A possible explanation of the low-level brightness–contrast illusions in the light of an extended classical receptive field model of retinal ganglion cells

The low-level brightness–contrast illusions constitute a special class within visual illusions. Speculations exist that these illusions may be processed through the filtering action of the retinal ganglion cells without necessitating much intervention from higher order processes of visual perception. Concept of the classical receptive field of the ganglion cell, derived from early physiological studies, prompted the idea that a Difference of Gaussian (DoG) model might explain the low-level illusions. In spite of its many successes, the DoG model fails to explain some of these illusions. It has been shown in this paper that it is possible to simulate those illusions with a model that takes into cognizance the role of the extended classical receptive field     

Differential targeting of optical neuromodulators to ganglion cell soma and dendrites allows dynamic control of center-surround antagonism

Retinal degenerative diseases cause photoreceptor loss and often result in remodeling and deafferentation of the inner retina. Fortunately, ganglion cell morphology appears to remain intact long after photoreceptors and distal retinal circuitry have degenerated. We have introduced the optical neuromodulators channelrhodopsin-2 (ChR2) and halorhodopsin (NpHR) differentially into the soma and dendrites of ganglion cells to recreate antagonistic center-surround receptive field interactions. We then reestablished the physiological receptive field dimensions of primate parafoveal ganglion cells by convolving Gaussian-blurred versions of the visual scene at the appropriate wavelength for each neuromodulator with the Gaussians inherent in the soma and dendrites. These Gaussian-modified ganglion cells responded with physiologically relevant antagonistic receptive field components and encoded edges with parafoveal resolution. This approach bypasses the degenerated areas of the distal retina and could provide a first step in restoring sight to individuals suffering from retinal disease.     

A possible mechanism of stochastic resonance in the light of an extra-classical receptive field model of retinal ganglion cells

Traditionally the intensity discontinuities in an image are detected as zero-crossings of the second derivative with the help of a Laplacian of Gaussian (LOG) operator that models the receptive field of retinal Ganglion cells. Such zero-crossings supposedly form a raw primal sketch edge map of the external world in the primary visual cortex of the brain. Based on a new operator which is a linear combination of the LOG and a Dirac-delta function that models the extra-classical receptive field of the ganglion cells, we find that zero-crossing points thus generated, store in presence of noise, apart from the edge information, the shading information of the image in the form of density variation of these points. We have also shown that an optimal image contrast produces best mapping of the shading information to such zero-crossing density variation for a given amount of noise contamination. Furthermore, we have observed that an optimal amount of noise contamination reproduces the minimum optimal contrast and hence gives rise to the best representation of the original image. We show that this phenomenon is similar in nature to that of stochastic resonance phenomenon observed in psychophysical experiments.     

Features and functions of nonlinear spatial integration by retinal ganglion cells

Ganglion cells in the vertebrate retina integrate visual information over their receptive fields. They do so by pooling presynaptic excitatory inputs from typically many bipolar cells, which themselves collect inputs from several photoreceptors. In addition, inhibitory interactions mediated by horizontal cells and amacrine cells modulate the structure of the receptive field. In many models, this spatial integration is assumed to occur in a linear fashion. Yet, it has long been known that spatial integration by retinal ganglion cells also incurs nonlinear phenomena. Moreover, several recent examples have shown that nonlinear spatial integration is tightly connected to specific visual functions performed by different types of retinal ganglion cells. This work discusses these advances in understanding the role of nonlinear spatial integration and reviews recent efforts to quantitatively study the nature and mechanisms underlying spatial nonlinearities. These new insights point towards a critical role of nonlinearities within ganglion cell receptive fields for capturing responses of the cells to natural and behaviorally relevant visual stimuli. In the long run, nonlinear phenomena of spatial integration may also prove important for implementing the actual neural code of retinal neurons when designing visual prostheses for the eye.     

Delayed responses of ganglion cells in the frog retina: the influence of stimulus parameters upon the discharge pattern

The delayed response from frog retinal ganglion cells is preceded by a long silent period which has been shown to depend upon (i) intensity of the stimulus light flash, (ii) background illumination, and (iii) instantaneous level of adaptation. Also the duration of the delayed response and the total number of spikes elicited are functions of these three parameters. A linear relationship has been found between the silent period and both delayed response duration and total number of spikes. Double-flash experiments indicate that the ganglion cell output is strongly inhibited during the silent period. Experiments using an inhomogenous stimulus field have led to the conclusion that parts of the receptive field contribute independently to the delayed response.Supported by the Deutsche Forschungsgemeinschaft.S. G. P. was a postdoctoral fellow supported by a U. S. Public Health Service grant, NIH 1 F 2 NB 24,455-01.     

