New Evidence for Retrospectively Cued Perception.

Past research suggests a continuity between perception and memory, as reflected in influences of orienting of spatial attention by cues presented after a visual target offset (post-target cues) on target perception. Conducting two experiments, we tested and confirmed this claim. Our study revealed an elevated reliance on post-target cues for target detection with diminishing target visibility, leading to better performance in validly versus invalidly cued trials, indicative of contrast gain. We demonstrated this post-target cueing impact on target perception without a postcue response prompt, meaning that our results truly reflected a continuity between perception and memory rather than a task-specific impact of having to memorize the target due to a response prompt. While previous studies found an improvement in accuracy through valid compared to invalid cues using liminal targets, in Experiment 1, we further showed an influence of attention on participants' response time by the post-target cues with cues presented away from a clearly visible target. This suggests that visual interactions at the target location provided no better explanation of post-target cueing effects. Our results generalize prior research with liminal targets and confirm the view of a perception-memory continuum so that visual target processing is not shielded against visuospatial orienting of attention elicited by events following the offset of the visual target.

Cortical Zinc Signaling Is Necessary for Changes in Mouse Pupil Diameter That Are Evoked by Background Sounds with Different Contrasts.

Luminance-independent changes in pupil diameter (PD) during wakefulness influence and are influenced by neuromodulatory, neuronal, and behavioral responses. However, it is unclear whether changes in neuromodulatory activity in a specific brain area are necessary for the associated changes in PD or whether some different mechanisms cause parallel fluctuations in both PD and neuromodulation. To answer this question, we simultaneously recorded PD and cortical neuronal activity in male and female mice. Namely, we measured PD and neuronal activity during adaptation to sound contrast, which is a well-described adaptation conserved in many species and brain areas. In the primary auditory cortex (A1), increases in the variability of sound level (contrast) induce a decrease in the slope of the neuronal input-output relationship, neuronal gain, which depends on cortical neuromodulatory zinc signaling. We found a previously unknown modulation of PD by changes in background sensory context: high stimulus contrast sounds evoke larger increases in evoked PD compared with low-contrast sounds. To explore whether these changes in evoked PD are controlled by cortical neuromodulatory zinc signaling, we imaged single-cell neural activity in A1, manipulated zinc signaling in the cortex, and assessed PD in the same awake mouse. We found that cortical synaptic zinc signaling is necessary for increases in PD during high-contrast background sounds compared with low-contrast sounds. This finding advances our knowledge about how cortical neuromodulatory activity affects PD changes and thus advances our understanding of the brain states, circuits, and neuromodulatory mechanisms that can be inferred from pupil size fluctuations.

Binocular properties of contrast adaptation in human vision.

Adaptation to contrast has been known and studied for 50 years, and the functional importance of dynamic gain control mechanisms is widely recognized. Understanding of binocular combination and binocular fusion has also advanced in the last 20 years, but aside from interocular transfer (IOT), we still know little about binocular properties of contrast adaptation. Our observers adapted to a high contrast 3.6 c/deg grating, and we assessed contrast detection and discrimination across a wide range of test contrasts (plotted as threshold vs contrast [TvC] functions). For each combination of adapt/test eye(s), the adapted TvC data followed a 'dipper' curve similar to the unadapted data, but displaced obliquely to higher contrasts. Adaptation had effectively re-scaled all contrasts by a common factor Cs that varied with the combination of adapt and test eye(s). Cs was well described by a simple 2-parameter model that had separate monocular and binocular gain controls, sited before and after binocular summation respectively. When these two levels of adaptation were inserted into an existing model for contrast discrimination, the extended 2-stage model gave a good account of the TvC functions, their shape invariance with adaptation, and the contrast scaling factors. The underlying contrast-response function is of almost constant shape, and adaptation shifts it to higher contrasts by the factor log10(Cs) - a 'pure contrast gain control'. Evidence of partial IOT in cat V1 cells supports the 2-stage scheme, but is not consistent with a classic (single-stage) model.

