A Unified Model of Spatiotemporal Processing in the Retina

A computational model of visual processing in the vertebrate retina provides a unified explanation of a range of data previously treated by disparate models. Three results are reported here: the model proposes a functional explanation for the primary feed-forward retinal circuit found in vertebrate retinae, it shows how this retinal circuit combines nonlinear adaptation with the desirable properties of linear processing, and it accounts for the origin of parallel transient (nonlinear) and sustained (linear) visual processing streams as simple variants of the same retinal circuit. The retina, owing to its accessibility and to its fundamental role in the initial transduction of light into neural signals, is among the most extensively studied neural structures in the nervous system. Since the pioneering anatomical work by Ramón y Cajal at the turn of the last century[1], technological advances have abetted detailed descriptions of the physiological, pharmacological, and functional properties of many types of retinal cells. However, the relationship between structure and function in the retina is still poorly understood. This article outlines a computational model developed to address fundamental constraints of biological visual systems. Neurons that process nonnegative input signals-such as retinal illuminance-are subject to an inescapable tradeoff between accurate processing in the spatial and temporal domains. Accurate processing in both domains can be achieved with a model that combines nonlinear mechanisms for temporal and spatial adaptation within three layers of feed-forward processing. The resulting architecture is structurally similar to the feed-forward retinal circuit connecting photoreceptors to retinal ganglion cells through bipolar cells. This similarity suggests that the three-layer structure observed in all vertebrate retinae[2] is a required minimal anatomy for accurate spatiotemporal visual processing. This hypothesis is supported through computer simulations showing that the model's output layer accounts for many properties of retinal ganglion cells[3],[4],[5],[6]. Moreover, the model shows how the retina can extend its dynamic range through nonlinear adaptation while exhibiting seemingly linear behavior in response to a variety of spatiotemporal input stimuli. This property is the basis for the prediction that the same retinal circuit can account for both sustained (X) and transient (Y) cat ganglion cells[7] by simple morphological changes. The ability to generate distinct functional behaviors by simple changes in cell morphology suggests that different functional pathways originating in the retina may have evolved from a unified anatomy designed to cope with the constraints of low-level biological vision.Sloan Fellowshi

A Nonlinear Model of Spatiotemporal Retinal Processing: Simulations of X and Y Retinal Ganglion Cell Behavior

This article describes a nonlinear model of neural processing in the vertebrate retina, comprising model photoreceptors, model push-pull bipolar cells, and model ganglion cells. Previous analyses and simulations have shown that with a choice of parameters that mimics beta cells, the model exhibits X-like linear spatial summation (null response to contrast-reversed gratings) in spite of photoreceptor nonlinearities; on the other hand, a choice of parameters that mimics alpha cells leads to Y-like frequency doubling. This article extends the previous work by showing that the model can replicate qualitatively many of the original findings on X and Y cells with a fixed choice of parameters. The results generally support the hypothesis that X and Y cells can be seen as functional variants of a single neural circuit. The model also suggests that both depolarizing and hyperpolarizing bipolar cells converge onto both ON and OFF ganglion cell types. The push-pull connectivity enables ganglion cells to remain sensitive to deviations about the mean output level of nonlinear photoreceptors. These and other properties of the push-pull model are discussed in the general context of retinal processing of spatiotemporal luminance patterns.Alfred P. Sloan Research Fellowship (BR-3122); Air Force Office of Scientific Research (F49620-92-J-0499

A reaction-diffusion model of cholinergic retinal waves

Prior to receiving visual stimuli, spontaneous, correlated activity called retinal waves drives activity-dependent developmental programs. Early-stage waves mediated by acetylcholine (ACh) manifest as slow, spreading bursts of action potentials. They are believed to be initiated by the spontaneous firing of Starburst Amacrine Cells (SACs), whose dense, recurrent connectivity then propagates this activity laterally. Their extended inter-wave intervals and shifting wave boundaries are the result of the slow after-hyperpolarization of the SACs creating an evolving mosaic of recruitable and refractory cells, which can and cannot participate in waves, respectively. Recent evidence suggests that cholinergic waves may be modulated by the extracellular concentration of ACh. Here, we construct a simplified, biophysically consistent, reaction-diffusion model of cholinergic retinal waves capable of recapitulating wave dynamics observed in mice retina recordings. The dense, recurrent connectivity of SACs is modeled through local, excitatory coupling occurring via the volume release and diffusion of ACh. In contrast with previous, simulation-based models, we are able to use non-linear wave theory to connect wave features to underlying physiological parameters, making the model useful in determining appropriate pharmacological manipulations to experimentally produce waves of a prescribed spatiotemporal character. The model is used to determine how ACh mediated connectivity may modulate wave activity, and how the noise rate and sAHP refractory period contributes to critical wave size variability.Comment: 38 pages, 10 figure

