scholarly journals Morphology and function of three VIP-expressing amacrine cell types in the mouse retina

2015 ◽  
Vol 114 (4) ◽  
pp. 2431-2438 ◽  
Author(s):  
Alejandro Akrouh ◽  
Daniel Kerschensteiner

Amacrine cells (ACs) are the most diverse class of neurons in the retina. The variety of signals provided by ACs allows the retina to encode a wide range of visual features. Of the 30–50 AC types in mammalian species, few have been studied in detail. Here, we combine genetic and viral strategies to identify and to characterize morphologically three vasoactive intestinal polypeptide-expressing GABAergic AC types (VIP1-, VIP2-, and VIP3-ACs) in mice. Somata of VIP1- and VIP2-ACs reside in the inner nuclear layer and somata of VIP3-ACs in the ganglion cell layer, and they show asymmetric distributions along the dorsoventral axis of the retina. Neurite arbors of VIP-ACs differ in size (VIP1-ACs ≈ VIP3-ACs > VIP2-ACs) and stratify in distinct sublaminae of the inner plexiform layer. To analyze light responses and underlying synaptic inputs, we target VIP-ACs under 2-photon guidance for patch-clamp recordings. VIP1-ACs depolarize strongly to light increments (ON) over a wide range of stimulus sizes but show size-selective responses to light decrements (OFF), depolarizing to small and hyperpolarizing to large stimuli. The switch in polarity of OFF responses is caused by pre- and postsynaptic surround inhibition. VIP2- and VIP3-ACs both show small depolarizations to ON stimuli and large hyperpolarizations to OFF stimuli but differ in their spatial response profiles. Depolarizations are caused by ON excitation outweighing ON inhibition, whereas hyperpolarizations result from pre- and postsynaptic OFF-ON crossover inhibition. VIP1-, VIP2-, and VIP3-ACs thus differ in response polarity and spatial tuning and contribute to the diversity of inhibitory and neuromodulatory signals in the retina.

2021 ◽  
Author(s):  
Miloslav Sedlacek ◽  
William Grimes ◽  
Morgan Musgrove ◽  
Amurta Nath ◽  
Hua Tian ◽  
...  

In retinal neurons, morphology strongly influences visual response features. Ganglion cell (GC) dendrites ramify in distinct strata of the inner plexiform layer (IPL) so that GCs responding to light increments (ON) or decrements (OFF) receive appropriate excitatory inputs. This vertical stratification prescribes response polarity and ensures consistent connectivity between cell types, whereas the lateral extent of GC dendritic arbors typically dictates receptive field (RF) size. Here, we identify circuitry in mouse retina that contradicts these conventions. A2 amacrine cells are interneurons understood to mediate 'cross-over' inhibition by relaying excitatory input from the ON layer to inhibitory outputs in the OFF layer. Ultrastructural and physiological analyses show, however, that some A2s deliver powerful inhibition to OFF GC somas and proximal dendrites in the ON layer, rendering their inhibitory RFs smaller than their dendritic arbors. This OFF pathway, avoiding entirely the OFF region of the IPL, challenges several tenets of retinal circuitry.


2012 ◽  
Vol 29 (1) ◽  
pp. 11-29 ◽  
Author(s):  
CHI ZHANG ◽  
MAUREEN A. McCALL

AbstractAmacrine cells are a morphologically and functionally diverse group of inhibitory interneurons. Morphologically, they have been divided into approximately 30 types. Although this diversity is probably important to the fine structure and function of the retinal circuit, the amacrine cells have been more generally divided into two subclasses. Glycinergic narrow-field amacrine cells have dendrites that ramify close to their somas, cross the sublaminae of the inner plexiform layer, and create cross talk between its parallel ON and OFF pathways. GABAergic wide-field amacrine cells have dendrites that stretch long distances from their soma but ramify narrowly within an inner plexiform layer sublamina. These wide-field cells are thought to mediate inhibition within a sublamina and thus within the ON or OFF pathway. The postsynaptic targets of all amacrine cell types include bipolar, ganglion, and other amacrine cells. Almost all amacrine cells use GABA or glycine as their primary neurotransmitter, and their postsynaptic receptor targets include the most common GABAA, GABAC, and glycine subunit receptor configurations. This review addresses the diversity of amacrine cells, the postsynaptic receptors on their target cells in the inner plexiform layer of the retina, and some of the inhibitory mechanisms that arise as a result. When possible, the effects of GABAergic and glycinergic inputs on the visually evoked responses of their postsynaptic targets are discussed.


