scholarly journals A model of high-frequency oscillatory potentials in retinal ganglion cells

2003 ◽  
Vol 20 (5) ◽  
pp. 465-480 ◽  
Author(s):  
GARRETT T. KENYON ◽  
BARTLETT MOORE ◽  
JANELLE JEFFS ◽  
KATE S. DENNING ◽  
GREG J. STEPHENS ◽  
...  

High-frequency oscillatory potentials (HFOPs) have been recorded from ganglion cells in cat, rabbit, frog, and mudpuppy retina and in electroretinograms (ERGs) from humans and other primates. However, the origin of HFOPs is unknown. Based on patterns of tracer coupling, we hypothesized that HFOPs could be generated, in part, by negative feedback from axon-bearing amacrine cells excited via electrical synapses with neighboring ganglion cells. Computer simulations were used to determine whether such axon-mediated feedback was consistent with the experimentally observed properties of HFOPs. (1) Periodic signals are typically absent from ganglion cell PSTHs, in part because the phases of retinal HFOPs vary randomly over time and are only weakly stimulus locked. In the retinal model, this phase variability resulted from the nonlinear properties of axon-mediated feedback in combination with synaptic noise. (2) HFOPs increase as a function of stimulus size up to several times the receptive-field center diameter. In the model, axon-mediated feedback pooled signals over a large retinal area, producing HFOPs that were similarly size dependent. (3) HFOPs are stimulus specific. In the model, gap junctions between neighboring neurons caused contiguous regions to become phase locked, but did not synchronize separate regions. Model-generated HFOPs were consistent with the receptive-field center dynamics and spatial organization of cat alpha cells. HFOPs did not depend qualitatively on the exact value of any model parameter or on the numerical precision of the integration method. We conclude that HFOPs could be mediated, in part, by circuitry consistent with known retinal anatomy.

1996 ◽  
Vol 13 (2) ◽  
pp. 303-309 ◽  
Author(s):  
Franklin R. Amthor ◽  
Norberto M. Grzywacz ◽  
David K. Merwine

AbstractThe excitatory receptive-field centers of On-Off directionally selective (DS) ganglioncells of the rabbit retina correspond closely to the lateral extent of their dendritic arborizations. Some investigators have hypothesized from this that theories for directionalselectivity that entail a lateral spread of excitation from outside the ganglion cell dendritic tree, such as from starburst amacrine cells, are therefore untenable. We show herethat significant motion facilitation is conducted from well outside the classical excitatory receptive-field center (and, therefore, dendritic arborization) of On-Off DS ganglioncells for preferred-direction, but not null-direction moving stimuli. These results are consistent with a role in directional selectivity for cells with processes lying beyond the On-Off ganglion cell's excitatory receptive-field center. These results also highlight the fundamental distinction in retinal ganglion cell receptive-field organization between classical excitatory mechanisms and those that facilitate other excitation without producing directly observable excitation by themselves.


1992 ◽  
Vol 67 (2) ◽  
pp. 430-442 ◽  
Author(s):  
H. M. Sakai ◽  
K. Naka

1. We have applied Wiener analysis to a study of response dynamics of N (sustained) and C (transient) amacrine cells. Stimuli were a spot and an annulus of light, the luminance of which was modulated by two independent white-noise signals. First- and second-order Wiener kernels were computed for each spot and annulus input. The analysis allowed us to separate a modulation response into its linear and nonlinear components, and into responses generated by a receptive-field center and its surround. 2. Organization of the receptive field of N amacrine cells consists of both linear and nonlinear components. The receptive field of linear components was center-surround concentric and opposite in polarity, whereas that of second-order nonlinear components was monotonic. 3. In NA (center-depolarizing) amacrine cells, the membrane DC potentials brought about by the mean luminance of a white-noise spot or a steady spot were depolarizations, whereas those brought about by the mean luminance of a white-noise annulus or a steady annulus were hyperpolarizations. In NB (center-hyperpolarizing) amacrine cells, this relationship was reversed. If both receptive-field center and surround were stimulated by a spot and annulus, membrane DC potentials became close to the dark level and the amplitude of modulation responses became larger. 4. The linear responses of a receptive-field center of an N amacrine cell, measured in terms of the first-order Wiener kernel, were facilitated if the surround was stimulated simultaneously. The amplitude of the kernel became larger, and its peak response time became shorter. The same facilitation occurred in the linear responses of a receptive-field surround if the center was stimulated simultaneously. 5. The second-order nonlinear responses were not usually generated in N amacrine cells if the stimulus was either a white-noise spot or a white-noise annulus alone. Significant second-order nonlinearity appeared if the other region of the receptive field was also stimulated. 6. Membrane DC potentials of C amacrine cells remained at the dark level with either a white-noise spot or a white-noise annulus. The cell responded only to modulations. 7. The major characteristics of center and surround responses of C amacrine cells could be approximated by second-order Wiener kernels of the same structure. The receptive field of second-order nonlinear components of C amacrine cells was monotonic.(ABSTRACT TRUNCATED AT 400 WORDS)


