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Primate visual cortex exhibits key organizational principles: cortical magnification, eccentricity-dependent receptive field size and spatial frequency tuning as well as radial bias. We provide compelling evidence that these principles arise from the interplay of the non-uniform distribution of retinal ganglion cells, and a quasi-uniform convergence rate from the retina to the cortex. We show that convolutional neural networks outfitted with a retinal sampling layer, which resamples images according to retinal ganglion cell density, develop these organizational principles. Surprisingly, our results indicate that radial bias is spatial-frequency dependent and only manifests for high spatial frequencies. For low spatial frequencies, the bias shifts towards orthogonal orientations. These findings introduce a novel hypothesis about the origin of radial bias. Quasi-uniform convergence limits the range of spatial frequencies (in retinal space) that can be resolved, while retinal sampling determines the spatial frequency content throughout the retina.

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The spatial-frequency (SF) tuning of neurons in the early visual cortex is adjusted for stimulus contrast. As the contrast increases, SF tuning is modulated so that the transmission of fine features is facilitated. A variety of mechanisms are involved in shaping SF tunings, but those responsible for the contrast-dependent modulations are unclear. To address this, we measured the time course of SF tunings of area 17 neurons in male cats under different contrasts with a reverse correlation. After response onset, the optimal SF continuously shifted to a higher SF over time, with a larger shift for higher contrast. At high contrast, whereas neurons with a large shift of optimal SF exhibited a large bandwidth decrease, those with a negligible shift increased the bandwidth over time. Between these two extremes, the degree of SF shift and bandwidth change continuously varied. At low contrast, bandwidth generally decreased over time. These dynamic effects enhanced the processing of high-frequency range under a high-contrast condition and allowed time-average SF tuning curves to show contrast-dependent modulation, like that of steady-state SF tuning curves reported previously. Combinations of two mechanisms, one that decreases bandwidth and shifts optimal SF, and another that increases bandwidth without shifting optimal SF, would explain the full range of SF tuning dynamics. Our results indicate that one of the essential roles of tuning dynamics of area 17 neurons, which have been observed for various visual features, is to adjust tunings depending on contrast.SIGNIFICANCE STATEMENT The spatial scales of features transmitted by cortical neurons are adjusted depending on stimulus contrast. However, the underlying mechanism is not fully understood. We measured the time course of spatial frequency tunings of cat area 17 neurons under different contrast conditions and observed a variety of dynamic effects that contributed to spatial-scale adjustment, allowing neurons to adjust their spatial frequency tuning range depending on contrast. Our results suggest that one of the essential roles of tuning dynamics of area 17 neurons, which have been observed for various visual features, is to adjust tunings depending on contrast.

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The visual system processes sensory inputs sequentially, perceiving coarse information before fine details. Here we study the neural basis of coarse-to-fine processing and its computational benefits in natural vision. We find that primary visual cortical neurons in awake mice respond to natural scenes in a coarse-to-fine manner, primarily driven by individual neurons rapidly shifting their spatial frequency preference from low to high over a brief response period. This shift transforms the population response in a way that counteracts the statistical regularities of natural scenes, thereby reducing redundancy and generating a more efficient neural representation. The increase in representational efficiency does not occur in either dark-reared or anesthetized mice, which show significantly attenuated coarse-to-fine spatial processing. Collectively, these results illustrate that coarse-to-fine processing is state dependent, develops postnatally via visual experience, and provides a computational advantage by generating more efficient representations of the complex spatial statistics of ethologically relevant natural scenes.

