Bipolar Cell Inputs Research Articles

Neurocircuitry of two types of neurotensin-containing amacrine cells in the turtle retina

The ultrastructural features and synaptic contacts of two types of neurotensin-containing amacrine cell in turtle retina were examined by electron immunocytochemistry, and the retinal peptides were characterized using radioimmunoassay and high-pressure liquid chromatography. The two types of cell were distinguished on the basis of their sizes, dendritic arborizations, synaptic connections and cytoplasmic staining characteristics. Type A cells had lightly labeled cytoplasm and large vertically elongated cell bodies which gave rise to a single primary process which in turn branched and ramified as smooth tapering processes in stratum 3 of the inner plexiform layer. Type A cells received approximately equal synaptic input from amacrine and bipolar cells. Type A amacrines had much more overall synaptic input than synaptic output, and they made conventional synaptic contacts onto bipolar, amacrine, and ganglion cells. Type B cells had a much darker-staining cytoplasm and a smaller cell body which gave rise to numerous delicate beaded dendrites which arborized in strata 3, 4 and 5 of the inner plexiform layer. Type B cells received primarily amacrine and some bipolar cell input. Type B cells had equal amounts of synaptic input and output and they made conventional synaptic contacts onto amacrine, bipolar, and ganglion cells. Whereas there were numerous large vesicles (120nm diameter) that stained for neurotensin in both types of cells, conventional synaptic vesicles (60 nm diameter) were not labeled. In several cases these large labeled vesicles appeared to fuse with the cell membrane in non-synaptic regions and release their contents into extracellular space, which suggested a non-synaptic release of the neurotensin from type A neurons. Immunochemical and Chromatographie studies demonstrated that the neurotensin-related material in retina was indistinguishable from neurotensin found in brain. These results are consistent with a neuroactive role for the neurotensin present within the large vesicles. The differences in the synaptic contacts and dendritic arborizations of the two amacrine cell types suggest they play distinctive functions in visual processing.

Electron microscopic analysis of amacrine and bipolar cell inputs on Y-, X- and W-cells in the cat retina

In the cat retina, bipolar and amacrine cell inputs were analyzed electron microscopically in 5 ganglion cells (two Y-cells, two X-cells and one W-cell) that were well-isolated and had clear morphological features 9,26,28. For Y- and X-cells, subtypes of a and b were further identified according to the sublamina of the inner plexiform layer in which their dendrites extended 22,26. Y-a and Y-b ganglion cells had large somas, thick axons, and several thick dendrites that branched extensively with a large dendritic field. X-a and X-b cells had medium-sized somas, medium-sized axons and extremely narrow dendritic fields. The W-cell studied had a medium-sized soma, a medium-sized axon, and extremely thin dendrites that extended widely. For each of the 5 ganglion cells, ultrathin serial sections were made to study relative occurrence of amacrine and bipolar synapses in whole length of dendrites. About 50% of the terminals were bipolar in the Y-a and Y-b cell dendrites, 36–38% in the X-a and X-b cell dendrites, whereas only 19.7% were bipolar in the W cell dendrites. Bipolar terminals tended to make synaptic contacts with the distal dendrites of Y- and W-cells.

(3H) glycine-accumulating neurons of the human retina.

Isolated human retinas were incubated in physiological saline containing micromolar (3H) glycine. The types, distributions, and synaptologies of glycine-accumulating neurons were determined by light and electron microscope autoradiography. Two types of amacrine cells were discriminated on the bases of number of processes descending into the inner plexiform layer, density of label in light-microscope autoradiographs, size, and synaptic features: (1) Gly1 amacrine cells have moderate labeling, several oblique dendrites arising from the soma, and electron lucent synaptic terminals containing large presynaptic specializations, nd (2) Gly2 amacrine cells have dense labeling, a single proximal dendrite, and moderately electron-dense terminals with small presynaptic specializations. Gly1 amacrine cells constitute approximately 15% and Gly2 amacrine cells approximately 38% of all cells in the amacrine cell layer. The laminar distribution of label in the inner plexiform layer was measured by scanning microdensitometry, which provided a format for categorizing types of synaptic contacts. Many features of glycine-accumulating amacrine cell contacts were similar to those of cat AII/Gly2 amacrine cells: a diffuse yet bisublaminar distribution of label, concentration of synaptic output in sublamina a, rod bipolar cell input in sublamina b and gap junctions in mid-inner plexiform layer involving labeled cells. The evidence seems to indicate that human Gly2 amacrine cells and cat AII/Gly2 amacrine cells are homologous cell types. finally, some cone bipolar cells were labeled.

