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The primary visual cortex contains a detailed map of retinal stimulus position (retinotopic map) and eye input (ocular dominance map) that results from the precise arrangement of thalamic afferents during cortical development. For reasons that remain unclear, the patterns of ocular dominance are very diverse across species and can take the shape of highly organized stripes, convoluted beads, or no pattern at all. Here, we use a new image-processing algorithm to measure ocular dominance patterns more accurately than in the past. We use these measurements to demonstrate that ocular dominance maps follow a common organizing principle that makes the cortical axis with the slowest retinotopic gradient orthogonal to the ocular dominance stripes. We demonstrate this relation in multiple regions of the primary visual cortex from individual animals, and different species. Moreover, consistent with the increase in the retinotopic gradient with visual eccentricity, we demonstrate a strong correlation between eccentricity and ocular dominance stripe width. We also show that an eye/polarity grid emerges within the visual cortical map when the representation of light and dark stimuli segregates along an axis orthogonal to the ocular dominance stripes, as recently demonstrated in cats. Based on these results, we propose a developmental model of visual cortical topography that sorts thalamic afferents by eye input and stimulus polarity, and then maximizes the binocular retinotopic match needed for depth perception and the light-dark retinotopic mismatch needed to process stimulus orientation. In this model, the different ocular dominance patterns simply emerge from differences in local retinotopic cortical topography.SIGNIFICANCE STATEMENTThalamocortical afferents segregate in primary visual cortex by eye input and light-dark polarity. This afferent segregation forms cortical patterns that vary greatly across species for reasons that remain unknown. Here we show that the formation of ocular dominance patterns follows a common organizing principle across species that aligns the cortical axis of ocular dominance segregation with the axis of slowest retinotopic gradient. Based on our results, we propose a model of visual cortical topography that sorts thalamic afferents by eye input and stimulus polarity along orthogonal axes with the slowest and fastest retinotopic gradients, respectively. This organization maximizes the binocular retinotopic match needed for depth perception and the light-dark retinotopic mismatch needed to process stimulus orientation in carnivores and primates.

Visual information reaches the cerebral cortex through parallel ON and OFF pathways that signal the presence of light and dark stimuli in visual scenes. We have previously demonstrated that optical blur reduces visual salience more for light than dark stimuli because it removes the high spatial frequencies from the stimulus, and low spatial frequencies drive weaker ON than OFF cortical responses. Therefore, we hypothesized that sustained optical blur during brain development should weaken ON cortical pathways more than OFF, increasing the dominance of darks in visual perception. Here we provide support for this hypothesis in humans with anisometropic amblyopia who suffered sustained optical blur early after birth in one of the eyes. In addition, we show that the dark dominance in visual perception also increases in strabismic amblyopes that have their vision to high spatial frequencies reduced by mechanisms not associated with optical blur. Together, we show that amblyopia increases visual dark dominance by 3–10 times and that the increase in dark dominance is strongly correlated with amblyopia severity. These results can be replicated with a computational model that uses greater luminance/response saturation in ON than OFF pathways and, as a consequence, reduces more ON than OFF cortical responses to stimuli with low spatial frequencies. We conclude that amblyopia affects the ON cortical pathway more than the OFF, a finding that could have implications for future amblyopia treatments. SIGNIFICANCE STATEMENT Amblyopia is a loss of vision that affects 2–5% of children across the world and originates from a deficit in visual cortical circuitry. Current models assume that amblyopia affects similarly ON and OFF visual pathways, which signal light and dark features in visual scenes. Against this current belief, here we demonstrate that amblyopia affects the ON visual pathway more than the OFF, a finding that could have implications for new amblyopia treatments targeted at strengthening a weak ON visual pathway.

Accurate measures of contrast sensitivity are important for evaluating visual disease progression and for navigation safety. Previous measures suggested that cortical contrast sensitivity was constant across widely different luminance ranges experienced indoors and outdoors. Against this notion, here, we show that luminance range changes contrast sensitivity in both cat and human cortex, and the changes are different for dark and light stimuli. As luminance range increases, contrast sensitivity increases more within cortical pathways signaling lights than those signaling darks. Conversely, when the luminance range is constant, light-dark differences in contrast sensitivity remain relatively constant even if background luminance changes. We show that a Naka-Rushton function modified to include luminance range and light-dark polarity accurately replicates both the statistics of light-dark features in natural scenes and the cortical responses to multiple combinations of contrast and luminance. We conclude that differences in light-dark contrast increase with luminance range and are largest in bright environments.