Synchronized firing among retinal ganglion cells signals motion reversal

We show that when a moving object suddenly reverses direction, there is a brief, synchronous burst of firing within a population of retinal ganglion cells. This burst can be driven by either the leading or trailing edge of the object. The latency is constant for movement at different speeds, objects of different size, and bright versus dark contrasts. The same ganglion cells that signal a motion reversal also respond to smooth motion. We show that the brain can build a pure reversal detector using only a linear filter that reads out synchrony from a group of ganglion cells. These results indicate that not only can the retina anticipate the location of a smoothly moving object, but that it can also signal violations in its own prediction. We show that the reversal response cannot be explained by models of the classical receptive field and suggest that nonlinear receptive field subunits may be responsible.     

Can the data of Campbell and Robson be explained without assuming fourier analysis?

Certain experiments on the detection of low-contrast gratings, occasionally cited as evidence of Fourier analysis within the visual system, are interpreted without the assumption of Fourier analysis. Theoretical curves are obtained and compared with the published experimental points, showing mostly satisfactory agreement. The computations utilize Gaussian receptive fields (on-center and off-center) for the retinal ganglion cells, spatial summation, center-surround antagonism, quasilinear response at low contrasts (X-cells), and the assumption that the first significant convergence is primarily between cells of like response type and like receptive field geometry.     

视网膜神经节细胞感受野的一种新模型 I.含大周边的感受野模型

感受野是视觉系统信息处理的基本结构和功能单元。Ｘ、Ｙ细胞是两类主要的视网膜神经节细胞。生理实验发现,在经典感受野之外还存在一个大范围的在周边去抑制区。文中采用周边去抑制区对经典外周的去抑制非线性使用方式,建立一个二维的与实验结果联系紧密的Ｘ、Ｙ细胞统一的复合感受野模型。该模型不仅能模拟Ｘ细胞的ｎｕｌｌ－ｔｅｓｔ反应和Ｙ细胞的ｏｎ－ｏｆｆ反应,还模拟了Ｙ细胞在低空频刺激时的信频反应、圆面积空间的倍频     

同心圆感受野去抑制特性的数学模拟

以感受野外周区内各亚区之间的抑制性相互作用为基础,提出了一个能描述视网膜神经节细胞传输特性的数学模型,此模型能很好地解释传统感受野外大范围去抑制区产生的机制。当用来处理亮度对比边缘时,它既能很好地增强边缘对比,又可有效地提升被传统感受野中心／外周拮抗机制所滤除了的区域亮度对比和亮度梯度信息。本文也用不同空间频率的光栅和真实图像检验了模型的空间频率传递特性,并与其它模型进行了比较。     

Transformation of Stimulus Correlations by the Retina

Redundancies and correlations in the responses of sensory neurons may seem to waste neural resources, but they can also carry cues about structured stimuli and may help the brain to correct for response errors. To investigate the effect of stimulus structure on redundancy in retina, we measured simultaneous responses from populations of retinal ganglion cells presented with natural and artificial stimuli that varied greatly in correlation structure; these stimuli and recordings are publicly available online. Responding to spatio-temporally structured stimuli such as natural movies, pairs of ganglion cells were modestly more correlated than in response to white noise checkerboards, but they were much less correlated than predicted by a non-adapting functional model of retinal response. Meanwhile, responding to stimuli with purely spatial correlations, pairs of ganglion cells showed increased correlations consistent with a static, non-adapting receptive field and nonlinearity. We found that in response to spatio-temporally correlated stimuli, ganglion cells had faster temporal kernels and tended to have stronger surrounds. These properties of individual cells, along with gain changes that opposed changes in effective contrast at the ganglion cell input, largely explained the pattern of pairwise correlations across stimuli where receptive field measurements were possible.     

