Amacrine cell contributions to red-green color opponency in central primate retina: A model study

To investigate the contributions of amacrine cells to red-green opponency, a linear computational model of the central macaque retina was developed based on a published cone mosaic. In the model, amacrine cells of ON and OFF types received input from all neighboring midget bipolar cells of the same polarity, but OFF amacrine cells had a bias toward bipolar cells whose center responses were mediated by middle wavelength sensitive cones. This bias might arise due to activity dependent plasticity because there are midget bipolar cells driven by short wavelength sensitive cones in the OFF pathway. The model midget ganglion cells received inputs from neighboring amacrine cells of both types. As in physiological experiments, the model ganglion cells showed spatially opponent responses to achromatic stimuli, but they responded to cone isolating stimuli as though center and surround were each driven by a single cone type. Without amacrine cell input, long and middle wavelength sensitive cones contributed to both the centers and surrounds of model ganglion cell receptive fields. According to the model, the summed amacrine cell input was red-green opponent even though inputs to individual amacrine cells were unselective. A key prediction is that GABA and glycine depolarize two of the four types of central midget ganglion cells; this may reflect lower levels of the potassium chloride co-transporter in their dendrites.

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The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina

Visual Neuroscience ◽

10.1017/s0952523800007744 ◽

1996 ◽

Vol 13 (6) ◽

pp. 1099-1107 ◽

Cited By ~ 6

Author(s):

Péter Buzás ◽

Sára Jeges ◽

Robert Gábriel

Keyword(s):

Ganglion Cell ◽

Cross Sections ◽

Information Transfer ◽

Ganglion Cells ◽

Receptive Fields ◽

Plexiform Layer ◽

Amacrine Cells ◽

Bipolar Cells ◽

Inner Plexiform Layer ◽

Flow Through

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.

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Interneuron Circuits Tune Inhibition in Retinal Bipolar Cells

Journal of Neurophysiology ◽

10.1152/jn.00458.2009 ◽

2010 ◽

Vol 103 (1) ◽

pp. 25-37 ◽

Cited By ~ 45

Author(s):

Erika D. Eggers ◽

Peter D. Lukasiewicz

Keyword(s):

Ganglion Cell ◽

Bipolar Cell ◽

Amacrine Cell ◽

Ganglion Cells ◽

Feedback Inhibition ◽

Amacrine Cells ◽

Bipolar Cells ◽

Light Stimuli ◽

Cell Inhibition ◽

Cell Networks

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.

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Heterocellular coupling between amacrine cell and ganglion cells

10.1101/328815 ◽

2018 ◽

Author(s):

Robert E. Marc ◽

Crystal Sigulinsky ◽

Rebecca L. Pfeiffer ◽

Daniel Emrich ◽

James R. Anderson ◽

...

Keyword(s):

Gap Junctions ◽

Ganglion Cell ◽

Bipolar Cell ◽

Amacrine Cell ◽

Ganglion Cells ◽

Plexiform Layer ◽

Amacrine Cells ◽

Bipolar Cells ◽

Inner Plexiform Layer ◽

Tem Analysis

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.

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Center-surround interactions underlie bipolar cell motion sensing in the mouse retina

10.1101/2021.05.31.446404 ◽

2021 ◽

Author(s):

Sarah Strauss ◽

Maria M Korympidou ◽

Yanli Ran ◽

Katrin Franke ◽

Timm Schubert ◽

...

Keyword(s):

Bipolar Cell ◽

Ganglion Cells ◽

Receptive Fields ◽

Amacrine Cells ◽

Bipolar Cells ◽

Mouse Retina ◽

Motion Processing ◽

Local Motion ◽

Motion Sensing ◽

Motion Sensitivity

Motion is a critical aspect of vision. We studied the representation of motion in mouse retinal bipolar cells and found, surprisingly, that some bipolar cells possess motion-sensing capabilities that rely on their center-surround receptive fields. Using a glutamate sensor, we directly observed motion-sensitive bipolar cell synaptic output, which was strongest for local motion and dependent on the motion's origin. We characterized bipolar cell receptive fields and found that there are motion and non-motion sensitive bipolar cell types, the majority being motion sensitive. Next, we used these bipolar cell receptive fields along with connectomics to design biophysical models of downstream cells. The models and experiments demonstrated that bipolar cells pass motion-sensitive excitation to starburst amacrine cells through direction-specific signals mediated by bipolar cells' center-surround receptive field structure. As bipolar cells provide excitation to most amacrine and ganglion cells, their motion sensitivity may contribute to motion processing throughout the visual system.

