‘Starburst’ amacrine cells and cholinergic neurons: mirror-symmetric ON and OFF amacrine cells of rabbit retina

1983 ◽  
Vol 261 (1) ◽  
pp. 138-144 ◽  
Author(s):  
Edward V. Famiglietti
Keyword(s):  
Cholinergic Neurons ◽  
Amacrine Cells ◽  
Rabbit Retina ◽  
Starburst Amacrine Cells

Development of excitatory and inhibitory neurotransmitters in transitory cholinergic neurons, starburst amacrine cells, and GABAergic amacrine cells of rabbit retina, with implications for previsual and visual development of retinal ganglion cells

2010 ◽  
Vol 27 (1-2) ◽  
pp. 19-42 ◽  
Author(s):  
EDWARD V. FAMIGLIETTI ◽  
SARAH J. SUNDQUIST
Keyword(s):  
Ganglion Cells ◽  
Cholinergic Neurons ◽  
Amacrine Cells ◽  
Visual Development ◽  
Adult Rabbit ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Ultrastructural Studies ◽  
Adult Pattern ◽  
Starburst Amacrine Cells

AbstractStarburst amacrine cells (SACs), the only acetylcholine (ACh)-releasing amacrine cells (ACs) in adult rabbit retina, contain GABA and are key elements in the retina’s directionally selective (DS) mechanism. Unlike many other GABAergic ACs, they use glutamic acid decarboxlyase (GAD)67, not GAD65, to synthesize GABA. Using immunocytochemistry, we demonstrate the apoptosis at birth (P0) of transitory putative ACs that exhibit immunoreactivity (IR) for the ACh-synthetic enzyme choline acetyltransferase (ChAT), GAD67, and the GABA transporter, GAT1. Only a few intact, displaced ChAT-immunoreactive SAC bodies are detected at P0. At P2, ChAT-IR is detected in the two narrowly stratified substrata of starburst dendrites in the inner plexiform layer (IPL). Quantitative analysis reveals that in the first postnatal week, only a small fraction of SACs cells express ChAT- and GABA-IR. Not until the end of the second week are they expressed in all SACs. At P0, a three-tiered stratification of GABA-IR is present in the IPL, entirely different from the adult pattern of seven substrata, emerging at P3–P4, and optimally visualized at P13. At P0, GAD65 is detectable in normally placed AC bodies. At P1, GAD65-IR appears in dendrites of nonstarburst GABAergic ACs, and by P5 is robust in the adult pattern of four substrata in the IPL. GAD65-IR never co-localizes with ChAT-IR. In a temporal comparison of our data with physiological, pharmacological, and ultrastructural studies, we suggest that transitory ChAT-immunoreactive cells share with SACs production of stage II (nicotinic) waves of previsual synchronous activity in ganglion cells (GCs). Further, we conclude that (1) GAD65-immunoreactive, non-SAC GABAergic ACs are the most likely candidates responsible for the suppression of stage III (muscarinic/AMPA-kainate) waves and (2) DS responses first appear in DS GCs, when about 50% of SACs express ChAT- and GABA-IR, and in 100% of DS GCs, when expression occurs in all SACs.

Neural architecture of the “transient” ON directionally selective (class IIb1) ganglion cells in rabbit retina, partly co-stratified with starburst amacrine cells

2016 ◽  
Vol 33 ◽  
Author(s):  
EDWARD V. FAMIGLIETTI
Keyword(s):  
T Cells ◽  
Ganglion Cell ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Dendritic Morphology ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Branching Pattern ◽  
Stimulus Velocity ◽  
Starburst Amacrine Cells

AbstractRecent physiological studies coupled with intracellular staining have subdivided ON directionally selective (DS) ganglion cells of rabbit retina into two types. One exhibits more “transient” and more “brisk” responses (ON DS-t), and the other has more “sustained’ and more “sluggish” responses (ON DS-s), although both represent the same three preferred directions and show preference for low stimulus velocity, as reported in previous studies of ON DS ganglion cells in rabbit retina. ON DS-s cells have the morphology of ganglion cells previously shown to project to the medial terminal nucleus (MTN) of the accessory optic system, and the MTN-projecting, class IVus1 cells have been well-characterized previously in terms of their dendritic morphology, branching pattern, and stratification. ON DS-t ganglion cells have a distinctly different morphology and exhibit heterotypic coupling to amacrine cells, including axon-bearing amacrine cells, with accompanying synchronous firing, while ON DS-s cells are not coupled. The present study shows that ON DS-t cells are morphologically identical to the previously well-characterized, “orphan” class IIb1 ganglion cell, previously regarded as a member of the “brisk-concentric” category of ganglion cells. Its branching pattern, quantitatively analyzed, is similar to that of the morphological counterparts of X and Y cells, and very different from that of the ON DS-s ganglion cell. Close analysis of the dendritic stratification of class IIb1 ganglion cells together with fiducial cells indicates that they differ from that of the ON DS-s cells. In agreement with one of the three previous studies, class IIb1/ON DS-t cells, unlike class IVus1/ON DS-s ganglion cells, in the main do not co-stratify with starburst amacrine cells. As the present study shows, however, portions of their dendrites do deviate from the main substratum, coming within range of starburst boutons. Parsimony favors DS input from starburst amacrine cells both to ON DS-s and to ON DS-t ganglion cells, given the similarity of their DS responses, but further studies will be required to substantiate the origin of the DS responses of ON DS-t cells. Previously reported OFF DS responses in ON DS-t cells, unmasked by pharmacological agents, and mediated by gap junctions with amacrine cells, suggests an unusual trans-sublaminar organization of directional selectivity in the inner plexiform layer, connecting sublamina a and sublamina b.