Internal neural states influence the short-term effect of monocular deprivation in human adults.

The adult human visual system maintains the ability to be altered by sensory deprivation. What has not been considered is whether the internal neural states modulate visual sensitivity to short-term monocular deprivation. In this study we manipulated the internal neural state and reported changes in intrinsic neural oscillations with a patched eye open or closed. We investigated the influence of eye open/eye closure on the unpatched eye's contrast sensitivity and ocular dominance (OD) shifts induced by short-term monocular deprivation. The results demonstrate that internal neural states influence not only baseline contrast sensitivity but also the extent to which the adult visual system can undergo changes in ocular dominance.

Makeup applied to facial features increases perceived skin evenness.

Facial cosmetics have powerful effects on person perception, such as increasing perceived attractiveness and competence. One specific aspect of facial appearance affected by makeup is apparent skin evenness. Here, we tested the notion that makeup makes facial skin look more homogeneous in part because of changes made not to the skin, but to the facial features. In two studies, participants made ratings of perceived skin evenness. Ratings were made on two versions of the same faces. In one version, no makeup of any kind was worn, while in the other version, the faces had makeup applied only on the features (digitally in Study 1 and by a professional makeup artist in Study 2). Critically, no makeup was worn on the skin in either condition, such that the physical skin homogeneity was identical. Across both studies, skin was rated as appearing more even in the condition with makeup applied to the facial features. This indicates that cosmetics make facial skin appear more even partly due to products applied only to the facial features. These findings are consistent with recent work demonstrating that skin appearance is affected by contrast with adjacent surfaces, possibly via contrast gain control.

Visual contrast perception in visual snow syndrome reveals abnormal neural gain but not neural noise.

Visual snow syndrome is a neurological condition characterized by a persistent visual disturbance, visual snow, in conjunction with additional visual symptoms. Cortical hyperexcitability is a potential pathophysiological mechanism, which could be explained by increased gain in neural responses to visual input. Alternatively, neural noise in the visual pathway could be abnormally elevated. We assessed these two potential competing neural mechanisms in our studies of visual contrast perception. Cortical hyperexcitation also occurs in migraine, which commonly co-occurs with visual snow syndrome. Therefore, to determine whether the effect of visual snow syndrome can be distinguished from interictal migraine, we recruited four participant groups: controls, migraine alone, visual snow syndrome alone and visual snow syndrome with migraine. In the first experiment, we estimated internal noise in 20 controls, 21 migraine participants and 32 visual snow syndrome participants (16 with migraine) using a luminance increment detection task. In the second experiment, we estimated neural contrast gain in 21 controls, 22 migraine participants and 35 visual snow syndrome participants (16 with migraine) using tasks assessing sensitivity to changes in contrast from a reference. Contrast gain and sensitivity were measured for the putative parvocellular and 'on' and 'off' magnocellular pathways, respectively. We found that luminance increment thresholds and internal noise estimates were normal in both visual snow syndrome and migraine. Contrast gain measures for putative parvocellular processing and contrast sensitivity for putative off magnocellular processing were abnormally increased in visual snow syndrome, regardless of migraine status. Therefore, our results indicate that visual snow syndrome is characterized by increased neural contrast gain but not abnormal neural noise within the targeted pathways.

Contrast adaptation and interocular transfer in cortical cells: A re-analysis & a two-stage gain-control model of binocular combination.

