Robust directional computation in on-off directionally selective ganglion cells of rabbit retina

2007 ◽  
Vol 24 (4) ◽  
pp. 647-661 ◽  
Author(s):  
NORBERTO M. GRZYWACZ ◽  
FRANKLIN R. AMTHOR
Keyword(s):  
Spatial Frequency ◽  
Ganglion Cell ◽  
Striate Cortex ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Directional Selectivity ◽  
Rabbit Retina ◽  
Stimulus Parameters ◽  
Sinusoidal Gratings ◽  
Temporal Interactions

The spatial and temporal interactions in the receptive fields of On-Off directionally selective (DS) ganglion cells endow them with directional selectivity. Using a variety of stimuli, such as sinusoidal gratings, we show that these interactions make directional selectivity of the DS ganglion cell robust with respect to stimulus parameters such as contrast, speed, spatial frequency, and extent of motion. Moreover, unlike the directional selectivity of striate-cortex cells, On-Off DS ganglion cells display directional selectivity to motions not oriented perpendicularly to the contour of the objects. We argue that these cells may achieve such high robustness by combining multiple mechanisms of directional selectivity.

Orientation and Direction Tuning of Goldfish Ganglion Cells

1989 ◽  
Vol 2 (1) ◽  
pp. 3-13 ◽  
Author(s):  
Joseph Bilotta ◽  
Israel Abramov
Keyword(s):  
Receptive Field ◽  
Spatial Frequency ◽  
Ganglion Cell ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Orientation Tuning ◽  
Retinal Ganglion ◽  
Spatial Frequencies ◽  
Sinusoidal Gratings ◽  
Direction Tuning

AbstractOrientation and direction tuning were examined in goldfish ganglion cells by drifting sinusoidal gratings across the receptive field of the cell. Each ganglion cell was first classified as X-, Y- or W-like based on its responses to a contrast-reversal grating positioned at various spatial phases of the cell's receptive field. Sinusoidal gratings were drifted at different orientations and directions across the receptive field of the cell; spatial frequency and contrast of the grating were also varied. It was found that some X-like cells responded similarly to all orientations and directions, indicating that these cells had circular and symmetrical fields. Other X-like cells showed a preference for certain orientations at high spatial frequencies suggesting that these cells possess an elliptical center mechanism (since only the center mechanism is sensitive to high spatial frequencies). In virtually all cases, X-like cells were not directionally tuned. All but one Y-like cell displayed orientation tuning but, as with X-like cells, orientation tuning appeared only at high spatial frequencies. A substantial portion of these Y-like cells also showed a direction preference. This preference was dependent on spatial frequency but in a manner different from orientation tuning, suggesting that these two phenomena result from different mechanisms. All W-like cells possessed orientation and direction tuning, both of which depended on the spatial frequency of the stimulus. These results support past work which suggests that the center and surround components of retinal ganglion cell receptive fields are not necessarily circular or concentric, and that they may actually consist of smaller subareas.

Properties of stimulus-dependent synchrony in retinal ganglion cells

2007 ◽  
Vol 24 (6) ◽  
pp. 827-843 ◽  
Author(s):  
SUSMITA CHATTERJEE ◽  
DAVID K. MERWINE ◽  
FRANKLIN R. AMTHOR ◽  
NORBERTO M. GRZYWACZ
Keyword(s):  
Ganglion Cell ◽  
Retinal Ganglion Cells ◽  
Functional Role ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Rabbit Retina ◽  
Retinal Ganglion ◽  
Spike Synchrony ◽  
Full Field ◽  
Dependent Correlation

Neighboring retinal ganglion cells often spike synchronously, but the possible function and mechanism of this synchrony is unclear. Recently, the strength of the fast correlation between ON-OFF directionally selective cells of the rabbit retina was shown to be stimulus dependent. Here, we extend that study, investigating stimulus-dependent correlation among multiple ganglion-cell classes, using multi-electrode recordings. Our results generalized those for directionally selective cells. All cell pairs exhibiting significant spike synchrony did it for an extended edge but rarely for full-field stimuli. The strength of this synchrony did not depend on the amplitude of the response and correlations could be present even when the cells' receptive fields did not overlap. In addition, correlations tended to be orientation selective in a manner predictable by the relative positions of the receptive fields. Finally, extended edges and full-field stimuli produced significantly greater and smaller correlations than predicted by chance respectively. We propose an amacrine-network model for the enhancement and depression of correlation. Such an apparently purposeful control of correlation adds evidence for retinal synchrony playing a functional role in vision.

