Extra-receptive-field motion facilitation in on-off directionally selective ganglion cells of the rabbit retina

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.

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.


1993 ◽  
Vol 69 (6) ◽  
pp. 2188-2199 ◽  
Author(s):  
N. M. Grzywacz ◽  
F. R. Amthor

1. We have investigated the facilitation of extracellularly recorded responses of ON-OFF directionally selective (DS) ganglion cells of the rabbit retina to two-slit preferred-direction apparent motion produced by both prolonged light steps, which simulate movement of an edge past two apertures, 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 preferred-direction facilitation whose rise time (220 +/- 150 ms, average rise to 90% of maximum for 6 cells) is typically longer than the rise time of the excitatory response elicited by each slit. The decay time to baseline of facilitation during prolonged light steps is generally longer than 500 ms and hence greatly exceeds the typical duration of the excitatory response elicited by the slits. 3. Prolonged light steps are generally effective for facilitating any given excitatory receptive-field locus from a roughly ovoid area that typically extends on the order of 100-200 microns in the preferred direction, which is less than one-half the size of the excitatory receptive-field center. Within 100 microns, facilitation can occur for motion diagonal to the preferred-null axis as long as the projection of the motion on the preferred-null axis points in the preferred direction. 4. The time course of preferred-direction facilitation between two slits does not appear to have a strong systematical dependence on the interslit distance over the range in which facilitation is effective. 5. Short light flashes are ineffective for eliciting facilitation and, at sufficiently long interslit delays, elicit inhibition all around the test slit. This inhibition may be due to the antagonistic surround mechanism within the receptive-field center, which is effectively elicited by short-duration stimuli. 6. The effect of preferred-direction facilitation is addition-like, rather than multiplication-like. That is, the facilitatory effect of the first slit appears as the addition of a fixed value to the response-versus-contrast curve of the second slit, rather than a multiplication of the curve by a constant factor. The functional relationship between strength of facilitation and contrast of the first slit is sigmoidal, however, and thus nonlinear. 7. Experiments with long light steps show that the interaction between excitation and preferred-direction facilitation is largely segregated between the ON and OFF pathways.(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 (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.


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)


1991 ◽  
Vol 65 (2) ◽  
pp. 352-359 ◽  
Author(s):  
E. Cohen ◽  
P. Sterling

1. We have investigated the anatomic basis for the Gaussian-like receptive field center of the on-beta ("X") ganglion cell in the area centralis of cat retina. Three adjacent on-beta cells were reconstructed from electron micrographs of 279 serial sections cut vertically through a patch of retina at approximately 1 degree eccentricity. 2. All the bipolar synapses on these cells were identified, and about one-half of these were traced to type b1 bipolar cells, which formed a regular array in the plane of the retina. 3. On average, seven b1 cells contributed to a beta cell: bipolar axons near the middle of the beta dendritic field tended to give many contacts (12-33 contacts); axons near the edge of the field tended to give few contacts (3-4 contacts). 4. Each b1 cell collected from four to seven cones, and the mean number of cones converging through the b1 array to a beta cell was 30. 5. Assuming equal effectiveness for all b1----beta cell synapses, a spatial weighting function was derived from these results. The mean radius of this function at 1/e amplitude for three beta cells was 18.0 +/- 1.1 (SD) microns. This is considerably narrower than the corresponding measurements of the beta cell receptive field center (28 +/- 3 microns) at this eccentricity. 6. It is concluded, in agreement with previous work, that all cones encompassed by the beta cell's dendritic field and those slightly beyond it connect directly to the beta cell via the b1 bipolar cell array. However, the center of the beta cell receptive field is still broader by approximately 60%. This suggests that pooling of cone signals may occur at the level of the outer plexiform layer.


1979 ◽  
Vol 73 (3) ◽  
pp. 265-286 ◽  
Author(s):  
D F Wunk ◽  
F S Werblin

The postsynaptic potentials (PSPs) that form the ganglion cell light response were isolated by polarizing the cell membrane with extrinsic currents while stimulating at either the center or surround of the cell's receptive field. The time-course and receptive field properties of the PSPs were correlated with those of the bipolar and amacrine cells. The tiger salamander retina contains four main types of ganglion cell: "on" center, "off" center, "on-off", and a "hybrid" cell that responds transiently to center, but sustainedly, to surround illumination. The results lead to these inferences. The on-ganglion cell receives excitatory synpatic input from the on bipolars and that synapse is "silent" in the dark. The off-ganglion cell receives excitatory synaptic input from the off bipolars with this synapse tonically active in the dark. The on-off and hybrid ganglion cells receive a transient excitatory input with narrow receptive field, not simply correlated with the activity of any presynaptic cell. All cell types receive a broad field transient inhibitory input, which apparently originates in the transient amacrine cells. Thus, most, but not all, ganglion cell responses can be explained in terms of synaptic inputs from bipolar and amacrine cells, integrated at the ganglion cell membrane.


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