scholarly journals AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina

2003 ◽  
Vol 466 (1) ◽  
pp. 80-90 ◽  
Author(s):  
Sally I. Firth ◽  
Wei Li ◽  
Stephen C. Massey ◽  
David W. Marshak
Keyword(s):  
Ampa Receptors ◽  
Acetylcholine Release ◽  
Amacrine Cells ◽  
Rabbit Retina ◽  
Starburst Amacrine Cells

Pharmacology of Directionally Selective Ganglion Cells in the Rabbit Retina

1997 ◽  
Vol 77 (2) ◽  
pp. 675-689 ◽  
Author(s):  
Christopher A. Kittila ◽  
Stephen C. Massey
Keyword(s):  
Ganglion Cells ◽  
Amacrine Cells ◽  
Gaba Release ◽  
Excitatory Input ◽  
Directional Selectivity ◽  
Dependent Manner ◽  
Rabbit Retina ◽  
Response Curves ◽  
Wide Range ◽  
Starburst Amacrine Cells

Kittila, Christopher A. and Stephen C. Massey. Pharmacology of directionally selective ganglion cells in the rabbit retina. J. Neurophysiol. 77: 675–689, 1997. In this report we describe extracellular recordings made from on and on-off directionally selective (DS) ganglion cells in the rabbit retina during perfusion with agonists and antagonists to acetylcholine (ACh), glutamate, and γ-aminobutyric acid (GABA). Nicotinic ACh agonists strongly excited DS ganglion cell in a dose-dependent manner. Dose-response curves showed a wide range of potencies, with (±)-exo-2-(6-chloro-3pyridinyl)-7-azabicyclo[2.2.1] heptane dihydrochloride (epibatidine) ≫ nicotine > 1,1-dimethyl-4-phenylpiperazinium iodide = carbachol. In addition, the mixed cholinergic agonist carbachol produced a small excitation, mediated by muscarinic receptors, that could be blocked by atropine. The specific nicotinic antagonists hexamethonium bromide (100 μM), dihydro-β-erythroidine (50 μM), mecamylamine (50 μM), and tubocurarine (50 μM) blocked the responses to nicotinic agonists. In addition, nicotinic antagonists reduced the light-driven input to DS ganglion cells by ∼50%. However, attenuated responses were still DS. We deduce that cholinergic input is not required for directional selectivity. These experiments reveal the importance of bipolar cell input mediated by glutamate. N-methyl-d-aspartic acid (NMDA) excited DS ganglion cells, but NMDA antagonists did not abolish directional selectivity. However, a combined cholinergic and NMDA blockade reduced the responses of DS ganglion cells by >90%. This indicates that most of the noncholinergic excitatory input appears to be mediated by NMDA receptors, with a small residual made upb y  α - a m i n o - 3 - h y d r o x y - 5 - m e t h y l - 4 - i s o x a z o l e p r o p i o n i c  a c i d(AMPA)/kainate (KA) receptors. Responses to AMPA and KA were highly variable and often evoked a mixture of excitation and inhibition due to the release of ACh and GABA. Under cholinergic blockade AMPA/KA elicited a strong GABA-mediated inhibition in DS ganglion cells. AMPA/KA antagonists, such as 2,3-dihydroxy-6-nitro-7-sulfamoylbenzo(F)quinoxaline dione and GYKI-53655, promoted null responses and abolished directional selectivity due to the blockade of GABA release. We conclude that GABA release, mediated by non-NMDA glutamate receptors, is an essential part of the mechanism of directional selectivity. The source of the GABA is unknown, but may arise from starburst amacrine cells.

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

2005 ◽  
Vol 22 (4) ◽  
pp. 535-549 ◽  
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.

