Early Visual Pathway Research Articles

Seeing without knowing: Operational principles along the early visual pathway

Single cases may lead to unexpected hypotheses in psychology. We retrospectively analyzed single case studies that suggested organizational principles along the early visual pathway, which have remained unanswered until now. In spite of the inhomogeneity of sensitivity, paradoxically the visual field on the subjective level appears to be homogeneous; constancy of brightness of supra-threshold stimuli throughout the visual field is claimed to be responsible for homogeneity; specific summation properties of retinal ganglion cells are hypothesized to guarantee this effect. With a brain-injured patient having suffered a partial visual field loss it can be shown that color induction is a retinal phenomenon; lateral inhibitory processes at the level of amacrine cells are hypothesized as neural network. Third case: In a patient having suffered a bilateral occipital lobe infarction, some functional recovery has been demonstrated; divergence and convergence of projection in the ascending neural pathway are suggested as a structural basis for recovery. Slowed down binocular rivalry discloses a sequential mechanism in the construction of a visual percept. Fourth case: The pre-wired projection of the retina to the visual cortex in spite of a severe squint of one eye is confirmed, but paradoxically some local neuroplasticity is also suggested. Fifth case: Using habituation of local sensitivity in the visual field and its resetting by interhemispheric interactions as an experimental paradigm, it is suggested that spatial attention is controlled at the midbrain level. Sixth case: Observations on residual vision or "blindsight" support the hypothesis that the visual cortex is the one and only structure responsible for visual perception on a conscious level. The unifying principle of these retrospective analyses is that subjective visual phenomena can lead to unexpected but testable hypotheses of neural processing on the structural and functional level in the early visual pathway.

Serial grouping of 2D-image regions with object-based attention in humans.

After an initial stage of local analysis within the retina and early visual pathways, the human visual system creates a structured representation of the visual scene by co-selecting image elements that are part of behaviorally relevant objects. The mechanisms underlying this perceptual organization process are only partially understood. We here investigate the time-course of perceptual grouping of two-dimensional image-regions by measuring the reaction times of human participants and report that it is associated with the gradual spread of object-based attention. Attention spreads fastest over large and homogeneous areas and is slowed down at locations that require small-scale processing. We find that the time-course of the object-based selection process is well explained by a 'growth-cone' model, which selects surface elements in an incremental, scale-dependent manner. We discuss how the visual cortical hierarchy can implement this scale-dependent spread of object-based attention, leveraging the different receptive field sizes in distinct cortical areas.

Biophysical Network Modelling of the dLGN Circuit: Different Effects of Triadic and Axonal Inhibition on Visual Responses of Relay Cells.

Despite its prominent placement between the retina and primary visual cortex in the early visual pathway, the role of the dorsal lateral geniculate nucleus (dLGN) in molding and regulating the visual signals entering the brain is still poorly understood. A striking feature of the dLGN circuit is that relay cells (RCs) and interneurons (INs) form so-called triadic synapses, where an IN dendritic terminal can be simultaneously postsynaptic to a retinal ganglion cell (GC) input and presynaptic to an RC dendrite, allowing for so-called triadic inhibition. Taking advantage of a recently developed biophysically detailed multicompartmental model for an IN, we here investigate putative effects of these different inhibitory actions of INs, i.e., triadic inhibition and standard axonal inhibition, on the response properties of RCs. We compute and investigate so-called area-response curves, that is, trial-averaged visual spike responses vs. spot size, for circular flashing spots in a network of RCs and INs. The model parameters are grossly tuned to give results in qualitative accordance with previous in vivo data of responses to such stimuli for cat GCs and RCs. We particularly investigate how the model ingredients affect salient response properties such as the receptive-field center size of RCs and INs, maximal responses and center-surround antagonisms. For example, while triadic inhibition not involving firing of IN action potentials was found to provide only a non-linear gain control of the conversion of input spikes to output spikes by RCs, axonal inhibition was in contrast found to substantially affect the receptive-field center size: the larger the inhibition, the more the RC center size shrinks compared to the GC providing the feedforward excitation. Thus, a possible role of the different inhibitory actions from INs to RCs in the dLGN circuit is to provide separate mechanisms for overall gain control (direct triadic inhibition) and regulation of spatial resolution (axonal inhibition) of visual signals sent to cortex.