1987 ◽  
Vol 57 (2) ◽  
pp. 357-380 ◽  
Author(s):  
D. N. Mastronarde

Cells in the cat's dorsal lateral geniculate nucleus (LGN) were studied by presentation of visual stimuli and also by simultaneous recording of their ganglion cell inputs in the retina. This paper describes receptive-field properties and a new system of classification for LGN X-cells that appear to receive essentially only one excitatory retinal input. These X-cells were of two distinct classes. The visual responses of one class of cell (XS, single) replicated the basic form of the responses of a retinal X-cell. The other class of cell (XL, lagged) had responses with two remarkable features: their firing lagged 40-80 ms behind that of XS-cells or ganglion cells at response onset, and they fired anomalously at times when XS-cells or ganglion cells would not be firing. Thus, for a flashing spot, XL-cells were inhibited from firing after stimulus onset, during the time when XS-cells or retinal X-cells had an initial transient peak in firing; XL-cells generally had an anomalous peak in firing after stimulus offset, after XS-cells or retinal X-cells had stopped firing. For a moving bar, XS-cells or retinal X-cells responded primarily while the bar was in the receptive-field center, whereas most of a typical XL-cell's response occurred after the bar had left the receptive-field center. The latencies of various features in the visual responses were analyzed. For several visual response latencies, the distribution was clearly bimodal, thus objectively demonstrating the existence of two cell classes. Using only the latencies from spot and bar responses, over 90% of these single-input cells could be reliably identified as belonging to one of the two classes. The remaining cells (7 of 128) were intermediate between the two classes in some but not all respects; because they had some properties in common, these cells were kept in a separate group (XPL, partially lagged). The axons of both XS- and XL-cells could be antidromically activated from visual cortex. Cortical latencies were typically 0.7-2.0 ms for XS-cells but much longer, typically 2.4-5.0 ms, for XL-cells. It is possible that XL-cells have not previously been recognized as a separate class because cells with such long latencies have been recorded infrequently in the past. Responses to central flashing spots were more transient than those of retinal X-cells for most XS-cells and more sustained for most XL-cells.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (4) ◽  
pp. 1547-1567 ◽  
Author(s):  
D. K. Merwine ◽  
F. R. Amthor ◽  
N. M. Grzywacz

1. The interaction between the center and surround mechanisms of a variety of rabbit retinal ganglion cell classes was examined in extracellular single-unit recordings in an isolated eyecup preparation. Ganglion cell classes studied included on and off brisk sustained and transient, on and off sluggish sustained and transient, on-off and on directionally selective, orientationally selective, and large field units. The surround effects observed were qualitatively similar in all these ganglion cell classes. 2. The average response-versus-contrast functions for stimuli within the ganglion cells' receptive-field centers were relatively linear between threshold and saturation for all ganglion cell classes examined. The major effect of surround stimulation on the center response-versus-contrast function was a reduction in the slope of the linear portion of the curve, rather than a downward, parallel shift of the function. Stimulation of the surround had no systematically significant effect on the contrast threshold for the center spot, and, when it did have a significant effect, it sometimes decreased, rather than increased the magnitude of threshold. 3. Step changes in surround contrast were most effective when they were made simultaneously with step changes in the center; surround inhibition decreased significantly when it preceded stimulation of the center by > 100 ms and was generally ineffective when preceding the center by > 500 ms. The decrease in the inhibitory effect of surround stimulation was a monotonic function of delay between 0 and 500 ms. 4. Stimulation of the surround by step changes in the contrast of a sine-wave grating annulus produced qualitatively similar results to those obtained for pure luminance modulations. This suggests that the surround mechanism observed in these experiments was not due to pure luminance adaptation within the surround. The inhibitory effect of sine-wave gratings in the surround decreased monotonically as a function of spatial frequency. 5. Stimulation with a spot and an annulus that were both entirely within the ganglion cell's excitatory receptive-field center typically yielded nonadditive summation at contrasts whose linear sum of responses were below saturation. The effect of an annulus within the receptive-field center on responses elicited by a central spot quantitatively resembled the inhibition elicited from annuli in the inhibitory surround, after the excitatory center response due to the annulus was taken into account. These results suggest that the inhibiton elicited from the surrounds of the ganglion cells in these experiments extended into their receptive-field centers.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 69 (6) ◽  
pp. 2174-2187 ◽  
Author(s):  
F. R. Amthor ◽  
N. M. Grzywacz

