Comparison of the responses of AII amacrine cells in the dark- and light-adapted rabbit retina

1999 ◽  
Vol 16 (4) ◽  
pp. 653-665 ◽  
Author(s):  
DAIYAN XIN ◽  
STEWART A. BLOOMFIELD

We studied the light-evoked responses of AII amacrine cells in the rabbit retina under dark- and light-adapted conditions. In contrast to the results of previous studies, we found that AII cells display robust responses to light over a 6–7 log unit intensity range, well beyond the operating range of rod photoreceptors. Under dark adaptation, AII cells showed an ON-center/OFF-surround receptive-field organization. The intensity–response profile of the center-mediated response component followed a dual-limbed sigmoidal function indicating a transition from rod to cone mediation as stimulus intensities were increased. Following light adaptation, the receptive-field organization of AII cells changed dramatically. Light-adapted AII cells showed both ON- and OFF-responses to stimulation of the center receptive field, but we found no evidence for an antagonistic surround. Interestingly, the OFF-center response appeared first following rapid light adaptation and was then replaced gradually over a 1–4 min period by the emerging ON-center response component. Application of the metabotropic glutamate receptor agonist APB, the ionotropic glutamate blocker CNQX, 8-bromo-cGMP, and the nitric oxide donor SNAP all showed differential effects on the various center-mediated responses displayed by dark- and light-adapted AII cells. Taken together, these pharmacological results indicated that different synaptic circuits are responsible for the generation of the different AII cell responses. Specifically, the rod-driven ON-center responses are apparently derived from rod bipolar cell synaptic inputs, whereas the cone-driven ON-center responses arise from signals crossing the gap junctions between AII cells and ON-center cone bipolar cells. Additionally, the OFF-center response of light-adapted AII cells reflects direct synaptic inputs from OFF-center cone bipolar cells to AII dendritic processes in the distal inner plexiform layer.

2011 ◽  
Vol 28 (3) ◽  
pp. 183-192 ◽  
Author(s):  
DWIGHT A. BURKHARDT ◽  
THEODORE M. BARTOLETTI ◽  
WALLACE B. THORESON

AbstractReceptive field organization of cone-driven bipolar cells was investigated by intracellular recording in the intact light-adapted retina of the tiger salamander (Ambystoma tigrinum). Centered spots and concentric annuli of optimum dimensions were used to selectively stimulate the receptive field center and surround with sinusoidal modulations of contrast at 3 Hz. At low contrasts, responses of both the center and surround of both ON and OFF bipolar cells were linear, showing high gain and thus contrast enhancement relative to cones. The contrast/response curves for the fundamental response, measured by a Fast Fourier Transform, reached half maximum amplitude quickly at 13% contrast followed by saturation at high contrasts. The variation of the normalized amplitude of the center and surround responses was remarkably similar, showing linear regression over the entire response range with very high correlations, r2 = 0.97 for both ON and OFF cells. The contrast/response curves of both center and surround for both ON and OFF cells were well fit (r2 = 0.98) by an equation for single-site binding. In about half the cells studied, the nonlinear waveforms of center and surround could be brought into coincidence by scaling and shifting the surround response in time. This implies that a nonlinearity, common to both center and surround, occurs after polarity inversion at the cone feedback synapse. Evidence from paired whole-cell recordings between single cones and OFF bipolar cells suggests that substantial nonlinearity is not due to transmission at the cone synapse but instead arises from intrinsic bipolar cell and network mechanisms. When sinusoidal contrast modulations were applied to the center and surround simultaneously, clear additivity was observed for small responses in both ON and OFF cells, whereas the interaction was strikingly nonadditive for large responses. The contribution of the surround was then greatly reduced, suggesting attenuation at the cone feedback synapse.