Contrasting Bottom-up Saliency and Top-Down Attention in the Early Visual Pathway

Contrasting Bottom-up Saliency and Top-Down Attention in the Early Visual Pathway

Linear Neural Circuitry Model for Visual Receptive Fields

The current state of art in the literature indicates that linear visual receptive fields are Gaussian or formed based on Gaussian kernels in biological visual systems. In this paper, by employing hypotheses based on the anatomy and physiology of vertebrate biological vision, we propose a neural circuitry possessing Gaussian-related visual receptive fields. Here, we present a plausible circuitry system matching the characteristic properties of an ideal visual front end of biological visual systems and then present a condition under which this circuit demonstrates a linear behaviour to model the linear receptive fields observed in the biological experimental data. The objective of this study is to understand the hardware circuitry from which various visual receptive fields in biological visual system can be deduced. In our model, a nonlinear neural network communicating with spikes is considered. The condition under which this neural network behaves linearly is discussed. The equivalent linear circuit proposed here employs some anatomical and physiological properties of the early biological visual pathway to derive the visual receptive field profiles for linear cells such as neurons with isotropic separable, non-isotropic separable and non-separable (velocity-adapted) Gaussian receptive fields in the LGN and striate cortex. In the model presented here, the theory of transmission lines for linear distributed electrical circuits is employed for two-dimensional transmission grids to model cell connectivities in a neural layer. The model presented here leads to a formulation similar to the Gaussian scale-space theory for the transmission of visual signals through various layers of neurons. Our model therefore presents a new insight on how the convolution process with Gaussian kernels can be implemented in vertebrate visual systems. The comparison of the numerical simulations of our model presented in this paper with the data analysis of receptive field profiles recorded in the biological literature demonstrates a complete agreement between our theoretical model and experimental data. Our model is also in good agreement with the numerical results of the Gaussian scale-space theory for the visual receptive fields.

Predicting Cortical Dark/Bright Asymmetries from Natural Image Statistics and Early Visual Transforms

The nervous system has evolved in an environment with structure and predictability. One of the ubiquitous principles of sensory systems is the creation of circuits that capitalize on this predictability. Previous work has identified predictable non-uniformities in the distributions of basic visual features in natural images that are relevant to the encoding tasks of the visual system. Here, we report that the well-established statistical distributions of visual features -- such as visual contrast, spatial scale, and depth -- differ between bright and dark image components. Following this analysis, we go on to trace how these differences in natural images translate into different patterns of cortical input that arise from the separate bright (ON) and dark (OFF) pathways originating in the retina. We use models of these early visual pathways to transform natural images into statistical patterns of cortical input. The models include the receptive fields and non-linear response properties of the magnocellular (M) and parvocellular (P) pathways, with their ON and OFF pathway divisions. The results indicate that there are regularities in visual cortical input beyond those that have previously been appreciated from the direct analysis of natural images. In particular, several dark/bright asymmetries provide a potential account for recently discovered asymmetries in how the brain processes visual features, such as violations of classic energy-type models. On the basis of our analysis, we expect that the dark/bright dichotomy in natural images plays a key role in the generation of both cortical and perceptual asymmetries.