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Most neurons in the primary visual cortex (V1) of mammals show sharp orientation selectivity and band-pass spatial frequency tuning. Here, we examine whether sharpening of the broad tuning that exists subcortically, namely in the retina and the lateral geniculate nucleus (LGN), underlie the sharper tuning seen for both the above features in tree shrew V1. Since the transition from poor feature selectivity to sharp tuning occurs entirely within V1 in tree shrews, we examined the orientation selectivity and spatial frequency tuning of neurons within individual electrode penetrations. We found that most layer 4 and layer 2/3 neurons in the same cortical column preferred the same stimulus orientation. However, a subset of layer 3c neurons close to the layer 4 border preferred near orthogonal orientations, suggesting that layer 2/3 neurons may inherit the orientation preferences of their layer 4 input neurons and also receive cross-orientation inhibition from layer 3c neurons. We also found that layer 4 neurons showed sharper orientation selectivity at higher spatial frequencies, suggesting that attenuation of low spatial frequency responses by spatially broad inhibition acting on layer 4 inputs to layer 2/3 neurons can enhance both orientation and spatial frequency selectivities. However, in a proportion of layer 2/3 neurons, the sharper tuning of layer 2/3 neurons appeared to arise also or even mainly from inhibition specific to high spatial frequencies acting on the layer 4 inputs to layer 2/3. Overall, our results are consistent with the suggestion that in tree shrews, sharp feature selectivity in layer 2/3 can be established by intracortical mechanisms that sharpen biases observed in layer 4, which are in turn inherited presumably from thalamic afferents.

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"Left" and "right" coordinates control our spatial behavior and even influence abstract thoughts. For number concepts, horizontal spatial-numerical associations (SNAs) have been widely documented: we associate few with left and many with right. Importantly, increments are universally coded on the right side even in preverbal humans and nonhuman animals, thus questioning the fundamental role of directional cultural habits, such as reading or finger counting. Here, we propose a biological, nonnumerical mechanism for the origin of SNAs on the basis of asymmetric tuning of animal brains for different spatial frequencies (SFs). The resulting selective visual processing predicts both universal SNAs and their context-dependence. We support our proposal by analyzing the stimuli used to document SNAs in newborns for their SF content. As predicted, the SFs contained in visual patterns with few versus many elements preferentially engage right versus left brain hemispheres, respectively, thus predicting left-versus rightward behavioral biases. Our "brain's asymmetric frequency tuning" hypothesis explains the perceptual origin of horizontal SNAs for nonsymbolic visual numerosities and might be extensible to the auditory domain.

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Facial expressions of emotion play a key role in social interactions. While in everyday life, their dynamic and transient nature calls for a fast processing of the visual information they contain, a majority of studies investigating the visual processes underlying their recognition have focused on their static display. The present study aimed to gain a better understanding of these processes while using more ecological dynamic facial expressions. In two experiments, we directly compared the spatial frequency (SF) tuning during the recognition of static and dynamic facial expressions. Experiment 1 revealed a shift toward lower SFs for dynamic expressions in comparison to static ones. Experiment 2 was designed to verify if changes in SF tuning curves were specific to the presence of emotional information in motion by comparing the SF tuning profiles for static, dynamic, and shuffled dynamic expressions. Results showed a similar shift toward lower SFs for shuffled expressions, suggesting that the difference found between dynamic and static expressions might not be linked to informative motion per se but to the presence of motion regardless its nature.

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Higher and lower cortical areas in the visual hierarchy are reciprocally connected [1]. Although much is known about how feedforward pathways shape receptive field properties of visual neurons, relatively little is known about the role of feedback pathways in visual processing. Feedback pathways are thought to carry top-down signals, including information about context (e.g., figure-ground segmentation and surround suppression) [2-5], and feedback has been demonstrated to sharpen orientation tuning of neurons in the primary visual cortex (V1) [6, 7]. However, the response characteristics of feedback neurons themselves and how feedback shapes V1 neurons' tuning for other features, such as spatial frequency (SF), remain largely unknown. Here, using a retrograde virus, targeted electrophysiological recordings, and optogenetic manipulations, we show that putatively feedback neurons in layer 5 (hereafter "L5 feedback") in higher visual areas, AL (anterolateral area) and PM (posteromedial area), display distinct visual properties in awake head-fixed mice. AL L5 feedback neurons prefer significantly lower SF (mean: 0.04 cycles per degree [cpd]) compared to PM L5 feedback neurons (0.15 cpd). Importantly, silencing AL L5 feedback reduced visual responses of V1 neurons preferring low SF (mean change in firing rate: -8.0%), whereas silencing PM L5 feedback suppressed responses of high-SF-preferring V1 neurons (-20.4%). These findings suggest that feedback connections from higher visual areas convey distinctly tuned visual inputs to V1 that serve to boost V1 neurons' responses to SF. Such like-to-like functional organization may represent an important feature of feedback pathways in sensory systems and in the nervous system in general.