The primary visual cortex of carnivores and primates is dominated by the OFF visual pathway and responds more strongly to dark than light stimuli. Here, we demonstrate that this cortical OFF dominance is modulated by the size and spatial frequency of the stimulus in awake primates and we uncover a main neuronal mechanism underlying this modulation. We show that large grating patterns with low spatial frequencies drive five times more OFF-dominated than ON-dominated neurons, but this pronounced cortical OFF dominance is strongly reduced when the grating size decreases and the spatial frequency increases, as when the stimulus moves away from the observer. We demonstrate that the reduction in cortical OFF dominance is not caused by a selective reduction of visual responses in OFF-dominated neurons but by a change in the ON/OFF response balance of neurons with diverse receptive field properties that can be ON or OFF dominated, simple, or complex. We conclude that cortical OFF dominance is continuously adjusted by a neuronal mechanism that modulates ON/OFF response balance in multiple cortical neurons when the spatial properties of the visual stimulus change with viewing distance and/or optical blur.

Summary: Visual information is processed in the cortex by ON and OFF pathways that respond to light and dark stimuli. Responses to darks are stronger, faster, and driven by a larger number of cortical neurons than responses to lights. Here, we demonstrate that these light-dark cortical asymmetries reflect a functional specialization of ON and OFF pathways for different stimulus properties. We show that large long-lasting stimuli drive stronger cortical responses when they are light, whereas small fast stimuli drive stronger cortical responses when they are dark. Moreover, we show that these light-dark asymmetries are preserved under a wide variety of luminance conditions that range from photopic to low mesopic light. Our results suggest that ON and OFF pathways extract different spatiotemporal information from visual scenes, making OFF local-fast signals better suited to maximize visual acuity and ON global-slow signals better suited to guide the eye movements needed for retinal image stabilization. : Mazade et al. find pronounced differences in the stimulus preferences of cortical pathways signaling lights (ON) and darks (OFF) in visual scenes. ON-preferred stimuli are large and steady, while OFF are small and brief. These results suggest an ON/OFF pathway specialization in global-slow and local-fast vision. Keywords: visual cortex, area V1, receptive field, thalamus, retina, LGN, thalamocortical, luminance, adaptation, image stabilization

Images are processed in the primary visual cortex by neurons that encode different stimulus orientations and spatial phases. In primates and carnivores, neighboring cortical neurons share similar orientation preferences, but spatial phases were thought to be randomly distributed. We discovered a columnar organization for spatial phase in cats that shares similarities with the columnar organization for orientation. For both orientation and phase, the mean difference across vertically aligned neurons was less than one-fourth of a cycle. Cortical neurons showed threefold more diversity in phase than orientation preference; however, the average phase of local neuronal populations was similar through the depth of layer 4. We conclude that columnar organization for visual space is not only defined by the spatial location of the stimulus, but also by absolute phase. Taken together with previous findings, our results suggest that this phase-visuotopy is responsible for the emergence of orientation maps.

Stimulus orientation in the primary visual cortex of primates and carnivores is mapped as iso-orientation domains radiating from pinwheel centres, where orientation preferences of neighbouring cells change circularly. Whether this orientation map has a function is currently debated, because many mammals, such as rodents, do not have such maps. Here we show that two fundamental properties of visual cortical responses, contrast saturation and cross-orientation suppression, are stronger within cat iso-orientation domains than at pinwheel centres. These differences develop when excitation (not normalization) from neighbouring oriented neurons is applied to different cortical orientation domains and then balanced by inhibition from un-oriented neurons. The functions of the pinwheel mosaic emerge from these local intra-cortical computations: Narrower tuning, greater cross-orientation suppression and higher contrast gain of iso-orientation cells facilitate extraction of object contours from images, whereas broader tuning, greater linearity and less suppression of pinwheel cells generate selectivity for surface patterns and textures., Stimulus orientation in the primary visual cortex of primates and carnivores is mapped into a geometrical mosaic but the functional implications of these maps remain debated. Here the authors reveal an association between the structure of cortical orientation maps in cats, and the functions of local cortical circuits in processing patterns and contours.