Mosaic Arrangement of Ganglion Cell Receptive Fields in Rabbit Retina

1997 ◽  
Vol 78 (4) ◽  
pp. 2048-2060 ◽  
Author(s):  
Steven H. Devries ◽  
Denis A. Baylor
Keyword(s):  
Receptive Field ◽  
Ganglion Cell ◽  
Functional Organization ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Rabbit Retina ◽  
Unit Recording ◽  
Retinal Surface ◽  
Spatial Sensitivity ◽  
Temporal Structures

DeVries, Steven H. and Denis A. Baylor. Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J. Neurophysiol. 78: 2048–2060, 1997. The arrangement of ganglion cell receptive fields on the retinal surface should constrain several properties of vision, including spatial resolution. Anatomic and physiological studies on the mammalian retina have shown that the receptive fields of several types of ganglion cells tile the retinal surface, with the degree of receptive field overlap apparently being similar for the different classes. It has been difficult to test the generality of this arrangement, however, because it is hard to sample many receptive fields in the same preparation with conventional single-unit recording. In our experiments, the response properties and receptive fields of up to 80 neighboring ganglion cells in the isolated rabbit retina were characterized simultaneously by recording with a multielectrode array. The cells were divided into 11 classes on the basis of their characteristic light responses and the temporal structures of their impulse trains. The mosaic arrangement of receptive fields for cells of a given class was examined after the spatial profile of each receptive field was fitted with a generalized Gaussian surface. For eight cell classes the mosaic arrangement was similar: the profiles of neighboring cells approached each other at the 1-σ border. Thus field centers were 2 σ apart. The layout of fields for the remaining three classes was not well characterized because the fields were poorly fitted by a single Gaussian or because the cells responded selectively to movement. The 2-σ center-center spacing may be a general principle of functional organization that minimizes spatial aliasing and confers a uniform spatial sensitivity on the ganglion cell population.

Interactive effects among several stimulus parameters on the responses of striate cortical complex cells

1991 ◽  
Vol 66 (2) ◽  
pp. 379-389 ◽  
Author(s):  
T. J. Gawne ◽  
B. J. Richmond ◽  
L. M. Optican
Keyword(s):  
Striate Cortex ◽  
Neuronal Response ◽  
Receptive Fields ◽  
Response Strength ◽  
Interactive Effects ◽  
Temporal Modulation ◽  
Complex Cells ◽  
Black And White ◽  
Interaction Terms ◽  
Stimulus Parameters

1. Although neurons within the visual system are often described in terms of their responses to particular patterns such as bars and edges, they are actually sensitive to many different stimulus features, such as the luminances making up the patterns and the duration of presentation. Many different combinations of stimulus parameters can result in the same neuronal response, raising the problem of how the nervous system can extract information about visual stimuli from such inherently ambiguous responses. It has been shown that complex cells transmit significant amounts of information in the temporal modulation of their responses, raising the possibility that different stimulus parameters are encoded in different aspects of the response. To find out how much information is actually available about individual stimulus parameters, we examined the interactions among three stimulus parameters in the temporally modulated responses of striate cortical complex cells. 2. Sixteen black and white patterns were presented to two awake monkeys at each of four luminance-combinations and five durations, giving a total of 320 unique stimuli. Complex cells were recorded in layers 2 and 3 of striate cortex, with the stimuli centered on the receptive fields as determined by mapping with black and white bars. 3. An analysis of variance (ANOVA) was applied to these data with the three stimulus parameters of pattern, the luminance-combinations, and duration as the independent variables. The ANOVA was repeated with the magnitude and three different aspects of the temporal modulation of the response as the dependent variables. For the 19 neurons studied, many of the interactions between the different stimulus parameters were statistically significant. For some response measures the interactions accounted for more than one-half of the total response variance. 4. We also analyzed the stimulus-response relationships with the use of information theoretical techniques. We defined input codes on the basis of each stimulus parameter alone, as well as their combinations, and output codes on the basis of response strength, and on three measures of temporal modulation, also taken individually and together. Transmitted information was greatest when the response of a neuron was interpreted as a temporally modulated message about combinations of all three stimulus parameters. The interaction terms of the ANOVA suggest that the response of a complex cell can only be interpreted as a message about combinations of all three stimulus parameters.(ABSTRACT TRUNCATED AT 400 WORDS)

The number and distribution of bipolar to ganglion cell synapses in the inner plexiform layer of the anuran retina

1996 ◽  
Vol 13 (6) ◽  
pp. 1099-1107 ◽  
Author(s):  
Péter Buzás ◽  
Sára Jeges ◽  
Robert Gábriel
Keyword(s):  
Ganglion Cell ◽  
Cross Sections ◽  
Information Transfer ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Plexiform Layer ◽  
Amacrine Cells ◽  
Bipolar Cells ◽  
Inner Plexiform Layer ◽  
Flow Through