Retinal waves regulate afferent terminal targeting in the early visual pathway

Current models of retinogeniculate development have proposed that connectivity between the retina and the dorsal lateral geniculate nucleus (dLGN) is established by gradients of axon guidance molecules, to allow initial coarse connections, and by competitive Hebbian-like processes, to drive eye-specific segregation and refine retinotopy. Here we show that when intereye competition is eliminated by monocular enucleation, blocking cholinergic stage II retinal waves disrupts the intraeye competition-mediated expansion of the retinogeniculate projection and results in the permanent disorganization of its laminae. This disruption of stage II retinal waves also causes long-term impacts on receptive field size and fine-scale retinotopy in the dLGN. Our results reveal a novel role for stage II retinal waves in regulating retinogeniculate afferent terminal targeting by way of intraeye competition, allowing for correct laminar patterning and the even allocation of synaptic territory. These findings should contribute to answering questions regarding the role of neural activity in guiding the establishment of neural circuits.

Altered white matter in early visual pathways of humans with amblyopia

Amblyopia is a visual disorder caused by poorly coordinated binocular input during development. Little is known about the impact of amblyopia on the white matter within the visual system. We studied the properties of six major visual white-matter pathways in a group of adults with amblyopia (n=10) and matched controls (n=10) using diffusion weighted imaging (DWI) and fiber tractography. While we did not find significant differences in diffusion properties in cortico-cortical pathways, patients with amblyopia exhibited increased mean diffusivity in thalamo-cortical visual pathways. These findings suggest that amblyopia may systematically alter the white matter properties of early visual pathways.

Delayed early primary visual pathway development in premature infants: high density electrophysiological evidence.

In the past decades, multiple studies have been interested in developmental patterns of the visual system in healthy infants. During the first year of life, differential maturational changes have been observed between the Magnocellular (P) and the Parvocellular (P) visual pathways. However, few studies investigated P and M system development in infants born prematurely. The aim of the present study was to characterize P and M system maturational differences between healthy preterm and fullterm infants through a critical period of visual maturation: the first year of life. Using a cross-sectional design, high-density electroencephalogram (EEG) was recorded in 31 healthy preterms and 41 fullterm infants of 3, 6, or 12 months (corrected age for premature babies). Three visual stimulations varying in contrast and spatial frequency were presented to stimulate preferentially the M pathway, the P pathway, or both systems simultaneously during EEG recordings. Results from early visual evoked potentials in response to the stimulation that activates simultaneously both systems revealed longer N1 latencies and smaller P1 amplitudes in preterm infants compared to fullterms. Moreover, preterms showed longer N1 and P1 latencies in response to stimuli assessing the M pathway at 3 months. No differences between preterms and fullterms were found when using the preferential P system stimulation. In order to identify the cerebral generator of each visual response, distributed source analyses were computed in 12-month-old infants using LORETA. Source analysis demonstrated an activation of the parietal dorsal region in fullterm infants, in response to the preferential M pathway, which was not seen in the preterms. Overall, these findings suggest that the Magnocellular pathway development is affected in premature infants. Although our VEP results suggest that premature children overcome, at least partially, the visual developmental delay with time, source analyses reveal abnormal brain activation of the Magnocellular pathway at 12 months of age.

Effects of visual attention on chromatic and achromatic detection sensitivities.

Visual attention has a significant effect on various visual functions, such as response time, detection and discrimination sensitivity, and color appearance. It has been suggested that visual attention may affect visual functions in the early visual pathways. In this study we examined selective effects of visual attention on sensitivities of the chromatic and achromatic pathways to clarify whether visual attention modifies responses in the early visual system. We used a dual task paradigm in which the observer detected a peripheral test stimulus presented at 4deg eccentricities while the observer concurrently carried out an attention task in the central visual field. In experiment 1, it was confirmed that peripheral spectral sensitivities were reduced more for short and long wavelengths than for middle wavelengths with the central attention task so that the spectral sensitivity function changed its shape by visual attention. This indicated that visual attention affected the chromatic response more strongly than the achromatic response. In experiment 2 it was obtained that the detection thresholds increased in greater degrees in the red-green and yellow-blue chromatic directions than in the white-black achromatic direction in the dual task condition. In experiment 3 we showed that the peripheral threshold elevations depended on the combination of color-directions of the central and peripheral stimuli. Since the chromatic and achromatic responses were separately processed in the early visual pathways, the present results provided additional evidence that visual attention affects responses in the early visual pathways.