Visual neurons can respond with extremely precise temporal patterning to visual stimuli that change on much slower time scales. Here, we investigate how the precise timing of cat thalamic spike trains—which can have timing as precise as 1 ms—is related to the stimulus, in the context of both artificial noise and natural visual stimuli. Using a nonlinear modeling framework applied to extracellular data, we demonstrate that the precise timing of thalamic spike trains can be explained by the interplay between an excitatory input and a delayed suppressive input that resembles inhibition, such that neuronal responses only occur in brief windows where excitation exceeds suppression. The resulting description of thalamic computation resembles earlier models of contrast adaptation, suggesting a more general role for mechanisms of contrast adaptation in visual processing. Thus, we describe a more complex computation underlying thalamic responses to artificial and natural stimuli that has implications for understanding how visual information is represented in the early stages of visual processing.

The primary visual cortex of primates and carnivores is organized into columns of neurons with similar preferences for stimulus orientation, but the developmental origin and function of this organization are still matters of debate. We found that the orientation preference of a cortical column is closely related to the population receptive field of its ON and OFF thalamic inputs. The receptive field scatter from the thalamic inputs was more limited than previously thought and matched the average receptive field size of neurons at the input layers of cortex. Moreover, the thalamic population receptive field (calculated as ON - OFF average) had separate ON and OFF subregions, similar to cortical neurons in layer 4, and provided an accurate prediction of the preferred orientation of the column. These results support developmental models of orientation maps that are based on the receptive field arrangement of ON and OFF visual inputs to cortex.

Artists and astronomers noticed centuries ago that humans perceive dark features in an image differently from light ones; however, the neuronal mechanisms underlying these dark/light asymmetries remained unknown. Based on computational modeling of neuronal responses, we have previously proposed that such perceptual dark/light asymmetries originate from a luminance/response saturation within the ON retinal pathway. Consistent with this prediction, here we show that stimulus conditions that increase ON luminance/response saturation (e.g., dark backgrounds) or its effect on light stimuli (e.g., optical blur) impair the perceptual discrimination and salience of light targets more than dark targets in human vision. We also show that, in cat visual cortex, the magnitude of the ON luminance/response saturation remains relatively constant under a wide range of luminance conditions that are common indoors, and only shifts away from the lowest luminance contrasts under low mesopic light. Finally, we show that the ON luminance/response saturation affects visual salience mostly when the high spatial frequencies of the image are reduced by poor illumination or optical blur. Because both low luminance and optical blur are risk factors in myopia, our results suggest a possible neuronal mechanism linking myopia progression with the function of the ON visual pathway.

On- and off-center geniculate afferents form two major channels of visual processing that are thought to converge in the primary visual cortex. However, humans with severely reduced on responses can have normal visual acuity when tested in a white background, which indicates that off channels can function relatively independently from on channels under certain conditions. Consistent with this functional independence of channels, we demonstrate here that on- and off-center geniculate afferents segregate in different domains of the cat primary visual cortex and that off responses dominate the cortical representation of the area centralis. On average, 70% of the geniculate afferents converging at the same cortical domain had receptive fields of the same contrast polarity. Moreover, off-center afferents dominated the representation of the area centralis in the cortex, but not in the thalamus, indicating that on- and off-center afferents are balanced in number, but not in the amount of cortical territory that they cover.

The primary visual cortex contains a detailed map of the visual scene, which is represented according to multiple stimulus dimensions including spatial location, ocular dominance and stimulus orientation. The maps for spatial location and ocular dominance arise from the spatial arrangement of thalamic afferent axons in the cortex. However, the origins of the other maps remain unclear. Here we show that the cortical maps for orientation, direction and retinal disparity in the cat (Felis catus) are all strongly related to the organization of the map for spatial location of light (ON) and dark (OFF) stimuli, an organization that we show is OFF-dominated, OFF-centric and runs orthogonal to ocular dominance columns. Because this ON-OFF organization originates from the clustering of ON and OFF thalamic afferents in the visual cortex, we conclude that all main features of visual cortical topography, including orientation, direction and retinal disparity, follow a common organizing principle that arranges thalamic axons with similar retinotopy and ON-OFF polarity in neighbouring cortical regions.

Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ON-center neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes.