AbstractThe main route of information flow through the vertebrate retina is from the photoreceptors towards the ganglion cells whose axons form the optic nerve. Bipolar cells of the frog have been so far reported to contact mostly amacrine cells and the majority of input to ganglion cells comes from the amacrines. In this study, ganglion cells of frogs from two species (Bufo marinus, Xenopus laevis) were filled retrogradely with horseradish peroxidase. After visualization of the tracer, light-microscopic cross sections showed massive labeling of the somata in the ganglion cell layer as well as their dendrites in the inner plexiform layer. In cross sections, bipolar output and ganglion cell input synapses were counted in the electron microscope. Each synapse was assigned to one of the five equal sublayers (SLs) of the inner plexiform layer. In both species, bipolar cells were most often seen to form their characteristic synaptic dyads with two amacrine cells. In some cases, however, the dyads were directed to one amacrine and one ganglion cell dendrite. This type of synapse was unevenly distributed within the inner plexiform layer with the highest occurrence in SL2 both in Bufo and Xenopus. In addition, SL4 contained also a high number of this type of synapse in Xenopus. In both species, we found no or few bipolar to ganglion cell synapses in the marginal sublayers (SLs 1 and 5). In Xenopus, 22% of the bipolar cell output synapses went onto ganglion cells, whereas in Bufo this was only 10%. We conclude that direct bipolar to ganglion cell information transfer exists also in frogs although its occurrence is not as obvious and regular as in mammals. The characteristic distribution of these synapses, however, suggests that specific type of the bipolar and ganglion cells participate in this process. These contacts may play a role in the formation of simple ganglion cell receptive fields.

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.

Computation of motion direction by quail retinal ganglion cells that have a nonconcentric receptive field

2000 ◽  
Vol 17 (2) ◽  
pp. 263-271 ◽  
Author(s):  
HIROYUKI UCHIYAMA ◽  
TAKAHIDE KANAYA ◽  
SHOICHI SONOHATA
Keyword(s):  
Receptive Field ◽  
Retinal Ganglion Cells ◽  
Japanese Quail ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Object Motion ◽  
Directional Selectivity ◽  
Retinal Ganglion ◽  
Motion Direction ◽  
Neuronal Mechanisms

One type of retinal ganglion cells prefers object motion in a particular direction. Neuronal mechanisms for the computation of motion direction are still unknown. We quantitatively mapped excitatory and inhibitory regions of receptive fields for directionally selective retinal ganglion cells in the Japanese quail, and found that the inhibitory regions are displaced about 1–3 deg toward the side where the null sweep starts, relative to the excitatory regions. Directional selectivity thus results from delayed transient suppression exerted by the nonconcentrically arranged inhibitory regions, and not by local directional inhibition as hypothesized by Barlow and Levick (1965).

scholarly journals Light adaptation alters inner retinal inhibition to shape OFF retinal pathway signaling

2016 ◽  
Vol 115 (6) ◽  
pp. 2761-2778 ◽  
Author(s):  
Reece E. Mazade ◽  
Erika D. Eggers
Keyword(s):  
Ganglion Cell ◽  
Bipolar Cell ◽  
Light Adaptation ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Excitatory Input ◽  
Bipolar Cells ◽  
Visual Sensitivity ◽  
Resting Membrane Potential ◽  
Wide Range

The retina adjusts its signaling gain over a wide range of light levels. A functional result of this is increased visual acuity at brighter luminance levels (light adaptation) due to shifts in the excitatory center-inhibitory surround receptive field parameters of ganglion cells that increases their sensitivity to smaller light stimuli. Recent work supports the idea that changes in ganglion cell spatial sensitivity with background luminance are due in part to inner retinal mechanisms, possibly including modulation of inhibition onto bipolar cells. To determine how the receptive fields of OFF cone bipolar cells may contribute to changes in ganglion cell resolution, the spatial extent and magnitude of inhibitory and excitatory inputs were measured from OFF bipolar cells under dark- and light-adapted conditions. There was no change in the OFF bipolar cell excitatory input with light adaptation; however, the spatial distributions of inhibitory inputs, including both glycinergic and GABAergic sources, became significantly narrower, smaller, and more transient. The magnitude and size of the OFF bipolar cell center-surround receptive fields as well as light-adapted changes in resting membrane potential were incorporated into a spatial model of OFF bipolar cell output to the downstream ganglion cells, which predicted an increase in signal output strength with light adaptation. We show a prominent role for inner retinal spatial signals in modulating the modeled strength of bipolar cell output to potentially play a role in ganglion cell visual sensitivity and acuity.

Balanced interactions in ganglion-cell receptive fields

1999 ◽  
Vol 16 (2) ◽  
pp. 319-332 ◽  
Author(s):  
A.M. GRANDA ◽  
J.R. DEARWORTH ◽  
B. SUBRAMANIAM
Keyword(s):  
Ganglion Cell ◽  
Retinal Ganglion Cells ◽  
Ganglion Cells ◽  
Receptive Fields ◽  
Three Dimensions ◽  
Retinal Ganglion ◽  
Response Functions ◽  
Extracellular Recordings ◽  
Inhibitory Components

Receptive fields of retinal ganglion cells in turtle have excitatory and inhibitory components that are balanced along the dimensions of wavelength, functional ON and OFF responses, and spatial assignments of center and surround. These components were analyzed by spectral light adaptations and by the glutamate agonist, 2-amino-4-phosphonobutyric acid (APB). Extracellular recordings to stationary and moving spots of light were used to map changes in receptive fields. ON spike counts minus OFF spike counts, derived from flashed stationary light spots, quantified functional shifts by calculating normalized mean response modulations. The data show that receptive fields are not static, but rather are dynamic arrangements which depend on linked, antagonistic balances among the three dimensions of wavelength, ON and OFF response functions, and center/surround areas.

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.

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