Microcircuitry of bipolar cells in cat retina

We have studied 15 bipolar neurons from a small patch (14 X 120 micron) of adult cat retina located within the area centralis. From electron micrographs of 189 serial ultrathin sections, the axon of each bipolar cell was substantially reconstructed with its synaptic inputs and outputs by means of a computer-controlled reconstruction system. Based on differences in stratification, cytology, and synaptic connections, we identified eight different cell types among the group of 15 neurons: one type of rod bipolar and seven types of cone bipolar neurons. These types correspond to those identified by the Golgi method and by intracellular recording. Those bipolar cell types for which we reconstructed three or four examples were extremely regular in form, size, and cytology, and also in the quantitative details of their synaptic connections. They appeared quite as specific in these respects as invertebrate "identified" neurons. The synaptic patterns observed for each type of bipolar neuron were complex but may be summarized as follows: the rod bipolar axon ended in sublamina b of the inner plexiform layer and provided major input to the AII amacrine cell. The axons of three types of cone bipolar cells also terminated in sublamina b and provided contacts to dendrites of on-beta and other ganglion cells. All three types, but especially the Cb1, received gap junction contacts from the AII amacrine cell. Axons of four types of cone bipolar cells terminated in sublamina a of the inner plexiform layer and contacted dendrites of off-beta and other ganglion cells. One of these cone bipolar cell types, CBa1, made reciprocal chemical contacts with the lobular appendage of the AII amacrine cell. These results show that the pattern of cone bipolar cell input to beta (X) and probably alpha (Y) ganglion cells is substantially more complex than had been suspected. At least two types of cone bipolar contribute to each type of ganglion cell where only a single type had been anticipated. In addition, many of the cone bipolar cell pathways in the inner plexiform layer are available to the rod system, since at least four types of cone bipolar receive electrical or chemical inputs from the AII amacrine cell. This may help to explain why, in a retina where rods far outnumber the cones, there should be so many types of cone bipolar cells.

A tonic gamma-aminobutyric acid-mediated inhibition of cholinergic amacrine cells in rabbit retina

Using the in vivo rabbit eyecup, we have studied the light-evoked release of acetylcholine (ACh) which is presumed to indicate the activity of cholinergic amacrine cells. Gamma-Aminobutyric acid (GABA) inhibited the light-evoked release of ACh (IC50 congruent to 1 mM), but the GABA antagonists bicuculline (5 micro M) and picrotoxin (20 micro M) potentiated the light-evoked release and markedly increased the resting release of ACh. This bicuculline/picrotoxin-evoked release was calcium dependent and the effects of bicuculline, but not picrotoxin, were blocked by muscimol, a potent GABA agonist. Muscimol also inhibited the light-evoked release of ACh (IC50 less than 1 micro M) and was at least 1000 times more potent than GABA. Nipecotic acid (1 mM), a GABA transport blocker, also inhibited the light-evoked release of ACh, but the effect was slow in onset and recovery was prompt. We conclude that the cholinergic amacrine cells of rabbit retina are inhibited by GABA. The relatively weak action of GABA, compared to muscimol, may be due to the presence of avid GABA transport systems. We ascribe the excitatory effects of bicuculline and picrotoxin to the antagonism of endogenous GABA, suggesting that the cholinergic cells are influenced by a tonic release of GABA. This is consistent with the effects of nipecotic acid. Although we are unable to specify the synaptic arrangements involved, we suggest that the most likely interaction is directly between GABA amacrine cells and the cholinergic amacrine cells and/or their presumed bipolar cell inputs.

