Alexandre Reynaud

The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave

Propagating waves occur in many excitable media and were recently found in neural systems from retina to neocortex. While propagating waves are clearly present under anaesthesia, whether they also appear during awake and conscious states remains unclear. One possibility is that these waves are systematically missed in trial-averaged data, due to variability. Here we present a method for detecting propagating waves in noisy multichannel recordings. Applying this method to single-trial voltage-sensitive dye imaging data, we show that the stimulus-evoked population response in primary visual cortex of the awake monkey propagates as a travelling wave, with consistent dynamics across trials. A network model suggests that this reliability is the hallmark of the horizontal fibre network of superficial cortical layers. Propagating waves with similar properties occur independently in secondary visual cortex, but maintain precise phase relations with the waves in primary visual cortex. These results show that, in response to a visual stimulus, propagating waves are systematically evoked in several visual areas, generating a consistent spatiotemporal frame for further neuronal interactions.

Dichoptic movie viewing treats childhood amblyopia

BACKGROUND Contrast-balanced dichoptic experience with perceptual-learning tasks or simple games has been shown to improve visual acuity significantly in amblyopia. However, these tasks are intensive and repetitive, and up to 40% of unsupervised patients are noncompliant. We investigated the efficacy of a potentially more engaging movie method to provide contrast-balanced binocular experience via complementary dichoptic stimulation. METHODS Eight amblyopic children 4-10 years of age were enrolled in a prospective cohort study to watch 3 dichoptic movies per week for 2 weeks on a passive 3D display. Dichoptic versions of 18 popular animated feature films were created. A patterned image mask of irregularly shaped blobs was multiplied with the movie images seen by the amblyopic eye and an inverse mask was multiplied with the images seen by the fellow eye. Fellow-eye contrast was initially set at a reduced level that allowed binocular vision and was then incremented by 10% at each visit. Best-corrected visual acuity, random dot stereoacuity, and interocular suppression were measured at baseline and 2 weeks. RESULTS Mean amblyopic eye visual acuity (with standard error of the mean) improved from a logarithm of minimum angle of resolution of 0.72 ± 0.08 at baseline to 0.52 ± 0.09 (P = 0.003); that is, 2.0 lines of improvement at the 2-week outcome visit. No significant change in interocular suppression or stereoacuity was found. CONCLUSIONS Passive viewing of dichoptic feature films is feasible and could be a promising new treatment for childhood amblyopia. The maximum improvement that may be achieved by watching dichoptic movies remains to be determined. No known side effects are associated with this new treatment.

Dynamics of local input normalization result from balanced short- and long-range intracortical interactions in area V1.

To efficiently drive many behaviors, sensory systems have to integrate the activity of large neuronal populations within a limited time window. These populations need to rapidly achieve a robust representation of the input image, probably through canonical computations such as divisive normalization. However, little is known about the dynamics of the corticocortical interactions implementing these rapid and robust computations. Here, we measured the real-time activity of a large neuronal population in V1 using voltage-sensitive dye imaging in behaving monkeys. We found that contrast gain of the population increases over time with a time constant of ∼30 ms and propagates laterally over the cortical surface. This dynamic is well accounted for by a divisive normalization achieved through a recurrent network that transiently increases in size after response onset with a slow swelling speed of 0.007–0.014 m/s, suggesting a polysynaptic intracortical origin. In the presence of a surround, this normalization pool is gradually balanced by lateral inputs propagating from distant cortical locations. This results in a centripetal propagation of surround suppression at a speed of 0.1–0.3 m/s, congruent with horizontal intracortical axons speed. We propose that a simple generalized normalization scheme can account for both the dynamical contrast response function through recurrent polysynaptic intracortical loops and for the surround suppression through long-range monosynaptic horizontal spread. Our results demonstrate that V1 achieves a rapid and robust context-dependent input normalization through a timely push–pull between local and lateral networks. We suggest that divisive normalization, a fundamental canonical computation, should be considered as a dynamic process.