Color opponent receptive fields self-organize in a biophysical model of visual cortex via spike-timing dependent plasticity.

Although many computational models have been proposed to explain orientation maps in primary visual cortex (V1), it is not yet known how similar clusters of color-selective neurons in macaque V1/V2 are connected and develop. In this work, we address the problem of understanding the cortical processing of color information with a possible mechanism of the development of the patchy distribution of color selectivity via computational modeling. Each color input is decomposed into a red, green, and blue representation and transmitted to the visual cortex via a simulated optic nerve in a luminance channel and red–green and blue–yellow opponent color channels. Our model of the early visual system consists of multiple topographically-arranged layers of excitatory and inhibitory neurons, with sparse intra-layer connectivity and feed-forward connectivity between layers. Layers are arranged based on anatomy of early visual pathways, and include a retina, lateral geniculate nucleus, and layered neocortex. Each neuron in the V1 output layer makes synaptic connections to neighboring neurons and receives the three types of signals in the different channels from the corresponding photoreceptor position. Synaptic weights are randomized and learned using spike-timing-dependent plasticity (STDP). After training with natural images, the neurons display heightened sensitivity to specific colors. Information-theoretic analysis reveals mutual information between particular stimuli and responses, and that the information reaches a maximum with fewer neurons in the higher layers, indicating that estimations of the input colors can be done using the output of fewer cells in the later stages of cortical processing. In addition, cells with similar color receptive fields form clusters. Analysis of spiking activity reveals increased firing synchrony between neurons when particular color inputs are presented or removed (ON-cell/OFF-cell).

Dietary Omega-3 Fatty Acids Modulate Large-Scale Systems Organization in the Rhesus Macaque Brain

Omega-3 fatty acids are essential for healthy brain and retinal development and have been implicated in a variety of neurodevelopmental disorders. This study used resting-state functional connectivity MRI to define the large-scale organization of the rhesus macaque brain and changes associated with differences in lifetime ω-3 fatty acid intake. Monkeys fed docosahexaenoic acid, the long-chain ω-3 fatty acid abundant in neural membranes, had cortical modular organization resembling the healthy human brain. In contrast, those with low levels of dietary ω-3 fatty acids had decreased functional connectivity within the early visual pathway and throughout higher-order associational cortex and showed impairment of distributed cortical networks. Our findings illustrate the similarity in modular cortical organization between the healthy human and macaque brain and support the notion that ω-3 fatty acids play a crucial role in developing and/or maintaining distributed, large-scale brain systems, including those essential for normal cognitive function.

Visual Circuits: Mouse Retina No Longer a Level Playing Field

Unlike humans, monkeys, or carnivores, mice are thought to lack a retinal subregion devoted to high-resolution vision; systematic analysis has now shown that mice encode visual space non-uniformly, increasing their spatial sampling of the binocular visual field.

Spatiotemporal flow of information in the early visual pathway

The spatial components of a visual scene are processed neurally in a sequence of coarse features followed by fine features. This coarse-to-fine temporal stream was initially considered to be a cortical function, but has recently been demonstrated in the dorsal lateral geniculate nucleus. The goal of this study was to test the hypothesis that coarse-to-fine processing is present at earlier stages of visual processing in the retinal ganglion cells that supply lateral geniculate nucleus (LGN) neurons. To compare coarse-to-fine processing in the cat's visual system, we measured the visual responses of connected neuronal pairs from the retina and LGN, and separate populations of cells from each region. We found that coarse-to-fine processing was clearly present at the ganglion cell layer of the retina. Interestingly, peak and high-spatial-frequency cutoff responses were higher in the LGN than in the retina, indicating that there was a progressive cascade of coarse-to-fine information from the retina to the LGN to the visual cortex. The analysis of early visual pathway receptive field characteristics showed that the physiological response interplay between the center and surround regions was consistent with coarse-to-fine features and may provide a primary role in the underlying mechanism. Taken together, the results from this study provided a framework for understanding the emergence and refinement of coarse-to-fine processing in the visual system.

