell pathway of the Anolis retina. Both GLU and ASP are present in horizontal cells and specific subpopulations of amacrine cells, but it is unclear if GLU or ASP have a neurotransmitter role in these cells.


1979 ◽  
Vol 74 (6) ◽  
pp. 671-689 ◽  
Author(s):  
J D Victor ◽  
R M Shapley

Retinal ganglion cells of the Y type in the cat retina produce two different types of response: linear and nonlinear. The nonlinear responses are generated by a separate and independent nonlinear pathway. The functional connectivity in this pathway is analyzed here by comparing the observed second-order frequency responses of Y cells with predictions of a "sandwich model" in which a static nonlinear stage is sandwiched between two linear filters. The model agrees well with the qualitative and quantitative features of the second-order responses. The prefilter in the model may well be the bipolar cells and the nonlinearity and postfilter in the model are probably associated with amacrine cells.


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