Temporal pattern discrimination within the receptive field of cat retinal ganglion cells

ON-center and OFF-center receptive fields of cat retinal ganglion cells can be divided into two categories: sensitive (type N) and insensitive (type L) to three statistical temporal visual stimuli with different second order statistics but identical first order statistics (Tsukada et al. 1982). The temporal pattern sensitivity of type N response is closely related to the nonlinear stage of Y cells depending on the interaction between center and surround mechanism. The temporal pattern sensitivity of type N responses has a spatial profile within the receptive field; it is highly sensitive in the center region of the receptive field and less sensitive toward the field periphery. The temporal pattern sensitivity in the center region of the receptive field to statistical properties (irregular or regular) of a surrounding flash annulus shows modulation like a switching element: when the surrounding area is stimulated by a more regular flash stimulus with normal distribution of inter-stimulus intervals the system is sensitive (switching on) to the temporal pattern, while a change to an irregular one with an exponential distribution makes it insensitive (switching off) to the temporal pattern.     

Physiological response properties of cat retinal ganglion cells projecting to suprachiasmatic nucleus

The aim of this experiment was to characterize the physiological properties of cat retinal ganglion cells that project to the suprachiasmatic nucleus (SCN). Retrogradely labeled SCN-projecting ganglion cells were recorded extracellularly in vitro. For the first time, this study provides crucial information on visual response properties of ganglion cells in the entrainment circuitry. All recorded cells gave sustained responses (n = 9). Although most of the cells (n = 8) had an "on" center receptive field, one cell showed "on-off" center receptive field properties. The range of receptive field sizes was 2 to 5 deg. For most of the cells tested, the spectral wavelength that evoked peak responses was 500 nm (3 out of 5 cells). All recorded cells (n = 9) preferred still or extremely slow-moving stimuli (3.3 deg/s). These results indicate that cat SCN-projecting cells receive inputs from conventional photoreceptors. The hypothesis that both conventional and cryptochromic photoreceptors are involved in transferring photic signals is discussed.     

Receptive field microstructure and dendritic geometry of retinal ganglion cells

We studied the fine spatial structure of the receptive fields of retinal ganglion cells and its relationship to the dendritic geometry of these cells. Cells from which recordings had been made were microinjected with Lucifer yellow, so that responses generated at precise locations within the receptive field center could be directly compared with that cell's dendritic structure. While many cells with small receptive fields had domeshaped sensitivity profiles, the majority of large receptive fields were composed of multiple regions of high sensitivity. The density of dendritic branches at any one location did not predict the regions of high sensitivity. Instead, the interactions between a ganglion cell's dendritic tree and the local mosaic of bipolar cell axons seem to define the fine structure of the receptive field center.     

A spatio-temporal model of ganglion cell receptive field in the cat retina

A spatio-temporal model of ganglion cell receptive fields is proposed on the basis of receptive field characteristics of cat retinal ganglion cells reported in our previous paper. The model consists of the linear and nonlinear mechanisms in the ganglion cell receptive field. The linear mechanism is assumed to be composed of antagonistic center and surround mechanisms. Then, by integrating these mechanisms we construct a spatio-temporal impulse response function of ganglion cell receptive field. Here we assume that spatio-temporal impulse response function may be factored into spatial and temporal terms. By Fouriertransforming the spatio-temporal impulse response function, we can obtain the spatio-temporal transfer function. Contrast sensitivity characteristics of X-and Y-cells in the cat retina may be explained by the transfer function.     

Spatial asymmetries in cat retinal ganglion cell responses

. Enroth-Cugell and Robson (1966) first proposed a classification of retinal ganglion cells into X cells, which exhibit approximate linear spatial summation and largely sustained responses, and Y cells, which exhibit nonlinearities and transient responses. Gaudiano (1992a, 1992b, 1994) has suggested that the dominant characteristics of both X and Y cells can be simulated with a single model simply by changing receptive field profiles to match those of the anatomical counterparts of X and Y cells. He also proposed that a significant component of the spatial nonlinearities observed in Y (and sometimes X) cells can result from photoreceptor nonlinearities coupled with push-pull bipolar connections. Specifically, an asymmetry was predicted in the ganglion cell response to rectangular gratings presented at different locations in the receptive field under two conditions: introduction/withdrawal (on-off) or contrast reversal. When measuring the response to these patterns as a function of spatial phase, the standard difference-of-Gaussians model predicts symmetrical responses about the receptive field center, while the push-pull model predicts slight but significant asymmetry in the on-off case only. To test this hypothesis, we have recorded ganglion cell responses from the optic tract fibers of anesthetized cat. The mean and standard deviations of responses to on-off and contrast-reversed patterns were compared. We found that all but one of the cells that yielded statistically significant data confirmed the hypothesis. These results largely support the theoretical prediction. Received: 21 March 1997 / Accepted in revised form: 6 May 1998     