How do V1 cells respond to, adapt to, and combine signals from the two eyes? We tested a simple functional model that has monocular and binocular stages of divisive contrast gain control (CGC) that sit before, and after, binocular summation respectively. Interocular suppression (IOS) was another potential influence on contrast gain. Howarth, Vorobyov & Sengpiel (2009, Cerebral Cortex, 19, 1835-1843) studied contrast adaptation and interocular transfer in cat V1 cells. In our re-analysis we found that ocular dominance (OD) and contrast adaptation at a fixed test contrast were well described by a re-scaling of the unadapted orientation tuning curve - a simple change in response gain. We compared six variants of the basic model, and one model fitted the gain data notably better than the others did. When the dominant eye was tested, adaptation reduced cell response gain more when that eye was adapted than when the other eye was adapted. But when the non-dominant eye was tested, adapting either eye gave about the same reduction in overall gain, and there was an interaction between OD and adapting eye that was well described by the best-fitting model. Two key features of this model are that signals driving IOS arise 'early', before attenuation due to OD, while suppressive CGC signals are 'late' and so affected by OD. We show that late CGC confers a functional advantage: it yields partial compensation for OD, which should reduce ocular imbalance at the input to binocular summation, and improve the cell's sensitivity to variation in stereo disparity.

The ups and downs of sensory eye balance: Monocular deprivation has a biphasic effect on interocular dominance.

Classic studies of ocular dominance plasticity in early development showed that monocular deprivation suppresses the neural representation and visual function of the deprived eye. However, recent studies have shown that a short period of monocular deprivation (<3 h) in normal adult humans, shifts sensory eye dominance in favor of the deprived eye. How can these opposing effects be reconciled? Here we argue that there are two systems acting in opposition at different time scales. A fast acting, stabilizing, homeostatic system that rapidly decreases gain in the non-deprived eye or increases gain in the deprived eye, and a relatively sluggish system that shifts balance toward the non-deprived eye, in an effort to reduce input of little utility to active vision. If true, then continuous deprivation should produce a biphasic effect on interocular balance, first shifting balance away from the non-deprived eye, then towards it. Here we investigated the time course of the deprivation effect by monocularly depriving typical adults for 10 h and conducting tests of sensory eye balance at six intervening time points. Consistent with previous short-term deprivation work, we found shifts in sensory eye dominance away from the non-deprived eye up until approximately 5 h. We then observed a turning point, with balance shifting back towards the non-deprived eye, -, a biphasic effect. We argue that this turning point marks where the rapid homeostatic response saturates and is overtaken by the slower system responsible for suppressing monocular input of limited utility.

Persistent Firing and Adaptation in Optic-Flow-Sensitive Descending Neurons.

A general principle of sensory systems is that they adapt to prolonged stimulation by reducing their response over time. Indeed, in many visual systems, including higher-order motion sensitive neurons in the fly optic lobes and the mammalian visual cortex, a reduction in neural activity following prolonged stimulation occurs. In contrast to this phenomenon, the response of the motor system controlling flight maneuvers persists following the offset of visual motion. It has been suggested that this gap is caused by a lingering calcium signal in the output synapses of fly optic lobe neurons. However, whether this directly affects the responses of the post-synaptic descending neurons, leading to the observed behavioral output, is not known. We use extracellular electrophysiology to record from optic-flow-sensitive descending neurons in response to prolonged wide-field stimulation. We find that, as opposed to most sensory and visual neurons, and in particular to the motion vision sensitive neurons in the brains of both flies and mammals, the descending neurons show little adaption during stimulus motion. In addition, we find that the optic-flow-sensitive descending neurons display persistent firing, or an after-effect, following the cessation of visual stimulation, consistent with the lingering calcium signal hypothesis. However, if the difference in after-effect is compensated for, subsequent presentation of stimuli in a test-adapt-test paradigm reveals adaptation to visual motion. Our results thus show a combination of adaptation and persistent firing in the neurons that project to the thoracic ganglia and thereby control behavioral output.

Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex.