A model for the temporal organization of X- and Y-type receptive fields in the primate retina

A model is proposed for the temporal characteristics of X- and Y-type responses of ganglion cells in the primate retina. The main suggestions of the model are: (I) The X-type temporal response is determined primarily by the delay between center and surround contributions. (II) The Y-type response is generated in the inner plexiform layer by a derivative-like operation on the bipolar cell's input, followed by a rectification in the convergence of these inputs onto the Y-ganglion-cell. (III) The derivative-like operation is obtained by recurrent inhibition in the dyad synaptic structure. The X- and Y-type responses predicted by the model, for a variety of stimuli, were examined and compared with available electrophysiological recordings. Finally, certain predictions derived from the model are discussed.

Interactions leading to colour opponency in ganglion cells of the turtle retina.

In the turtle retina, colour-dependent photoresponses could be recorded intracellularly from ganglion cells receiving only bipolar cell input. Thus, the mechanism for colour discrimination by these ganglion cells (type A) is contained in the outer plexiform layer of the retina and depends on interaction between horizontal and cone cells. Ganglion cells receiving an additional amacrine input (type B) are not influenced by colour, and have about 0.7 logarithmic unit lower absolute sensitivity to peak wavelength than have type A ganglion cells.

Intracellular analysis and structural correlates of the organization of inputs to ganglion cells in the retina of the turtle.

Intracellular recording from the ganglion cells of the retina of the turtle Pseudemys scripta elegans shows that the photoresponses are characterized by either of two reversal potentials. These have been related to the bipolar and amacrine cell inputs to ganglion cells. Of the recorded ganglion cells, 33% (type A) are driven predominantly by one type of input, attributed to bipolar cells. Other ganglion cells (66%, type B) receive a mixed input from bipolar and amacrine cells. Type A ganglion cells show a higher conduction velocity (up to 3 m/s) and a higher firing frequency (up to 160 spikes per second) than type B cells. By injecting Procion yellow into bipolar, amacrine and ganglion cells it may be observed that type A ganglion cells ramify only in those regions of the inner plexiform layer that contain cell processes originating exclusively from the bipolar cell type predicted from the recordings. Type B ganglion cells ramify throughout the inner plexiform layer in either a multi-stratified or a diffuse fashion.

Lateral contacts and interactions of horizontal cell dendrites in the retina of the larval tiger salamander

1. The contacts of horizontal cell dendrites with processes of other second order neurones were studied at the level of the electron microscope in serial sections of the salamander retina. Intracellular recordings of the responses to light of horizontal and bipolar cells were used to investigate the possible significance of some of the morphological findings.2. Horizontal cell dendrites make close membrane appositions (gap junctions) with one another and are post-synaptic to bipolar cell dendrites at presumed chemical synapses. On the other hand, there is no clear evidence that horizontal cell dendrites are presynaptic to any other neuronal processes at the outer plexiform layer, so that the output connexions of horizontal cell bodies remain a matter of speculation.3. It is suggested that the bipolar cell input and the gap junctions between dendrites contribute, respectively, depolarizing and hyperpolarizing components to the responses of horizontal cell bodies to surround illumination. In addition, the facilitatory effect of central illumination on the surround response of horizontal cell bodies may result, although perhaps only partly, from observed properties of the surround response of bipolar cells.4. In the course of these observations, bipolar cells were found to be presynaptic at the outer plexiform layer not only to horizontal cell dendrites, but also to other bipolar cells, horizontal cell axon terminals and certain processes belonging to an as yet unidentified neurone.

Pathways and polarities of synaptic interactions in the inner retina of the mudpuppy: I. Synaptic blocking studies

Intracellular recording techniques were applied to the perfused retina-eyecup of the mudpuppy ( Necturus maculosus). The use of input resistance measurements and the application of cobalt as a synaptic blocking agent provided evidence about the mode of synaptic operation for depolarizing and hyperpolarizing bipolar cell input to cells of the inner retina. In addition, cobalt produced a more rapid block of hyperpolarizing bipolars compared to depolarizing bipolars; in some postbipolar neurons, a temporary simplification of neuronal response waveform was observed, and such cells resembled the depolarizing bipolar. These experiments suggest that bipolar cell input is excitatory and that response characteristics of third-order neurons is partially dependent on the relative input from the two types of bipolar cells.