2004 ◽  
Vol 21 (5) ◽  
pp. 791-805 ◽  
Author(s):  
XIAO-BO XIA ◽  
STEPHEN L. MILLS

Gap junctions are commonplace in retina, often between cells of the same morphological type, but sometimes linking different cell types. The strength of coupling between cells derives from the properties of the connexins, but also is regulated by the intracellular environment of each cell. We measured the relative coupling of two different gap junctions made by AII amacrine cells of the rabbit retina. Permeability to the tracer Neurobiotin was measured at different concentrations of the neuromodulators dopamine, nitric oxide, or cyclic adenosine monophosphate (cAMP) analogs. Diffusion coefficients were calculated separately for the gap junctions between pairs of AII amacrine cells and for those connecting AII amacrine cells with ON cone bipolar cells. Increased dopamine caused diffusion rates to decline more rapidly across the AII–AII gap junctions than across the AII–bipolar cell gap junctions. The rate of decline at these sites was well fit by a model proposing that dopamine modulates two independent gates in AII–AII channels, but only a single gate on the AII side of the AII–bipolar channel. However, a membrane-permeant cAMP agonist modulated both types of channel equally. Therefore, the major regulator of channel closure in this network is the local cAMP concentration within each cell, as regulated by dopamine, rather than different cAMP sensitivity of their respective gates. In contrast, nitric oxide preferentially reduced AII–bipolar cell permeabilities. Coupling from AII amacrine cells to the different bipolar cell subtypes was differentially affected by dopamine, indicating that light adaptation actingviadopamine release alters network coupling properties in multiple ways.


1976 ◽  
Vol 67 (6) ◽  
pp. 679-690 ◽  
Author(s):  
R F Miller ◽  
R F Dacheux

A chloride-free environment produces selective changes in the retinal network which include a separation of on and off channels. The identification of chloride-sensitive and insensitivie neuronal activity permits identification of some of the connections and intervening polarities of synaptic interactions which are expressed in ganglion cell receptive field organization. These experiments support previous suggestions that surround antagonism is dependent on horizontal cell activity. In addition they suggest a model of the neuronal connections which subserve on-center, off-center, and on-off ganglion cells. Experimental tests of the on-off ganglion cell model favor the idea that this type of ganglion cell receives inhibitory input from amacrine cells and excitatory activation from depolarizing and hyperpolarizing bipolar cells.


2019 ◽  
Vol 36 ◽  
Author(s):  
Andrea S. Bordt ◽  
Diego Perez ◽  
Luke Tseng ◽  
Weiley Sunny Liu ◽  
Jay Neitz ◽  
...  

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.


1976 ◽  
Vol 67 (6) ◽  
pp. 661-678 ◽  
Author(s):  
R F Miller ◽  
R F Dacheux

Extracellular ganglion cell recordings in the perfused mudpuppy eyecup show that a chloride-free (c-f) perfusate abolishes the center and surround excitation of on-center cells, the surround excitation of off-center cells, and the on discharge of on-off cells. These changes in ganglion cell receptive field organization are anticipated in view of the effects of a c-f environment on the neurons which are presynaptic to the ganglion cells. However, chloride-dependent inhibitory postsynaptic (IPS) responses have been observed in on-off ganglion cells. These inhibitory postsynaptic potentials (IPSP's) are preceeded by (ESPS's) exitatory postsynaptic potentials and are apparently mediated by amacrine cells. The light-activated hyperpolarization of off cells is not the result of a chloride-dependent IPSP and probably results from disfacilitation.


1997 ◽  
Vol 14 (2) ◽  
pp. 395-401 ◽  
Author(s):  
Jay F. Muller ◽  
Ramon F. Dacheux

AbstractAlpha ganglion cells from the midperiphery of the rabbit retina were recorded intracellularly under visual control, in a superfused everted eyecup, and labeled with HRP. Their physiology and large somata with broad dendritic arbors identified them as uniform populations of ON- and OFF-center alpha ganglion cells, which typically displayed transient/sustained light-evoked responses. When dark adapted, the light-evoked responses from both ON- and OFF-center alpha ganglion cells were more sustained than those generally seen under light-adapted conditions. During dark-adapted (scotopic) conditions, stimulation with dim full-field illumination and small spots, either positioned over the soma or displaced 450 μm from the soma, all elicited pure center responses. After light adaptation (photopic conditions), the displaced small spots that previously evoked center responses elicited antagonistic surround responses from both ON- and OFF-center cells. Thus, as originally described in cat retina (Barlow et al., 1957), the receptive-field organization of ganglion cells changed between dark and light adaptation, and an absence or presence of surround antagonism was indicative of scotopic versus photopic states.