Spiking and nonspiking models of starburst amacrine cells in the rabbit retina

1997 ◽  
Vol 14 (6) ◽  
pp. 1073-1088 ◽  
Author(s):  
T. J. Velte ◽  
R. F. Miller
Keyword(s):  
Amacrine Cells ◽  
Membrane Resistance ◽  
Membrane Properties ◽  
Published Data ◽  
Rabbit Retina ◽  
Impulse Generation ◽  
Simulation Techniques ◽  
Anatomical Basis ◽  
Nonlinear Channels ◽  
Starburst Amacrine Cells

AbstractThe integrative properties of starburst amacrine cells in the rabbit retina were studied with compartmental models and computer-simulation techniques. The anatomical basis for these simulations was provided by computer reconstructions of intracellularly stained starburst amacrine cells and published data on dendritic diameter and biophysical properties. Passive and active membrane properties were included to simulate spiking and nonspiking behavior. Simulated synaptic inputs into one or more compartments consisted of a bipolar-like conductance change with peak and steady-state components provided by the sum of two Gaussian responses. Simulated impulse generation was achieved by using a model of impulse generation that included five nonlinear channels (INa, ICa, Ia,. Ik. Ik.Ca). The magnitude of the sodium channel conductance change was altered to meet several different types of impulse generation and propagation behaviors. We studied a range of model constraints which included variations in membrane resistance (Rm) from 4,000 Ω.cm2 to 100,000 Ω.cm2, and dendritic diameter from 0.1 to 0.3 μm. In a separate series of simulations, we studied the feasibility of voltage-clamping starburst amacrine cells using a soma-applied, single-electrode voltage clamp, based on models with and without dendritic and somatic spiking behavior. Our simulation studies suggest that single dendrites of starburst amacrine cells can behave as independent functional subunits when the Rm is high, provided that one or a small number of dendrites is synaptically co-activated. However, as the number of co-activated dendrites increases, the starburst cell behavior becomes more uniform and independent dendritic function is less prevalent. The presence of impulse activity in the dendrites raises new questions about dendritic function. However, dendritic impulses do not necessarily eliminate independent dendritic function, because dendritic impulses commonly fail as they propagate toward the soma, where they contribute EPSP-like responses which summate with conventional synaptic currents.

Displaced starburst amacrine cells of the rabbit retina contain the 67-kDa isoform, but not the 65-kDa isoform, of glutamate decarboxylase

1995 ◽  
Vol 12 (6) ◽  
pp. 1053-1061 ◽  
Author(s):  
Christopher Brandon ◽  
Mark H. Criswell
Keyword(s):  
Choline Acetyltransferase ◽  
Glutamate Decarboxylase ◽  
Lucifer Yellow ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
Biosynthetic Enzyme ◽  
Starburst Amacrine Cells

AbstractThe cholinergic identity of retinal starburst amacrine neurons is well established, but recent evidence suggests that these cells are GABAergic as well. Confirmation of this dual transmitter function requires the demonstration of glutamate decarboxylase (GAD), the biosynthetic enzyme for GABA, within starburst cells. The current work was undertaken to determine whether rabbit retinal starburst amacrine neurons contain either of the two known isoforms of GAD. To do this, we have examined the localization of the following: (1) the 65-kDa isoform of GAD; (2) the 67-kDa isoform of GAD; (3) choline acetyltransferase; and (4) the fluorescent dye DAPI, a marker for cholinergic amacrine cells. In addition, we labeled displaced starburst neurons directly, by injecting them with Lucifer Yellow in vitro. Four strata within the inner plexiform layer contained immunoreactive GAD65. A non-GAD65-immunoreactive zone separated the two innermost strata (G3 and G4); this zone contained (1) the dendrites of individual Lucifer Yellow-injected, displaced starburst amacrine cells; (2) dendrites immunoreactive for choline acetyltransferase; and (3) processes of DAPI-labeled amacrine cells. Immunoreactive GAD67 appeared in the same strata that contained GAD65, and in at least two additional strata, one of which lay at precisely the same depth as the proximal cholinergic stratum. In addition, the somas of displaced starburst cells were strongly immunoreactive for GAD67, but not for GAD65. These results demonstrate (1) that displaced starburst amacrine cells contain the 67-kDa isoform of GAD, but not the 65-kDa isoform; and (2) that the dendrites of starburst (67-kDa GAD) amacrines, and the dendrites of 65-kDa-GAD-containing amacrines, occupy different strata within the inner plexiform layer. Thus, displaced starburst cells do contain GAD, and can, presumably, manufacture GABA. The reasons for their preferential use of the 67-kDa GAD isoform remain to be elucidated.

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