Contrast gain control is the systematic adjustment of neuronal gain in response to the contrast of sensory input. It is widely observed in sensory cortical areas and has been proposed to be a canonical neuronal computation. Here, we investigated whether shunting inhibition from parvalbumin-positive interneurons-a mechanism involved in gain control in visual cortex-also underlies contrast gain control in auditory cortex. First, we performed extracellular recordings in the auditory cortex of anesthetized male mice and optogenetically manipulated the activity of parvalbumin-positive interneurons while varying the contrast of the sensory input. We found that both activation and suppression of parvalbumin interneuron activity altered the overall gain of cortical neurons. However, despite these changes in overall gain, we found that manipulating parvalbumin interneuron activity did not alter the strength of contrast gain control in auditory cortex. Furthermore, parvalbumin-positive interneurons did not show increases in activity in response to high-contrast stimulation, which would be expected if they drive contrast gain control. Finally, we performed in vivo whole-cell recordings in auditory cortical neurons during high- and low-contrast stimulation and found that no increase in membrane conductance was observed during high-contrast stimulation. Taken together, these findings indicate that while parvalbumin-positive interneuron activity modulates the overall gain of auditory cortical responses, other mechanisms are primarily responsible for contrast gain control in this cortical area.NEW & NOTEWORTHY We investigated whether contrast gain control is mediated by shunting inhibition from parvalbumin-positive interneurons in auditory cortex. We performed extracellular and intracellular recordings in mouse auditory cortex while presenting sensory stimuli with varying contrasts and manipulated parvalbumin-positive interneuron activity using optogenetics. We show that while parvalbumin-positive interneuron activity modulates the gain of cortical responses, this activity is not the primary mechanism for contrast gain control in auditory cortex.

Sparse identification of contrast gain control in the fruit fly photoreceptor and amacrine cell layer.

The fruit fly's natural visual environment is often characterized by light intensities ranging across several orders of magnitude and by rapidly varying contrast across space and time. Fruit fly photoreceptors robustly transduce and, in conjunction with amacrine cells, process visual scenes and provide the resulting signal to downstream targets. Here, we model the first step of visual processing in the photoreceptor-amacrine cell layer. We propose a novel divisive normalization processor (DNP) for modeling the computation taking place in the photoreceptor-amacrine cell layer. The DNP explicitly models the photoreceptor feedforward and temporal feedback processing paths and the spatio-temporal feedback path of the amacrine cells. We then formally characterize the contrast gain control of the DNP and provide sparse identification algorithms that can efficiently identify each the feedforward and feedback DNP components. The algorithms presented here are the first demonstration of tractable and robust identification of the components of a divisive normalization processor. The sparse identification algorithms can be readily employed in experimental settings, and their effectiveness is demonstrated with several examples.

Multi-Stage Cortical Plasticity Induced by Visual Contrast Learning.

Perceptual learning, the improved sensitivity via repetitive practice, is a universal phenomenon in vision and its neural mechanisms remain controversial. A central question is which stage of processing is changed after training. To answer this question, we measured the contrast response functions and electroencephalography (EEG) before and after ten daily sessions of contrast detection training. Behavioral results showed that training substantially improved visual acuity and contrast sensitivity. The learning effect was significant at the trained condition and partially transferred to control conditions. Event-related potential (ERP) results showed that training reduced the latency in both early and late ERPs at the trained condition. Specifically, contrast-gain-related changes were observed in the latency of P1, N1-P2 complex, and N2, which reflects neural changes across the early, middle, and high-level sensory stages. Meanwhile, response-gain-related changes were found in the latency of N2, which indicates stimulus-independent effect in higher-level stages. In sum, our findings indicate that learning leads to changes across different processing stages and the extent of learning and transfer may depend on the specific stage of information processing.

Corrigendum: The Binocular Balance at High Spatial Frequencies as Revealed by the Binocular Orientation Combination Task.

[This corrects the article DOI: 10.3389/fnhum.2019.00106.].

The Binocular Balance at High Spatial Frequencies as Revealed by the Binocular Orientation Combination Task.