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Synaptic inputs from identified bipolar and amacrine cells to a sparsely branched ganglion cell in rabbit retina

Visual Neuroscience ◽

10.1017/s0952523819000014 ◽

2019 ◽

Vol 36 ◽

Cited By ~ 4

Author(s):

Andrea S. Bordt ◽

Diego Perez ◽

Luke Tseng ◽

Weiley Sunny Liu ◽

Jay Neitz ◽

...

Keyword(s):

Ganglion Cell ◽

Retinal Ganglion Cells ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Bipolar Cells ◽

Rabbit Retina ◽

Retinal Ganglion ◽

Synaptic Inputs ◽

Class Iv

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.

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Stratification of alpha ganglion cells and ON/OFF directionally selective ganglion cells in the rabbit retina

Visual Neuroscience ◽

10.1017/s0952523805224148 ◽

2005 ◽

Vol 22 (4) ◽

pp. 535-549 ◽

Cited By ~ 17

Author(s):

JIAN ZHANG ◽

WEI LI ◽

HIDEO HOSHI ◽

STEPHEN L. MILLS ◽

STEPHEN C. MASSEY

Keyword(s):

Bipolar Cell ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Bipolar Cells ◽

Confocal Imaging ◽

Rabbit Retina ◽

Firing Rates ◽

Starburst Amacrine Cells ◽

Cholinergic Sensitivity

The correlation between cholinergic sensitivity and the level of stratification for ganglion cells was examined in the rabbit retina. As examples, we have used ON or OFF α ganglion cells and ON/OFF directionally selective (DS) ganglion cells. Nicotine, a cholinergic agonist, depolarized ON/OFF DS ganglion cells and greatly enhanced their firing rates but it had modest excitatory effects on ON or OFF α ganglion cells. As previously reported, we conclude that DS ganglion cells are the most sensitive to cholinergic drugs. Confocal imaging showed that ON/OFF DS ganglion cells ramify precisely at the level of the cholinergic amacrine cell dendrites, and co-fasciculate with the cholinergic matrix of starburst amacrine cells. However, neither ON or OFF α ganglion cells have more than a chance association with the cholinergic matrix. Z-axis reconstruction showed that OFF α ganglion cells stratify just below the cholinergic band in sublamina a while ON α ganglion cells stratify just below cholinergic b. The latter is at the same level as the terminals of calbindin bipolar cells. Thus, the calbindin bipolar cell appears to be a prime candidate to provide the bipolar cell input to ON α ganglion cells in the rabbit retina. We conclude that the precise level of stratification is correlated with the strength of cholinergic input. Alpha ganglion cells receive a weak cholinergic input and they are narrowly stratified just below the cholinergic bands.

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Functional organization of catfish retina

Journal of Neurophysiology ◽

10.1152/jn.1977.40.1.26 ◽

1977 ◽

Vol 40 (1) ◽

pp. 26-43 ◽

Cited By ~ 125

Author(s):

K. Naka

Keyword(s):

Receptive Field ◽

Ganglion Cell ◽

Functional Organization ◽

Ganglion Cells ◽

Horizontal Cell ◽

Receptive Fields ◽

Amacrine Cells ◽

Type A ◽

Bipolar Cells ◽

The Other

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.

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Amacrine cell-mediated input to bipolar cells: Variations on a common mechanistic theme

Visual Neuroscience ◽

10.1017/s0952523811000241 ◽

2012 ◽

Vol 29 (1) ◽

pp. 41-49 ◽

Cited By ~ 11

Author(s):

WILLIAM N. GRIMES

Keyword(s):

Visual Processing ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Negative Influence ◽

Bipolar Cells ◽

Single Class ◽

Anatomy And Physiology ◽

Functional Context ◽

The Brain

AbstractFeedback is a ubiquitous feature of neural circuits in the mammalian central nervous system (CNS). Analogous to pure electronic circuits, neuronal feedback provides either a positive or negative influence on the output of upstream components/neurons. Although the particulars (i.e., connectivity, physiological encoding/processing/signaling) of circuits in higher areas of the brain are often unclear, the inner retina proves an excellent model for studying both the anatomy and physiology of feedback circuits within the functional context of visual processing. Inner retinal feedback to bipolar cells is almost entirely mediated by a single class of interneurons, the amacrine cells. Although this might sound like a simple circuit arrangement with an equally simple function, anatomical, molecular, and functional evidence suggest that amacrine cells represent an extremely diverse class of CNS interneurons that contribute to a variety of retinal processes. In this review, I classify the amacrine cells according to their anatomical output synapses and target cell(s) (i.e., bipolar cells, ganglion cells, and/or amacrine cells) and discuss specifically our current understandings of amacrine cell-mediated feedback and output to bipolar cells on the synaptic, cellular, and circuit levels, while drawing connections to visual processing.