Adaptation-dependent synchronous activity contributes to receptive field size change of bullfrog retinal ganglion cell

Nearby retinal ganglion cells of similar functional subtype have a tendency to discharge spikes in synchrony. The synchronized activity is involved in encoding some aspects of visual input. On the other hand, neurons always continuously adjust their activities in adaptation to some features of visual stimulation, including mean ambient light, contrast level, etc. Previous studies on adaptation were primarily focused on single neuronal activity, however, it is also intriguing to investigate the adaptation process in population neuronal activities. In the present study, by using multi-electrode recording system, we simultaneously recorded spike discharges from a group of dimming detectors (OFF-sustained type ganglion cells) in bullfrog retina. The changes in receptive field properties and synchronization strength during contrast adaptation were analyzed. It was found that, when perfused using normal Ringer's solution, single neuronal receptive field size was reduced during contrast adaptation, which was accompanied by weakening in synchronization strength between adjacent neurons' activities. When dopamine (1 μM) was applied, the adaptation-related receptive field area shrinkage and synchronization weakening were both eliminated. The activation of D1 receptor was involved in the adaptation-related modulation of synchronization and receptive field. Our results thus suggest that the size of single neuron's receptive field is positively related to the strength of its synchronized activity with its neighboring neurons, and the dopaminergic pathway is responsible for the modulation of receptive field property and synchronous activity of the ganglion cells during the adaptation process.     

Asymmetry in structure of in termediate and large neurons of frog retinal ganglion layer

We have carried out a morphometric investigation of the symmetry of intermediate (type II) and large (types III and V) ganglion cells on silver-impregnated retinal wholemounts of frog retina. We selected the nucleolus of theneuron and the axis passing through the nucleolus in the direction of the optic disk (central and bilateral symmetry) as elements of symmetry. We have shown that the dendritic ramification angles of all cell types are smaller than 360° and those of type II cells smaller than 180°; the cell somata do not lie in the center of the dendritic field and consequently the ganglion cells do not possess radial symmetry. In the vast majority of ganglion cells the directions of the start of the axon and dendrites are opposite to each other, the dendrites being oriented in the direction from the retinal center towards the periphery in all quadrants of the retinal map. For the estimation of the bilateral symmetry we measured the distance from the most remote dendritic terminals to the axis on the left and right of the axis, and counted the number of ramification knots and basal dendrites. We established that the majority of ganglion cells are asymmetrical as regards two or three of the characteristics mentioned. Consequently the asymmetrical structure of ganglion cells of the frog is a normal characteristic rather than an exception. The correlation between the asymmetry of the structure of ganglion cells and the functional asymmetry of their receptive fields is discussed.N. I. Lobachevskii Research Institute of Applied Mathematics and Cybernetics, University of Gorki. Translated from Neirofiziologiya, Vol. 17, No. 4, pp. 456–462, July–August, 1985.     

Adaptation to Changes in Higher-Order Stimulus Statistics in the Salamander Retina

Adaptation in the retina is thought to optimize the encoding of natural light signals into sequences of spikes sent to the brain. While adaptive changes in retinal processing to the variations of the mean luminance level and second-order stimulus statistics have been documented before, no such measurements have been performed when higher-order moments of the light distribution change. We therefore measured the ganglion cell responses in the tiger salamander retina to controlled changes in the second (contrast), third (skew) and fourth (kurtosis) moments of the light intensity distribution of spatially uniform temporally independent stimuli. The skew and kurtosis of the stimuli were chosen to cover the range observed in natural scenes. We quantified adaptation in ganglion cells by studying linear-nonlinear models that capture well the retinal encoding properties across all stimuli. We found that the encoding properties of retinal ganglion cells change only marginally when higher-order statistics change, compared to the changes observed in response to the variation in contrast. By analyzing optimal coding in LN-type models, we showed that neurons can maintain a high information rate without large dynamic adaptation to changes in skew or kurtosis. This is because, for uncorrelated stimuli, spatio-temporal summation within the receptive field averages away non-gaussian aspects of the light intensity distribution.