How to precisely quantify the binocular eye balance (i.e., the contribution that each eye makes to the binocular percept) across a range of spatial frequencies using a binocular combination task, is an important issue in both clinical and basic research. In this study, we aimed to compare the precision of a binocular orientation combination paradigm with that of the standard binocular phase combination paradigm in measuring the binocular eye balance at low to high spatial frequencies. Nine normal adults (average age: 24.6 ± 2.0 years old) participated. Subjects viewed an LED screen dichoptically with polarized glasses in a dark room. The method of constant stimuli was used to quantitatively assess the point of subjective equality (PSE), i.e., the interocular contrast ratio when two eyes are balanced in binocular combination, for stimulus spatial frequencies from 0.5 to 8 cycles/degree. Precision was quantified by the variance [i.e., standard error (SE), obtained from 100 bootstrap estimates] associated to the PSE. Using stimuli whose interocular phase difference at the edge of the gratings was matched at 45°, we found that the orientation paradigm provides more precision than the standard binocular phase combination paradigm, especially at high frequencies (Experiment 1). Such differences remained when using stimuli that had three times larger interocular phase difference (Experiment 2) or displayed at four times higher stimuli resolution (Experiment 3). Our results indicate that a binocular combination tasked based on orientation rather than phase, provides a more precise estimate of binocular eye balance in human adults at high spatial frequencies, thus allowing a binocular balance to be assessed within the spatial region where amblyopes are most defective (i.e., high spatial frequencies).

Nonlinear Lateral Interactions in V1 Population Responses Explained by a Contrast Gain Control Model.

How do cortical responses to local image elements combine to form a spatial pattern of population activity in primate V1? Here, we used voltage-sensitive dye imaging, which measures summed membrane potential activity, to examine the rules that govern lateral interactions between the representations of two small local-oriented elements in macaque (Macaca mulatta) V1. We find strong subadditive and mostly orientation-independent interactions for nearby elements [2-4 mm interelement cortical distance (IED)] that gradually become linear at larger separations (>6 mm IED). These results are consistent with a population gain control model describing nonlinear V1 population responses to single oriented elements. However, because of the membrane potential-to-spiking accelerating nonlinearity, the model predicts supra-additive lateral interactions of spiking responses for intermediate separations at a range of locations between the two elements, consistent with some prior facilitatory effects observed in electrophysiology and psychophysics. Overall, our results suggest that population-level lateral interactions in V1 are primarily explained by a simple orientation-independent contrast gain control mechanism.SIGNIFICANCE STATEMENT Interactions between representations of simple visual elements such as oriented edges in primary visual cortex (V1) are thought to contribute to our ability to easily integrate contours and segment surfaces, but the mechanisms that govern these interactions are primarily unknown. Our study provides novel evidence that lateral interactions at the population level are governed by a simple contrast gain-control mechanism, and we show how this divisive gain-control mechanism can give rise to apparently facilitatory spiking responses.

Binocular contrast-gain control for natural scenes: Image structure and phase alignment.

In the context of natural scenes, we applied the pattern-masking paradigm to investigate how image structure and phase alignment affect contrast-gain control in binocular vision. We measured the discrimination thresholds of bandpass-filtered natural-scene images (targets) under various types of pedestals. Our first experiment had four pedestal types: bandpass-filtered pedestals, unfiltered pedestals, notch-filtered pedestals (which enabled removal of the spatial frequency), and misaligned pedestals (which involved rotation of unfiltered pedestals). Our second experiment featured six types of pedestals: bandpass-filtered, unfiltered, and notch-filtered pedestals, and the corresponding phase-scrambled pedestals. The thresholds were compared for monocular, binocular, and dichoptic viewing configurations. The bandpass-filtered pedestal and unfiltered pedestals showed classic dipper shapes; the dipper shapes of the notch-filtered, misaligned, and phase-scrambled pedestals were weak. We adopted a two-stage binocular contrast-gain control model to describe our results. We deduced that the phase-alignment information influenced the contrast-gain control mechanism before the binocular summation stage and that the phase-alignment information and structural misalignment information caused relatively strong divisive inhibition in the monocular and interocular suppression stages. When the pedestals were phase-scrambled, the elimination of the interocular suppression processing was the most convincing explanation of the results. Thus, our results indicated that both phase-alignment information and similar image structures cause strong interocular suppression.

The contribution of forward masking to saccadic inhibition of return.