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Suppressive rod-cone interaction in distal vertebrate retina: intracellular records from Xenopus and Necturus

Journal of Neurophysiology ◽

10.1152/jn.1987.57.5.1361 ◽

1987 ◽

Vol 57 (5) ◽

pp. 1361-1382 ◽

Cited By ~ 39

Author(s):

T. E. Frumkes ◽

T. Eysteinsson

Keyword(s):

Intracellular Recording ◽

Light Adaptation ◽

Ganglion Cells ◽

Small Diameter ◽

Amacrine Cells ◽

Underlying Mechanism ◽

Bipolar Cells ◽

Enhancement Effect ◽

Inhibitory Influence ◽

Color Opponency

The influence of dim diffuse adapting fields upon the sensitivity to focal photic stimulation was studied by means of intracellular recording in retinal neurons of the south african clawed frog, Xenopus and the mudpuppy, Necturus. In cones and in most horizontal and bipolar cells lacking color opponency, dim diffuse backgrounds have little influence upon the response to diffuse flicker of low (less than 2 Hz) temporal frequencies; however, with small diameter test probes of higher temporal frequencies, presentation of dim backgrounds enhance the peak-to-peak amplitude of responses to sinusoidal flicker by as much as 800%. This background enhancement effect adheres to the spectral sensitivity of the green-absorbing rod photopigment, and appears to be largely independent of the influence of the adapting field upon cone photopigment or ambient membrane potential in the recorded neuron. This effect cannot be obtained with rod-driven flicker responses. We designate this background influence on flicker, suppressive rod-cone interaction (SRCI) and attribute it to a tonic suppressive (probably inhibitory) influence of rods upon cone pathways that is removed by rod light adaptation. SRCI is also observed in the response of most sustained ON and OFF ganglion cells. However, no corresponding effect occurs in rods, color-opponent second-order neurons, ON-OFF amacrine cells, or most ON-OFF ganglion cells. The spatial and temporal limitations of SRCI observed by means of intracellular recording in amphibians are very similar to those documented by means of psychophysical or electroretinogram (ERG) procedures in a wide variety of species including humans (2, 4, 11, 22, 23, 29). SRCI most probably reflects a process that is mediated by horizontal cells. The specifics of the underlying mechanism remain unclear.

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Intrinsic properties and functional circuitry of the AII amacrine cell

Visual Neuroscience ◽

10.1017/s0952523811000368 ◽

2012 ◽

Vol 29 (1) ◽

pp. 51-60 ◽

Cited By ~ 85

Author(s):

JONATHAN B. DEMB ◽

JOSHUA H. SINGER

Keyword(s):

Visual Processing ◽

Amacrine Cell ◽

Ganglion Cells ◽

Amacrine Cells ◽

Cell Types ◽

Bipolar Cells ◽

Retinal Neuron ◽

Motion Sensitivity ◽

Network Properties ◽

Aii Amacrine

AbstractAmacrine cells represent the most diverse class of retinal neuron, comprising dozens of distinct cell types. Each type exhibits a unique morphology and generates specific visual computations through its synapses with a subset of excitatory interneurons (bipolar cells), other amacrine cells, and output neurons (ganglion cells). Here, we review the intrinsic and network properties that underlie the function of the most common amacrine cell in the mammalian retina, the AII amacrine cell. The AII connects rod and cone photoreceptor pathways, forming an essential link in the circuit for rod-mediated (scotopic) vision. As such, the AII has become known as the rod–amacrine cell. We, however, now understand that AII function extends to cone-mediated (photopic) vision, and AII function in scotopic and photopic conditions utilizes the same underlying circuit: AIIs are electrically coupled to each other and to the terminals of some types of ON cone bipolar cells. The direction of signal flow, however, varies with illumination. Under photopic conditions, the AII network constitutes a crossover inhibition pathway that allows ON signals to inhibit OFF ganglion cells and contributes to motion sensitivity in certain ganglion cell types. We discuss how the AII’s combination of intrinsic and network properties accounts for its unique role in visual processing.

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