A Neural Model of How the Brain Computes Heading from Optic Flow in Realistic Scenes

Animals avoid obstacles and approach goals in novel cluttered environments using visual information, notably optic flow, to compute heading, or direction of travel, with respect to objects in the environment. We present a neural model of how heading is computed that describes interactions among neurons in several visual areas of the primate magnocellular pathway, from retina through V1, MT+, and MSTd. The model produces outputs which are qualitatively and quantitatively similar to human heading estimation data in response to complex natural scenes. The model estimates heading to within 1.5° in random dot or photo-realistically rendered scenes and within 3° in video streams from driving in real-world environments. Simulated rotations of less than 1 degree per second do not affect model performance, but faster simulated rotation rates deteriorate performance, as in humans. The model is part of a larger navigational system that identifies and tracks objects while navigating in cluttered environments.National Science Foundation (SBE-0354378, BCS-0235398); Office of Naval Research (N00014-01-1-0624); National-Geospatial Intelligence Agency (NMA201-01-1-2016

Suboptimal eye movements for seeing fine details.

Human eyes are never stable, even during attempts of maintaining gaze on a visual target. Considering transient response characteristics of retinal ganglion cells, a certain amount of motion of the eyes is required to efficiently encode information and to prevent neural adaptation. However, excessive motion of the eyes leads to insufficient exposure to the stimuli, which creates blur and reduces visual acuity. Normal miniature eye movements fall in between these extremes, but it is unclear if they are optimally tuned for seeing fine spatial details. We used a state-of-the-art retinal imaging technique with eye tracking to address this question. We sought to determine the optimal gain (stimulus/eye motion ratio) that corresponds to maximum performance in an orientation-discrimination task performed at the fovea. We found that miniature eye movements are tuned but may not be optimal for seeing fine spatial details

A Theoretical Analysis of the Influence of Fixational Instability on the Development of Thalamocortical Connectivity

Under natural viewing conditions, the physiological inotability of visual fixation keeps the projection of the stimulus on the retina in constant motion. After eye opening, chronic exposure to a constantly moving retinal image might influence the experience-dependent refinement of cell response characteristics. The results of previous modeling studies have suggested a contribution of fixational instability in the Hebbian maturation of the receptive fields of V1 simple cells (Rucci, Edelman, & Wray, 2000; Rucci & Casile, 2004). This paper presents a mathematieal explanation of our previous computational results. Using quasi-linear models of LGN units and V1 simple cells, we derive analytical expressions for the second-order statistics of thalamocortical activity before and after eye opening. We show that in the presence of natural stimulation, fixational instability introduces a spatially uncorrelated signal in the retinal input, whieh strongly influences the structure of correlated activity in the model

Modeling convergent ON and OFF pathways in the early visual system

For understanding the computation and function of single neurons in sensory systems, one needs to investigate how sensory stimuli are related to a neuron’s response and which biological mechanisms underlie this relationship. Mathematical models of the stimulus–response relationship have proved very useful in approaching these issues in a systematic, quantitative way. A starting point for many such analyses has been provided by phenomenological “linear–nonlinear” (LN) models, which comprise a linear filter followed by a static nonlinear transformation. The linear filter is often associated with the neuron’s receptive field. However, the structure of the receptive field is generally a result of inputs from many presynaptic neurons, which may form parallel signal processing pathways. In the retina, for example, certain ganglion cells receive excitatory inputs from ON-type as well as OFF-type bipolar cells. Recent experiments have shown that the convergence of these pathways leads to intriguing response characteristics that cannot be captured by a single linear filter. One approach to adjust the LN model to the biological circuit structure is to use multiple parallel filters that capture ON and OFF bipolar inputs. Here, we review these new developments in modeling neuronal responses in the early visual system and provide details about one particular technique for obtaining the required sets of parallel filters from experimental data

Towards building a more complex view of the lateral geniculate nucleus: Recent advances in understanding its role

The lateral geniculate nucleus (LGN) has often been treated in the past as a linear filter that adds little to retinal processing of visual inputs. Here we review anatomical, neurophysiological, brain imaging, and modeling studies that have in recent years built up a much more complex view of LGN . These include effects related to nonlinear dendritic processing, cortical feedback, synchrony and oscillations across LGN populations, as well as involvement of LGN in higher level cognitive processing. Although recent studies have provided valuable insights into early visual processing including the role of LGN, a unified model of LGN responses to real-world objects has not yet been developed. In the light of recent data, we suggest that the role of LGN deserves more careful consideration in developing models of high-level visual processing