1982 ◽  
Vol 47 (5) ◽  
pp. 928-947 ◽  
Author(s):  
R. Nelson

1. In a perfused eyecup preparation, AII amacrine cells of the cat retina were penetrated with glass microelectrodes and their electrical responses to photic stimuli recorded. 2. Intracellular injections of the stains Procion, lucifer, or horseradish peroxidase revealed dendritic tree diameters of 30-80 micrometers (48 +/- 16 micrometers, mean +/0 SD) and cell body diameters from 7 to 12 micrometers (9 +/- 3 micrometers) for these cells. The dendrites were broadly stratified throughout the inner plexiform layer (IPL) but possessed large, terminal varicosities in the IPL and inner nuclear lyer (INL) proximal to the cell body. 3. The waveform of these cells in response to photic stimulation suggested division into four components: a) an initial rapid depolarization of the cell membrane followed by a slower decay toward the dark level; b) suppression of the dark noise of the cell; c) with dim or moderately intense stimuli, an off-hyperpolarization; d) in some cases a hyperpolarizing surround response. 4. The receptive fields of AII cells have been characterized using spatial stimuli consisting of long narrow slits. Curves have been fitted to spatial data using two space constants, one for the center mechanism and an opposing one for the surround. For the central mechanism, space constants ranged from 20 to 80 micrometers (46 +/- 22 micrometers), while for the surround they ranged from 60 to 130 micrometers (85 +/- 28 micrometers). The mean half-width of the center mechanism, calculated from the mean space constant, was about 0.25 degrees of visual angle (64 micrometers). The receptive-field properties of AII amacrine cells resemble those of center-depolarizing bipolar cells of other species. 5. Spectral studies of AII amacrine cells reveal that they are rod driven at all criterion voltage levels. Furthermore, adaptation of the rods by rod-saturating backgrounds eliminates 95% of the response amplitude of the AII amacrine cells. Under these conditions the tiny response component remaining is driven by the cat's long wavelength (556-nm peak) cones. 6. AII amacrine cells depolarize to rod stimulation more rapidly than other rod-dominated cells, such as rod bipolar cells, which hyperpolarize. For stimuli corresponding to about 10% of rod saturation, the latency to half-maximum amplitude is about 65 ms for AII cells, 40 ms faster than rod-dominated hyperpolarizing units. The leading edge of the response waveform for AII cells is also much more restricted in time. With the above stimulus it requires about 20 ms to increase from 25 to 75% of its peak, a period almost 4 times shorter than required by rod-dominated S-potential responses. With saturating stimuli the AII response requires only 5 ms to increase from 25 ot 75% of its peak. 7. Although prominent in the rod system, AII amacrine cells do not appear to be able to detect single quantum events. Threshold signals require the bleaching of about 200 rhodopsin molecules within a receptive field containing some 1,300 rods...


1976 ◽  
Vol 67 (6) ◽  
pp. 639-659 ◽  
Author(s):  
R F Miller ◽  
R F Dacheux

Intracellular recordings from receptors, horizontal cells, bipolars, and amacrines have been carried out in the perfused mudpuppy eyecup. The introduction of a chloride-free (c-f) medium results in initial transient potential changes in many cells followed by a slow loss of light-evoked activity of the depolarizing bipolar, the horizontal cell, and the on depolarization of amacrine cells. The hyperpolarizing bipolar remains responsive to light stimulation in a c-f medium, but the antagonistic surround mechanism is abolished. These effects are reversible after returning to a normal ionic medium. The results of this study provide insight into the retinal connections which underlie ganglion cell receptive field organization. It is concluded that the depolarizing bipolar is excitatory to on ganglion cells and is also the pathway for on-excitation of on-off cells. The hyperpolarizing bipolar mediates the off discharge of off and on-off cells. Amacrine cells receive input from both depolarizing and hyperpolarizing bipolar cells. These findings raise the possibility that transmembrane movements of chloride ions are critical for the light responsiveness of horizontal and depolarizing bipolar cell activity.


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