A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells

2002 ◽  
Vol 19 (2) ◽  
pp. 145-162 ◽  
Author(s):  
E.V. FAMIGLIETTI
Keyword(s):  
Ganglion Cells ◽  
Dendritic Tree ◽  
Amacrine Cells ◽  
Dendritic Morphology ◽  
Bipolar Cells ◽  
Structural Basis ◽  
Rabbit Retina ◽  
Low Velocity ◽  
Accessory Optic System ◽  
Starburst Amacrine Cells

Directionally selective (DS) ganglion cells of rabbit retina are of two principal types. ON DS ganglion cells prefer low velocity in one of three directions of movement and project axons to the accessory optic system (AOS), whereas ON–OFF DS ganglion cells prefer higher velocity in one of four directions and project to tectum and thalamus. Each has a distinct, recognizable dendritic morphology, based upon the correlation of form, physiology, and central projections. In previous Golgi studies, ON and ON–OFF DS cells were found to be partly co-stratified, and ON–OFF DS cells were found to co-stratify with starburst amacrine (SA) cells, the cholinergic amacrine cells of the retina, which also contain elevated levels of GABA. SA cells are radially symmetrical, have synaptic boutons in a distal annular zone of its dendritic tree, are presynaptic primarily to ganglion cell dendrites, co-stratify with ON–OFF DS ganglion cells, and contain the neurotransmitters shown pharmacologically to be involved in DS responses. For these reasons, SA cells are thought to play a role in the DS mechanism. Several models of this mechanism have utilized SA cell dendritic geometry in a centrifugal, radial format to impose directional inputs on DS ganglion cells.

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 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.

The DAPI-3 amacrine cells of the rabbit retina

1997 ◽  
Vol 14 (3) ◽  
pp. 473-492 ◽  
Author(s):  
Layne L. Wright ◽  
Colin L. Macqueen ◽  
Guy N. Elston ◽  
Heather M. Young ◽  
David V. Pow ◽  
...  
Keyword(s):  
Ganglion Cells ◽  
Dendritic Tree ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Dendritic Morphology ◽  
Peripheral Retina ◽  
Inner Plexiform Layer ◽  
Rabbit Retina ◽  
High Level ◽  
Cholinergic Amacrine Cells

AbstractIn the rabbit retina, the nuclear dye, 4,6, diarnidino-2-phenylindole (DAPI), selectively labels a third type of amacrine cell, in addition to the previously characterized type a and type b cholinergic amacrine cells. In this study, these “DAPI-3” amacrine cells have been characterized with respect to their somatic distribution, dendritic morphology, and neurotransmitter content by combining intracellular injection of biotinylated tracers with wholemount immunocytochemistry. There are about 100,000 DAPI-3 amacrine cells in total, accounting for 2% of all amacrine cells in the rabbit retina, and their cell density ranges from about 130 cells/mm2 in far-peripheral retina to 770 cells/mm2 in the visual streak. The thin varicose dendrites of the DAPI-3 amacrine cells form a convoluted dendritic tree that is symmetrically bistratified in S1/S2 and S4 of the inner plexiform layer. Tracer coupling shows that the DAPI-3 amacrine cells have a fivefold dendritic-field overlap in each sublamina, with the gaps in the arborization of each cell being occupied by dendrites from neighboring cells. The DAPI-3 amacrine cells consistently show the strongest glycine immunoreactivity in the rabbit retina and they also accumulate exogenous [3H]-glycine to a high level. By contrast, the All amacrine cells, which are the best characterized glycinergic cells in the retina, are amongst the most weakly labelled of the glycine-immunopositive amacrine cells. The DAPI-3 amacrine cells costratify narrowly with the cholinergic amacrine cells and the On-Off direction-selective ganglion cells, suggesting that they may play an important role in movement detection.

The morphology of the bipolar cells, amacrine cells and ganglion cells in the retina of the turtle Pseudemys Scripta Elegans

1982 ◽  
Vol 298 (1092) ◽  
pp. 355-393 ◽  
Keyword(s):  
Ganglion Cells ◽  
Dendritic Tree ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Dendritic Morphology ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Visual Streak ◽  
Pseudemys Scripta ◽  
Oriented Parallel

The morphology of the neurons that contribute to the inner plexiform layer of the retina of the turtle Pseudemys scripta elegans has been studied by light microscopy of whole-mount material stained by the method of Golgi. Cells have been distinguished on the basis of criteria that include dendritic branching patterns, dendritic morphology, dendritic tree sizes and stratification of processes in the inner plexiform layer. Many of the neurons have dendritic trees oriented parallel to and a few exhibit an orthogonal orientation with the linear visual streak present in the retina of this species. The neurons of the turtle retina have been compared, where possible, with the neurons of the lizard retina as described by Cajal. The findings are discussed in relation to other vertebrate retinas, and correlations are made with recent electrophysiological recordings of the turtle retina. Comments are made with regard to the significance of orientation of neurons relative to the linear visual streak.