1992 ◽  
Vol 9 (3-4) ◽  
pp. 279-290 ◽  
Author(s):  
Dennis M. Dacey ◽  
Sarah Brace

AbstractIntracellular injections of Neurobiotin were used to determine whether the major ganglion cell classes of the macaque monkey retina, the magnocellular-projecting parasol, and the parvocellular-projecting midget cells showed evidence of cellular coupling similar to that recently described for cat retinal ganglion cells. Ganglion cells were labeled with the fluorescent dye acridine orange in an in vitro, isolated retina preparation and were selectively targeted for intracellular injection under direct microscopic control. The macaque midget cells, like the beta cells of the cat's retina, showed no evidence of tracer coupling when injected with Neurobiotin. By contrast, Neurobiotin-filled parasol cells, like cat alpha cells, showed a distinct pattern of tracer coupling to each other (homotypic coupling) and to amacrine cells (heterotypic coupling).In instances of homotypic coupling, the injected parasol cell was surrounded by a regular array of 3–6 neighboring parasol cells. The somata and proximal dendrites of these tracer-coupled cells were lightly labeled and appeared to costratify with the injected cell. Analysis of the nearest-neighbor distances for the parasol cell clusters showed that dendritic-field overlap remained constant as dendritic-field size increased from 100–400 μm in diameter.At least two amacrine cell types showed tracer coupling to parasol cells. One amacrine type had a small soma and thin, sparsely branching dendrites that extended for 1–2 mm in the inner plexiform layer. A second amacrine type had a relatively large soma, thick main dendrites, and distinct, axon-like processes that extended for at least 2–3 mm in the inner plexiform layer. The main dendrites of the large amacrine cells were closely apposed to the dendrites of parasol cells and may be the site of Neurobiotin transfer between the two cell types. We suggest that the tracer coupling between neighboring parasol cells takes place indirectly via the dendrites of the large amacrine cells and provides a mechanism, absent in midget cells, for increasing parasol cell receptive-field size and luminance contrast sensitivity.


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.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Thomas A Ray ◽  
Suva Roy ◽  
Christopher Kozlowski ◽  
Jingjing Wang ◽  
Jon Cafaro ◽  
...  

A common strategy by which developing neurons locate their synaptic partners is through projections to circuit-specific neuropil sublayers. Once established, sublayers serve as a substrate for selective synapse formation, but how sublayers arise during neurodevelopment remains unknown. Here, we identify the earliest events that initiate formation of the direction-selective circuit in the inner plexiform layer of mouse retina. We demonstrate that radially migrating newborn starburst amacrine cells establish homotypic contacts on arrival at the inner retina. These contacts, mediated by the cell-surface protein MEGF10, trigger neuropil innervation resulting in generation of two sublayers comprising starburst-cell dendrites. This dendritic scaffold then recruits projections from circuit partners. Abolishing MEGF10-mediated contacts profoundly delays and ultimately disrupts sublayer formation, leading to broader direction tuning and weaker direction-selectivity in retinal ganglion cells. Our findings reveal a mechanism by which differentiating neurons transition from migratory to mature morphology, and highlight this mechanism’s importance in forming circuit-specific sublayers.


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.


1990 ◽  
Vol 5 (04) ◽  
pp. 371-378 ◽  
Author(s):  
Baosong Zhu ◽  
Charles Straznicky

AbstractUsing an antibody against serotonin (5-hydroxytryptamine, 5-HT), serotonin-like immunoreactive (serotonin IR) neurons were demonstrated in the retina of adultBufo marinus. All immunoreactive neurons were identified as amacrine cells (ACs). The dendrites of serotonin-IR ACs branched diffusely and densely throughout all levels of the inner plexiform layer (IPL) of the retina. The great majority of these cell somata were located in the vitread part of the inner nuclear layer (INL) and a few of them (ranging from 9–29 cells) were displaced into the ganglion cell layer (GCL). On the basis of the soma sizes, two populations of serotonin-IR ACs, large (type A) and small (type B), were distinguished. 6-Hydroxydopamine (6-OHDA) injected into the eye abolished immunoreactivity in the recently reported tyrosine hydroxylase (TH)-IR ACs (Zhu & Straznicky, 1990), whereas serotonin-IR ACs remained unaffected.The number of serotonin-IR cells per retina ranged from 23,750–27,390, with a ratio of 1:1.6 to 1:1.9 between type A and B cells. Both cell types were distributed nonuniformly across the retina. Cell densities were slightly lower in the peripheral (96 cells/mm2) than in the central (164 cells/mm2) retina. Linear regression analysis confirmed the presence of a decreasing density gradient from the retinal center to the retinal margin for both small and large cell types. The analysis of the nearest neighbor distances showed that the retinal distribution of serotonin-IR ACs was orderly.These results have been taken to indicate that 5-HT-IR cells correspond to a population of serotonincontaining ACs. It is suggested that dopamine and serotonin are contained in two different populations of ACs in the rtina ofBufo marinus.