Inhibition of return is the name typically given to the prolonged latency of motor responses directed to a previously cued target location. There is intense debate about the origins of this effect and its function, but most take for granted (despite lack of evidence) that it depends little on forward masking. Therefore, we re-examined the role of forward masking in inhibition of return. Forward masking was indexed by slower saccadic reaction times (SRTs) when the target orientation repeated the cue orientation at the same location. We confirmed effects of orientation repetition in the absence of an attentional bias when cues were presented on both sides of fixation (bilateral presentation). The effect of orientation repetition was reduced with high target contrast, consistent with a low-level origin such as contrast gain control in early visual areas. When presenting cues on only one side of fixation (unilateral presentation), we obtained inhibition of return with longer cue-target intervals and facilitation with targets presented shortly after the cue. The effect of orientation repetition was reduced when facilitation was observed, but was as strong as with bilateral cues when inhibition of return was observed. Therefore, forward masking may contribute to the inhibition of return effect by delaying reaction times to repeated features at the same location, but is not a principal cause of inhibition of return; in agreement with previous views. SIGNIFICANCE STATEMENT: The saccadic inhibition of return effect is a reaction-time cost when responding to a pre-cued location. Additional object updating costs are typically invoked to explain reaction-time costs observed when cue and target have the same shape. Yet, lower-level, forward masking of the target by the cue can not be ruled out. Importantly, we show an effect of orientation repetition that is consistent with low-level forward masking rather than object updating costs and that does not interact with inhibition of return.

Asymmetric high-contrast masking in S cone increment and decrement pathways.

Physiological, anatomical, and psychophysical evidence points to important differences between visual processing of short-wave cone increments and decrement (S+ and S-) stimuli. The present study uses the pedestal discrimination paradigm to investigate potential differences, using S+ and S- tests presented on (L)ong-wave, (M)edium-wave, S, L+M, L-M, and achromatic pedestals, of both contrast polarities. Results show that high contrast 'purplish' (S+ or -(L+M)) pedestals produce substantially more masking of both S+ and S- tests than 'yellowish' (S- or +(L+M)) pedestals do. The other pedestals produce no masking. These findings suggest greater nonlinearity - either a static nonlinearity or contrast gain control - in the mechanisms responsible for the 'purplish' polarity, likely the S ON pathway.

The Cortical Mechanisms Underlying Ocular Dominance Plasticity in Adults are Not Orientationally Selective.

Recently, it has been shown that short-term monocular deprivation in adult humans can temporally shift the ocular dominance in favor of the deprived eye. It is not clear whether this form of ocular dominance plasticity can be explained by cortical contrast adaptation, which is known to be orientationally selective. Here we show that if only one eye is deprived of a limited band of orientations for a short period of 2.5 h, the deprived eye's contribution to binocular function at all orientations rather than just those corresponding to the previously deprived orientations is strengthened. This isotropic enhancement is quite different from the orientational enhancement previously reported and suggests a separate neuroplastic mechanism specific to binocular function.

Absolute Not Relative Interocular Luminance Modulates Sensory Eye Dominance Plasticity in Adults.

If one eye is patched for a period of 2.5 h in human adults, transient changes in sensory eye dominance result with the previously patched eye's contribution being strengthened. Similar changes result from opaque and translucent occlusion suggesting that it is the deprivation of contrast not luminance information that drives these transient shift of sensory eye dominance. However, this does not rule out the possibility that luminance deprivation per se cannot produce changes in sensory eye dominance, indeed based on what we know of the physiology, where the contrast gain of visual neurons is luminance dependent, one would expect it should. We show that if the mean luminance of one eye is reduced 1000-fold for a period of 2.5 h, there are subsequent changes in sensory eye dominance. With further control experiments we show that this deprivation effect critically depends on the absolute luminance of each eye rather than the relative interocular luminance imbalance. These results indicate that changes in contrast gain at an early, monocular stage of the pathway can result in the transient shift of sensory eye dominance.