Modeling a space-variant cortical representation for apparent motion

Receptive field sizes of neurons in early primate visual areas increase with eccentricity, as does temporal processing speed. The fovea is evidently specialized for slow, fine movements while the periphery is suited for fast, coarse movements. In either the fovea or periphery discrete flashes can produce motion percepts. Grossberg and Rudd (1989) used traveling Gaussian activity profiles to model long-range apparent motion percepts. We propose a neural model constrained by physiological data to explain how signals from retinal ganglion cells to V1 affect the perception of motion as a function of eccentricity. Our model incorporates cortical magnification, receptive field overlap and scatter, and spatial and temporal response characteristics of retinal ganglion cells for cortical processing of motion. Consistent with the finding of Baker and Braddick (1985), in our model the maximum flash distance that is perceived as an apparent motion (Dmax) increases linearly as a function of eccentricity. Baker and Braddick (1985) made qualitative predictions about the functional significance of both stimulus and visual system parameters that constrain motion perception, such as an increase in the range of detectable motions as a function of eccentricity and the likely role of higher visual processes in determining Dmax. We generate corresponding quantitative predictions for those functional dependencies for individual aspects of motion processing. Simulation results indicate that the early visual pathway can explain the qualitative linear increase of Dmax data without reliance on extrastriate areas, but that those higher visual areas may serve as a modulatory influence on the exact Dmax increase.

Affective engagement and subsequent visual processing: Effects of contrast and spatial frequency.

The present study examined if viewing affective stimuli alters subsequent visual processing, as indexed by steady-state visual potentials (ssVEPs) and behavioral performance in an orientation discrimination task. Participants viewed task-irrelevant but emotionally arousing pictures from the International Affective Picture System (1 s) followed by a target stimulus stream consisting of low (2 cpd) or high-spatial frequency (6 cpd) Gabor patches, flickering at a temporal rate of 14 Hz. Luminance contrast of the patches gradually increased for the first half and decreased for the second half of the total duration, resulting in a waxing-waning pattern of stimulus contrast. The authors found that the waveform envelope of 14 Hz-ssVEPs corresponded to time-varying stimulus contrast. Analyses compared medium- and high-contrast time segments, as a function of emotional content and spatial frequency. Results showed greater ssVEP amplitudes for patches with high compared to medium contrast. Viewing emotionally arousing pictures selectively enhanced the ssVEP amplitudes for low-spatial frequency target patches and attenuated the ssVEP evoked by high-spatial frequency patches, across contrast levels. Response times were slower for patches following unpleasant pictures rather than pleasant and neutral, and error rates mirrored the interaction of emotional content and spatial frequency observed in the ssVEP data. Together, the present results suggest that additive gain mechanisms and early visual pathways may mediate costs and benefits of emotional engagement for subsequent sensory processing.

The Role of Delayed Suppression in Slow and Fast Contrast Adaptation in V1 Simple Cells

The sensitivity and rate of neural coding along the early visual pathways adapt to changes in contrast of the retinal image caused by external motion or self-generated eye movements. To identify the functional mechanisms of fast and slow contrast adaptation at the level of the visual cortex, we randomly varied, over both short and long timescales, the contrast of optimal sinusoidal gratings flashed in the receptive field of simple cells. We found that fast contrast-dependent suppression lagged excitation by ~11 ms and controlled the spike's temporal precision. During slow adaptation to low contrasts, the gain and latency of excitation increased whereas suppression became less visible, resulting in more sensitive but slower and more variable responses. We conclude that delayed suppression controls the response dynamics during both fast and slow contrast adaptation. More generally, we propose that sensory adaptation trades neuronal sensitivity for processing speed by changing the balance between excitation and delayed inhibition.