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The visual system demonstrates significant differences in information processing abilities between the central and peripheral parts of the visual field. Optical imaging based on intrinsic signals was used to investigate the difference in stimulus spatial and temporal frequency interactions related to receptive field eccentricity in the cat area 18. Changing either the spatial or the temporal frequency of grating stimuli had a significant impact on responses in the cortical areas corresponding to the centre of the visual field and more peripheral parts at 10 degrees eccentricity. The cortical region corresponding to the centre of the gaze was tuned to 0.4 cycles per degree (c/deg) for spatial frequency and 2 Hz for temporal frequency. In contrast, the cortical region corresponding to the periphery of the visual field was tuned to a lower spatial frequency of 0.15 c/deg and a higher temporal frequency of 4 Hz. Interestingly, when we simultaneously changed both the spatial frequency and the temporal frequency of the grating stimuli, the responses were significantly different from those estimated with an assumption of independence between the spatial and temporal frequency in the cortical region corresponding to the periphery of the visual field. However, in the cortical area corresponding to the centre of the gaze, spatial frequency showed significant independence from temporal frequency. These properties support the notion of relative specialization of visual information processing for peripheral representations in cortical areas.

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The detection of a Gabor patch (target) can be decreased or improved by the presence of co-oriented Gabor patches (flankers) having the same spatial frequency as the target. These phenomena are thought to be mediated by lateral interactions. Depending on the distance between target and flankers, commonly defined as a multiple of the wavelength (λ) of the carrier, flankers can increase or decrease a target's detectability. Studies with foveal presentation showed that for target-to-flankers distances<2λ contrast thresholds for the central target increase, while for target-to-flankers distances>3λ contrast thresholds decrease. Earlier studies on collinear facilitation at the near-periphery of the visual field (4° of eccentricity) showed inconsistent facilitation (Shani & Sagi, 2005, Vision Research, 45, 2009-2024) whereas more recent studies showed consistent facilitation for larger separations (7-8λ) (Maniglia et al., 2011, PLoS ONE, 6, e25568; Lev & Polat, 2011, Vision Research, 51, 2488-2498). However, all of these studies used medium-to-high spatial frequencies (3-8 cpd). In this study we tested lower spatial frequencies (1, 2, and 3 cpd) with different target-to-flankers distances. The rationale was that near-peripheral vision is tuned for lower spatial frequencies and this could be reflected in collinear facilitation. Results show consistent collinear facilitation at 8λ for all the spatial frequencies tested, but also show collinear facilitation at shorter target-to-flanker distance (6λ) for the lowest spatial frequencies tested (1 cpd). Additionally, collinear facilitation decreases as spatial frequency increases; opposite to the findings of Polat (2009, Spatial Vision, 22, 179-193) in the fovea, indicating a different spatial frequency tuning between foveal and peripheral lateral interactions.

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Several physiological studies in cats and monkeys have reported that the spatial frequency (SF) tuning of visual neurons varies depending on the luminance contrast and size of stimulus. However, comparatively little is known about the effect of changing the stimulus contrast and size on SF tuning in human perception. In the present study, we investigated the effects of stimulus size and luminance contrast on human SF tuning using the subspace-reverse-correlation method. Measuring SF tunings at six different stimulus sizes and three different luminance contrast conditions (90%, 10%, and 1%), we found that human perception exhibits significant stimulus-size-dependent SF tunings. At 90% and 10% contrast, participants exhibited relative SF tuning (cycles/image) rather than absolute SF tuning (cycles/°) at response peak latency. On the other hand, at 1% contrast, the magnitude of the size-dependent-peak SF shift was too small for strictly relative SF tuning. These results show that human SF tuning is not fixed, but varies depending on the stimulus size and contrast. This dependency may contribute to size-invariant object recognition within an appropriate contrast rage.

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