In a wide range of studies, the emergence of orientation selectivity in primary visual cortex has been attributed to a complex interaction between feed-forward thalamic input and inhibitory mechanisms at the level of cortex. Although it is well known that layer 4 cortical neurons are highly sensitive to the timing of thalamic inputs, the role of the stimulus-driven timing of thalamic inputs in cortical orientation selectivity is not well understood. Here we show that the synchronization of thalamic firing contributes directly to the orientation tuned responses of primary visual cortex in a way that optimizes the stimulus information per cortical spike. From the recorded responses of geniculate X-cells in the anesthetized cat, we synthesized thalamic sub-populations that would likely serve as the synaptic input to a common layer 4 cortical neuron based on anatomical constraints. We used this synchronized input as the driving input to an integrate-and-fire model of cortical responses and demonstrated that the tuning properties match closely to those measured in primary visual cortex. By modulating the overall level of synchronization at the preferred orientation, we show that efficiency of information transmission in the cortex is maximized for levels of synchronization which match those reported in thalamic recordings in response to naturalistic stimuli, a property which is relatively invariant to the orientation tuning width. These findings indicate evidence for a more prominent role of the feed-forward thalamic input in cortical feature selectivity based on thalamic synchronization., Author Summary While the visual system is selective for a wide range of different inputs, orientation selectivity has been considered the preeminent property of the mammalian visual cortex. Existing models of this selectivity rely on varying relative importance of feedforward thalamic input and intracortical influence. Recently, we have shown that pairwise timing relationships between single thalamic neurons can be predictive of a high degree of orientation selectivity. Here we have constructed a computational model that predicts cortical orientation tuning from thalamic populations. We show that this arrangement, relying on precise timing differences between thalamic responses, accurately predicts tuning properties as well as demonstrates that certain timing relationships are optimal for transmitting information about the stimulus to cortex.

ON and OFF visual pathways originate in the retina at the synapse between photoreceptor and bipolar cells. OFF bipolar cells are shorter in length and use receptors with faster kinetics than ON bipolar cells and, therefore, process information faster. Here, we demonstrate that this temporal advantage is maintained through thalamocortical processing, with OFF visual responses reaching cortex ∼3–6 ms before ON visual responses. Faster OFF visual responses could be demonstrated in recordings from large populations of cat thalamic neurons representing the center of vision (both X and Y) and from subpopulations making connection with the same cortical orientation column. While the OFF temporal advantage diminished as visual responses reached their peak, the integral of the impulse response was greater in OFF than ON neurons. Given the stimulus preferences from OFF and ON channels, our results indicate that darks are processed faster than lights in the thalamocortical pathway.

The temporal properties of pattern adaptation of relay cells induced by repeated sinusoidal drifting grating were investigated in the dorsal lateral geniculate nucleus (dLGN) of cats. The results showed that the response amplitude declined and the response latency prolonged when relay cells were pattern-adapted in dLGN, like the similar findings in visual cortex. However, in contrast to the result in cortex, the response phase of relay cells advanced. This implies that an inhibition with relatively long latency may participate in the pattern adaptation of dLGN cells and the adaptation in dLGN may be via a mechanism different from that of visual cortex.

The timing of spiking activity across neurons is a fundamental aspect of the neural population code. Individual neurons in the retina, thalamus, and cortex can have very precise and repeatable responses but exhibit degraded temporal precision in response to suboptimal stimuli. To investigate the functional implications for neural populations in natural conditions, we recorded in vivo the simultaneous responses, to movies of natural scenes, of multiple thalamic neurons likely converging to a common neuronal target in primary visual cortex. We show that the response of individual neurons is less precise at lower contrast, but that spike timing precision across neurons is relatively insensitive to global changes in visual contrast. Overall, spike timing precision within and across cells is on the order of 10 ms. Since closely timed spikes are more efficient in inducing a spike in downstream cortical neurons, and since fine temporal precision is necessary to represent the more slowly varying natural environment, we argue that preserving relative spike timing at a ∼10-ms resolution is a crucial property of the neural code entering cortex., Author Summary Neurons convey information about the world in the form of trains of action potentials (spikes). These trains are highly repeatable when the same stimulus is presented multiple times, and this temporal precision across repetitions can be as fine as a few milliseconds. It is usually assumed that this time scale also corresponds to the timing precision of several neighboring neurons firing in concert. However, the relative timing of spikes emitted by different neurons in a local population is not necessarily as fine as the temporal precision across repetitions within a single neuron. In the visual system of the brain, the level of contrast in the image entering the retina can affect single-neuron temporal precision, but the effects of contrast on the neural population code are unknown. Here we show that the temporal scale of the population code entering visual cortex is on the order of 10 ms and is largely insensitive to changes in visual contrast. Since closely timed spikes are more efficient in inducing a spike in downstream cortical neurons, and since fine temporal precision is necessary in representing the more slowly varying natural environment, preserving relative spike timing at a ∼10-ms resolution may be a crucial property of the neural code entering cortex., Early neural representation of visual scenes occurs with a temporal precision on the order of 10 ms, which is precise enough to strongly drive downstream neurons in the visual pathway. Unlike individual neurons, the neural population code is largely insensitive to pronounced changes in visual contrast.

Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli [1,2], but the neuronal mechanisms for this perceptual asymmetry remain undetermined. We investigated the neuronal mechanisms of this difference in spatial resolution by recording single ON- and OFF-center cells in the visual thalamus (LGN) and multi-unit activity in the visual cortex (V1) of cats. We found that receptive fields of ON-center cells were larger than receptive fields of OFF-center cells in LGN (Figure 1A, B top; ON/OFF = 1.27, p < 0.01) and V1 (ON/OFF = 1.29, p < 0.001), when mapped on binary backgrounds (light targets on dark backgrounds and dark targets on light backgrounds). Surprisingly, when receptive fields were mapped on gray backgrounds, these differences disappeared in the LGN (Figure 1 A, B bottom; ON/OFF = 0.97, p = 0.3) and were slightly reversed in V1 (ON/OFF = 0.8, p = 0.004). Thus, the difference in spatial resolution between ON and OFF neurons is not constant and changes dynamically with the background luminance, as is also the case for the difference in human spatial resolution for darks and lights. Figure 1 Functional asymmetries between ON and OFF channels. ON receptive fields are larger than OFF receptive fields (A, B; left) on dark but not gray backgrounds. Luminance response functions are more linear in ON (A; right) than OFF (B; right) channels in the ... We hypothesized that a nonlinear encoding of luminance increments and decrements could explain these differences. We found that OFF cells in LGN increase their responses roughly linearly (Figure ​(Figure1B,1B, right) with luminance decrements, independent of the background luminance (luminance half-saturation = L50; LGN OFF L50 light/gray = 0.99, p = 0.9; V1 OFF L50 light/gray = 1.03, p = 0.2). In marked contrast, ON-center cells saturate their responses with small increases in luminance (Figure ​(Figure1A,1A, top-left) and require bright backgrounds to approach the linearity of the OFF-center cells (Figure ​(Figure1A,1A, bottom-left; LGN ON L50 dark/gray = 0.28, p < 0.001; V1 ON L50 dark/gray = 0.3, p < 0.001). Although the integration of lights becomes more linear as the luminance of the background increases, ON responses still saturate more than OFF responses on gray backgrounds (V1 L50 darks/lights = 1.25, p < 0.001). Similar differences in response linearity could be demonstrated in recordings from local field potentials in awake primates. Consistent with our hypothesis, we show that a simple computational model based on the ON-channel nonlinearity can explain the larger receptive fields and lower spatial resolution of ON cells, the differences in human spatial resolution between darks than lights, the differences in the size of ON and OFF dendritic fields from retinal ganglion cells and the recently demonstrated OFF dominance in visual cortex (larger number of OFF- than ON-dominated cortical neurons). These results demonstrate a fundamental difference in processing between ON and OFF channels, which could have major implications in visual perception and cortical development.

SummaryIn this study, we characterize the adaptation of neurons in the cat lateral geniculate nucleus to changes in stimulus contrast and correlations. By comparing responses to high- and low-contrast natural scene movie and white noise stimuli, we show that an increase in contrast or correlations results in receptive fields with faster temporal dynamics and stronger antagonistic surrounds, as well as decreases in gain and selectivity. We also observe contrast- and correlation-induced changes in the reliability and sparseness of neural responses. We find that reliability is determined primarily by processing in the receptive field (the effective contrast of the stimulus), while sparseness is determined by the interactions between several functional properties. These results reveal a number of adaptive phenomena and suggest that adaptation to stimulus contrast and correlations may play an important role in visual coding in a dynamic natural environment.

SummaryVisual information is mediated by two major thalamic pathways that signal light decrements (OFF) and increments (ON) in visual scenes, the OFF pathway being faster than the ON. Here, we demonstrate that this OFF temporal advantage is transferred to visual cortex and has a correlate in human perception. OFF-dominated cortical neurons in cats responded ∼3 ms faster to visual stimuli than ON-dominated cortical neurons, and dark-mediated suppression in ON-dominated neurons peaked ∼14 ms faster than light-mediated suppression in OFF-dominated neurons. Consistent with the neuronal differences, human observers were 6–14 ms faster at detecting darks than lights and better at discriminating dark than light flickers. Neuronal and perceptual differences both vanished if backgrounds were biased toward darks. Our results suggest that the cortical OFF pathway is faster than the ON pathway at increasing and suppressing visual responses, and these differences have parallels in the human visual perception of lights and darks.