1995 ◽  
Vol 74 (6) ◽  
pp. 2460-2468 ◽  
Author(s):  
R. F. Dacheux ◽  
E. Raviola

1. The light responses from one type of ON-OFF amacrine cell were recorded intracellularly in the superfused rabbit retina under various conditions of light adaptation. These recordings were obtained from cells located in a central area. 5-7 mm inferior and directly below the optic nerve head. 2. ON-OFF amacrine cells responded to the initiation and termination of light stimuli with transient depolarizations. Their receptive fields were approximately 0.8-1 mm diam and did not exhibit antagonistic center-and-surround organization. 3. The cells received rod input because they responded to very dim scotopic stimuli. With prolonged dark adaptation, the cells became more sensitive to the initiation than termination of the stimulus, because the ON component of the light response had a lower threshold than the OFF component. 4. The cells continued to respond to test flashes when the retina was adapted to a background illumination of rod-saturating intensity. Thus ON-OFF amacrine cells also receive cone input. Under these photopic conditions, a secondary afterpotential was observed following the OFF component. Its characteristics were different from those of the rod aftereffect reported in other retinal cells of the rabbit because its latency and amplitude changed with increasing stimulus intensity. 5. Intracellular injections of horseradish peroxidase showed that the recordings were obtained from a class of ON-OFF amacrine cells whose wide-field, unistratified dendrites were rigorously confined to the middle of the inner plexiform layer or stratum 3. 6. The conspicuous rod and cone inputs into a class of amacrine cells that are connected neither to rod bipolars nor to All amacrine cells strongly support the idea that in the rabbit the rod pathway uses cone bipolars as interneurons to distribute scotopic signals to ganglion and cone-driven amacrine cells.


2001 ◽  
Vol 86 (5) ◽  
pp. 2285-2298 ◽  
Author(s):  
Ko Matsui ◽  
Jun Hasegawa ◽  
Masao Tachibana

In many vertebrate CNS synapses, the neurotransmitter glutamate activates postsynaptic non- N-methyl-d-aspartate (NMDA) and NMDA receptors. Since their biophysical properties are quite different, the time course of excitatory postsynaptic currents (EPSCs) depends largely on the relative contribution of their activation. To investigate whether the activation of the two receptor subtypes is affected by the synaptic interaction in the inner plexiform layer (IPL) of the mouse retina, we analyzed the properties of the light-evoked responses ofon-cone bipolar cells and on-transient amacrine cells in a retinal slice preparation. on-transient amacrine cells were whole cell voltage-clamped, and the glutamatergic synaptic input from bipolar cells was isolated by a cocktail of pharmacological agents (bicuculline, strychnine, curare, and atropine). Direct puff application of NMDA revealed the presence of functional NMDA receptors. However, the light-evoked EPSC was not significantly affected byd(−)-2-amino-5-phosphonopentanoic acid (d-AP5), but suppressed by 2,3-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulfonamide (NBQX) or 1-(4-aminophenyl)-4-methyl-7,8-methylenedioxy-5H-2,3-benzodiazepine hydrochloride (GYKI 52466). These results indicate that the light-evoked EPSC is mediated mainly by AMPA receptors under this condition. Since bipolar cells have GABACreceptors at their terminals, it has been suggested that bipolar cells receive feedback inhibition from amacrine cells. Application of (1,2,5,6-tetrahydropyridin-4-yl)methylphosphinic acid (TPMPA), a specific blocker of GABAC receptors, suppressed both the GABA-induced current and the light-evoked feedback inhibition observed in on-cone bipolar cells and enhanced the light-evoked EPSC of on-transient amacrine cells. In the presence of TPMPA, the light-evoked EPSC of amacrine cells was composed of AMPA and NMDA receptor-mediated components. Our results suggest that photoresponses of on-transient amacrine cells in the mouse retina are modified by the activation of presynaptic GABAC receptors, which may control the extent of glutamate spillover.


1999 ◽  
Vol 16 (6) ◽  
pp. 1105-1114 ◽  
Author(s):  
PU QIN ◽  
ROBERTA G. POURCHO

AMPA-selective glutamate receptors play a major role in glutamatergic neurotransmission in the retina and are expressed in a variety of neuronal subpopulations. In the present study, immunocytochemical techniques were used to visualize the distribution of GluR2 and GluR4 subunits in the cat retina. Results were compared with previous localizations of GluR1 and GluR2/3. Staining for GluR2 was limited to a small number of amacrine and ganglion cells whereas GluR4 staining was present in A-type horizontal cells, many amacrine cells including type AII amacrine cells, and the majority of the cells in the ganglion cell layer. Analysis of synaptic relationships in the outer plexiform layer showed the GluR4 subunit to be concentrated at the contacts of cone photoreceptors with A-horizontal cells. In the inner plexiform layer, both GluR2 and GluR4 were postsynaptic to cone bipolar cells at dyad contacts although GluR2 staining was limited to one of the postsynaptic elements whereas GluR4 immunoreactivity was often seen in both postsynaptic elements. Unlike GluR2, GluR4 was also postsynaptic to rod bipolar cells where it could be visualized in processes of AII amacrine cells. The data indicate that GluR3 and GluR4 subunits are colocalized in a number of cell types including A-type horizontal cells, AII amacrine cells, and alpha ganglion cells, but whether they are combined in the same multimeric receptors remains to be determined.


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