1. We have investigated the inhibitory mechanisms modulating the extracellularly recorded responses of ON-OFF directionally selective (DS) ganglion cells of the rabbit retina. Our investigations used both moving spots and apparent motion. The latter was produced by both prolonged light steps, which simulate movement of an edge, and light flashes, which simulate movement of a spot or slit. 2. Within the excitatory receptive-field center of DS ganglion cells, apparent motion with prolonged light steps elicits null-direction inhibition whose strength rises to 90% of maximum in 160 +/- 110 ms (7 cells) and then decays slowly, remaining above baseline longer than 2,000 ms for short interslit distances. 3. Prolonged light steps are generally effective for inhibiting any given excitatory receptive-field locus from an ovate-shaped area that extends asymmetrically in the direction that would be previously traversed by null-direction moving objects. This inhibitory area is typically larger than one-half the size of the receptive-field center. The strength of the inhibition is greater at short than long distances within this area. 4. The rise and fall times of the null-direction inhibition elicited by apparent motion using prolonged light steps are somewhat faster at large than short interslit distances. 5. Short light flashes (at sufficiently long interslit delays) elicit inhibition not only from the same asymmetric, ovate-shaped inhibitory field as long steps of light, but also from loci completely surrounding the second slit. This implies that the asymmetric, null-direction-specific inhibition is due to a temporally sustained mechanism. The symmetric inhibition elicited by short flashes may be due to the presence of the antagonistic surround mechanism within the receptive-field center. The apparent absence of this surround inhibition for preferred-direction apparent motion during prolonged light steps may be due to masking by facilitation that is strongly evoked by long steps, but not flashes of light (see accompanying paper). 6. The relatively slow rise time and sustained time course of the inhibition elicited by null-direction apparent motion within the excitatory receptive field center appears to distinguish it from the inhibition elicited by stimulation within the receptive field surround, which has a much faster rise time and more transient time course. However, the sustained, null-direction inhibitory mechanism that can be elicited by prolonged light steps within the excitatory receptive field center extends into the surround on the side of the receptive-field center previously traversed during null-direction motion.(ABSTRACT TRUNCATED AT 400 WORDS)


2003 ◽  
Vol 20 (4) ◽  
pp. 351-361 ◽  
Author(s):  
BRENDAN J. O'BRIEN ◽  
RANDAL C. RICHARDSON ◽  
DAVID M. BERSON

Cat retinal ganglion cells of the Y (or alpha) type respond to luminance changes opposite those preferred by their receptive-field centers with a transient hyperpolarization. Here, we examine the spatial organization and synaptic basis of this light response by means of whole-cell current-clamp recordings made in vitro. The hyperpolarization was largest when stimulus spots approximated the size of the receptive-field center, and diminished substantially for larger spots. The hyperpolarization was largely abolished by bath application of strychnine, a blocker of glycinergic inhibition. Picrotoxin, an antagonist of ionotropic GABA receptors, greatly reduced the attenuation of the hyperpolarizing response for large spots. The data are consistent with a model in which (1) the hyperpolarization reflects inhibition by glycinergic amacrine cells of bipolar terminals presynaptic to the alpha cells, and perhaps direct inhibition of the alpha cell as well; and (2) the attenuation of the hyperpolarization by large spots reflects surround inhibition of the glycinergic amacrine by GABAergic amacrine cells. This circuitry may moderate nonlinearities in the alpha-cell light response and could account for some excitatory and inhibitory influences on alpha cells known to arise from outside the classical receptive field.


2013 ◽  
Vol 31 (2) ◽  
pp. 139-151 ◽  
Author(s):  
DENNIS M. DACEY ◽  
JOANNA D. CROOK ◽  
ORIN S. PACKER

AbstractAnatomical and physiological approaches are beginning to reveal the synaptic origins of parallel ON- and OFF-pathway retinal circuits for the transmission of short (S-) wavelength sensitive cone signals in the primate retina. Anatomical data suggest that synaptic output from S-cones is largely segregated; central elements of synaptic triads arise almost exclusively from the “blue-cone” bipolar cell, a presumed ON bipolar, whereas triad-associated contacts derive primarily from the “flat” midget bipolar cell, a hyperpolarizing, OFF bipolar. Similarly, horizontal cell connectivity is also segregated, with only the H2 cell-type receiving numerous contacts from S-cones. Negative feedback from long (L-) and middle (M-) wavelength sensitive cones via the H2 horizontal cells elicits an antagonistic surround in S-cones demonstrating that S versus L + M or “blue-yellow” opponency is first established in the S-cone. However, the S-cone output utilizes distinct synaptic mechanisms to create color opponency at the ganglion cell level. The blue-cone bipolar cell is presynaptic to the small bistratified, “blue-ON” ganglion cell. S versus L + M cone opponency arises postsynaptically by converging S-ON and LM-OFF excitatory bipolar inputs to the ganglion cell’s bistratified dendritic tree. The common L + M cone surrounds of the parallel S-ON and LM-OFF cone bipolar inputs appear to cancel resulting in “blue-yellow” antagonism without center-surround spatial opponency. By contrast, in midget ganglion cells, opponency arises by the differential weighting of cone inputs to the receptive field center versus surround. In the macula, the “private-line” connection from a midget ganglion cell to a single cone predicts that S versus L + M opponency is transmitted from the S-cone to the S-OFF midget bipolar and ganglion cell. Beyond the macula, OFF-midget ganglion cell dendritic trees enlarge and collect additional input from multiple L and M cones. Thus S-OFF opponency via the midget pathway would be expected to become more complex in the near retinal periphery as L and/or M and S cone inputs sum to the receptive field center. An important goal for further investigation will be to explore the hypothesis that distinct bistratified S-ON versus midget S-OFF retinal circuits are the substrates for human psychophysical detection mechanisms attributed to S-ON versus S-OFF perceptual channels.


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