Color and Spatial Frequency Are Related to Visual Pattern Sensitivity in Migraine

To assess the potential for particular colors to alleviate visual discomfort when people with migraine view repetitive geometric or striped patterns. Visual stimuli, such as flicker, glare, or stripes, can trigger migraine and headache. They can also elicit feelings of discomfort and aversion. There are reports that color can be used to decrease the experience of discomfort and reduce migraine frequency. Five sets of striped patterns (3, 12 cycles per degree [cpd]) were created using cardinal colors tailored to selectively stimulate the early visual pathways: achromatic (black/white), tritan (black/purple, black/yellow), protan/deutan (black/red, black/green). All had the same high luminance contrast (0.9 Michelson contrast). Twenty-eight migraine (14 migraine with aura, 14 migraine without aura) and 14 control participants rated the discomfort and described the distortions seen in these patterns. They were also assessed for visual migraine/headache triggers, contrast sensitivity, color vision, acuity, stereopsis, visual discomfort from reading, and dyslexia. In the migraine groups, a comparable number of illusions were seen with the 3 and 12 cpd achromatic gratings, whereas in the control group the greatest number was seen with the 3 cpd grating. In the migraine groups only, all 4 colors reduced, to some extent, the number of illusions and 2 decreased the discomfort, particularly for the 12 cpd gratings. There were significant group differences for contrast sensitivity, reported visual migraine/headache triggers, and the visual discomfort scale. There were a few significant correlations between the different measures, notably between the achromatic visual discomfort measures and reports of visual migraine triggers. Color, independent of luminance or particular color contrasts, can have therapeutic effects for people with visually triggered migraine as it can reduce the number of perceived illusions when viewing stripes or text. The effect was not color-specific and was greatest for the 12 cpd gratings. Given the significant associations between the achromatic discomfort measures and reports of visual triggers, and the lack of significant associations between the chromatic discomfort measures and reports of visual triggers, further research is recommended to explore the potential to reduce the number of visually triggered migraines with color in addition to alleviating visual discomfort.

Distinct Functional Organizations for Processing Different Motion Signals in V1, V2, and V4 of Macaque

Motion perception is qualitatively invariant across different objects and forms, namely, the same motion information can be conveyed by many different physical carriers, and it requires the processing of motion signals consisting of direction, speed, and axis or trajectory of motion defined by a moving object. Compared with the representation of orientation, the cortical processing of these different motion signals within the early ventral visual pathway of the primate remains poorly understood. Using drifting full-field noise stimuli and intrinsic optical imaging, along with cytochrome-oxidase staining, we found that the orientation domains in macaque V1, V2, and V4 that processed orientation signals also served to process motion signals associated with the axis and speed of motion. In contrast, direction domains within the thick stripes of V2 demonstrated preferences that were independent of motion speed. The population responses encoding the orientation and motion axis could be precisely reproduced by a spatiotemporal energy model. Thus, our observation of orientation domains with dual functions in V1, V2, and V4 directly support the notion that the linear representation of the temporal series of retinotopic activations may serve as another motion processing strategy in primate ventral visual pathway, contributing directly to fine form and motion analysis. Our findings further reveal that different types of motion information are differentially processed in parallel and segregated compartments within primate early visual cortices, before these motion features are fully combined in high-tier visual areas.

A Retinal Source of Spatial Contrast Gain Control

Sensory cortex is able to encode a broad range of stimulus features despite a great variation in signal strength. In cat primary visual cortex (V1), for example, neurons are able to extract stimulus features like orientation or spatial configuration over a wide range of stimulus contrasts. The contrast-invariant spatial tuning found in V1 neuron responses has been modeled as a gain control mechanism, but at which stage of the visual pathway it emerges has remained unclear. Here we describe our findings that contrast-invariant spatial tuning occurs not only in the responses of lateral geniculate nucleus (LGN) relay cells but also in their afferent retinal input. Our evidence suggests that a similar contrast-invariant mechanism is found throughout the stages of the early visual pathway, and that the contrast-invariant spatial selectivity is evident in both retinal ganglion cell and LGN cell responses.