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.

Melanopsin and calbindin immunoreactivity in the inner retina of humans and marmosets

2019 ◽  
Vol 36 ◽  
Author(s):  
Ashleigh J. Chandra ◽  
Sammy C.S. Lee ◽  
Ulrike Grünert
Keyword(s):  
Ganglion Cell ◽  
Calcium Binding ◽  
Ganglion Cell Layer ◽  
Ganglion Cells ◽  
Cell Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Human Retina ◽  
Immunohistochemical Markers ◽  
Starburst Amacrine Cells

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.

Morphological and functional identifications of catfish retinal neurons. I. Classical morphology

1975 ◽  
Vol 38 (1) ◽  
pp. 53-71 ◽  
Author(s):  
K. Naka ◽  
N. R. Garraway
Keyword(s):  
Ganglion Cells ◽  
Horizontal Cell ◽  
Dendritic Tree ◽  
Amacrine Cells ◽  
Cell Types ◽  
Bipolar Cells ◽  
Inner Nuclear Layer ◽  
Horizontal Cells ◽  
Specific Cell ◽  
Definition Of

The morphology of the catfish horizontal cells is comparable to that in other fish retinas. The external horizontal cells contact cone receptors and are stellate in shape; the intermediate horizontal cells are even more so and contact rod receptors. The internal horizontal cells constitute the most proximal layer of the inner nuclear layer and may possibly be, in reality, extended processes from the other two horizontal cell types. Bipolar cells resemble those in other teleost retinas: the size and shape of their dendritic tree encompass a continuous spectrum ranging from what is known as the small to the large bipolar cells. The accepted definition of amacrine cells is sufficiently vague to justify our originating a more descriptive and less inferential name for the (axonless) neurons in the inner nuclear layer which radiate processes throughout the inner synaptic layer. These starbust and spaghetti cells vary considerably in the character and extent of their dendritic spread, but correlates exist in other vertebrate retinas. Ganglion cells are found not only in the classical ganglion layer but displaced into the inner nuclear layer as well. Several types can be distinguished on the basis of cell geometry and by the properties of their dendritic tree. Not all of the categorization corresponds with previous descriptions; our findings suggest that some reorganization may be necessary in the accepted classification of cells in the proximal areas of the vertebrate retina. A subtle yet remarkable pattern underlies the entire structure of the catfish retina; there exists a definite gradient of size within a particular class of cells, and of configuration among the subclasses of a specific cell type. It remains to be seen if these morphological spectra bear any functional consequences. The fact that the structure of the catfish retina most closely resembles those of other phylogenetically ancient animals, such as the skate and the dogfish shark, testifies to its primitive organization; morphological and functional mechanisms discernible in this simple system may, therefore, be applicable to the retinas of higher ordered vertebrates.

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

2019 ◽  
Vol 36 ◽  
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.

scholarly journals Receptive field properties of bipolar cell axon terminals in direction-selective sublaminas of the mouse retina

2014 ◽  
Vol 112 (8) ◽  
pp. 1950-1962 ◽  
Author(s):  
Minggang Chen ◽  
Seunghoon Lee ◽  
Silvia J. H. Park ◽  
Loren L. Looger ◽  
Z. Jimmy Zhou
Keyword(s):  
Receptive Field ◽  
Ganglion Cells ◽  
Amacrine Cells ◽  
Direction Selectivity ◽  
Bipolar Cells ◽  
Visual Signals ◽  
Mouse Retina ◽  
Patch Clamp Recording ◽  
Axon Terminals ◽  
Starburst Amacrine Cells

Retinal bipolar cells (BCs) transmit visual signals in parallel channels from the outer to the inner retina, where they provide glutamatergic inputs to specific networks of amacrine and ganglion cells. Intricate network computation at BC axon terminals has been proposed as a mechanism for complex network computation, such as direction selectivity, but direct knowledge of the receptive field property and the synaptic connectivity of the axon terminals of various BC types is required in order to understand the role of axonal computation by BCs. The present study tested the essential assumptions of the presynaptic model of direction selectivity at axon terminals of three functionally distinct BC types that ramify in the direction-selective strata of the mouse retina. Results from two-photon Ca2+ imaging, optogenetic stimulation, and dual patch-clamp recording demonstrated that 1) CB5 cells do not receive fast GABAergic synaptic feedback from starburst amacrine cells (SACs); 2) light-evoked and spontaneous Ca2+ responses are well coordinated among various local regions of CB5 axon terminals; 3) CB5 axon terminals are not directionally selective; 4) CB5 cells consist of two novel functional subtypes with distinct receptive field structures; 5) CB7 cells provide direct excitatory synaptic inputs to, but receive no direct GABAergic synaptic feedback from, SACs; and 6) CB7 axon terminals are not directionally selective, either. These findings help to simplify models of direction selectivity by ruling out complex computation at BC terminals. They also show that CB5 comprises two functional subclasses of BCs.

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