Stereopsis and mean luminance

Stereopsis is dependent on the average level of illumination, especially if it differs between the two eyes. We manipulate the mean luminance seen by both eyes or the interocular difference in mean luminance by using neutral density (ND) filters placed in front of both eyes or just one eye respectively. Stereo acuity was measured using a one temporal interval forced choice task for detecting the sign of a Gaussian depth perturbation in a noise field with a comparable spectrum to that found in natural images. We show that the effect of changing mean luminance is spatial scale independent within the range of 0.5 to 4 cpd, certainly not larger at higher spatial scales. To investigate its origin we manipulate two factors, the temporal synchrony between the two eyes and the interocular contrast. Both factors are implicated in the loss of stereo performance when the mean luminance is different between the eyes, suggesting an underlying explanation in terms of temporal low-pass filtering resulting in the combination of a luminance-dependent temporal delay and a luminance-dependent change in contrast gain.

Linear model decomposition for voltage-sensitive dye imaging signals: application in awake behaving monkey.

Voltage sensitive dye imaging (VSDI) is the only technique that allows to directly measure neuronal activity over a large cortical population. It thus gives access to the dynamics of lateral interactions within or between cortical areas. However, VSDI signal suffers from a weak signal-to-noise ratio and processing methods are either rudimentary or dedicated to spatial or temporal denoising alone. Here we present an innovative method inspired by fMRI data processing, where the goal is to allow, for the first time, denoising of spatio-temporally inseparable VSDI signals and in the most challenging experimental condition, i.e. single trials in awake behaving monkeys. The method is based on a linear model (LM) decomposition of individual VSDI trials. The LM was designed meticulously by identifying all noise and signal components that are known to affect VSDI. We then compared its output against the classical methods based on blank division and detrending. LM proved to be significantly much more efficient to denoise spatial maps and temporal dynamics compared to these usual techniques. It also largely reduced trial-to-trial variability. These performances resulted in a four-fold improvement of signal-to-noise ratio and a two-fold increase of response detectability. Hence, with this method, fewer trials were needed to reach a high signal-to-noise ratio. Lastly, we showed that the LM method can accommodate for a large range of response dynamics, a crucial property for estimating spatial spread of activity or contrast dynamics. We believe that this method will make a strong contribution to imaging dynamics of population responses with high spatial and temporal resolution in trial-based experiments of awake animals.

The amblyopic deficit for 2nd order processing: Generality and laterality.

A number of previous reports have suggested that the processing of second-order stimuli by the amblyopic eye (AE) is defective and that the fellow non-amblyopic eye (NAE) also exhibits an anomaly. Second-order stimuli involve extra-striate as well as striate processing and provide a means of exploring the extent of the cortical anomaly in amblyopia using psychophysics. We use a range of different second-order stimuli to investigate how general the deficit is for detecting second-order stimuli in adult amblyopes. We compare these results to our previously published adult normative database using the same stimuli and approach to determine the extent to which the detection of these stimuli is defective for both amblyopic and non-amblyopic eye stimulation. The results suggest that the second-order deficit affects a wide range of second-order stimuli, and by implication a large area of extra-striate cortex, both dorsally and ventrally. The NAE is affected only in motion-defined form judgments, suggesting a difference in the degree to which ocular dominance is disrupted in dorsal and ventral extra-striate regions.

Real-time modulation of perceptual eye dominance in humans

Ocular dominance (OD) has long served as the model for neural plasticity. The shift of OD has been demonstrated by monocular deprivation in animals only during early visual development. Here, for the first time, we show that perceptual eye dominance can be modulated in real time in normal human adults by varying the spatial image content of movies seen dichoptically by the two eyes over a period as short as 2.5 h. Unlike OD shifts seen in early visual development, this modulation in human eye dominance is not simply a consequence of reduced interocular correlation (e.g. synchronicity) or overall contrast energy, but due to the amplitude reductions of specific image components in one eyes view. The spatial properties driving this eye dominance change suggest that the underlying mechanism is binocular but not orientationally selective, therefore uniquely locating it to layer 4 B of area V1.

A normative framework for the study of second-order sensitivity in vision

While the contrast sensitivity approach has been successful in evaluating the processing of first-order stimuli, there is a need to develop comparable ways of assessing second-order vision. Our purpose here is to establish normative data on second-order contrast-, orientation-, and motion-modulation sensitivity in humans. We propose a unified framework, applying the quick contrast sensitivity function (qCSF) method, which was recently developed for the rapid measurement of contrast sensitivity across the full spatial-frequency range (Lesmes, Lu, Baek, & Albright, 2010), to measure both first- and second-order sensitivity functions. We first show that the qCSF methodology can be successfully adapted to different kinds of first- and second-order measurements. We provide a normative dataset for both first- and second-order sensitivity, and we show that the sensitivity to all these stimuli is equal in the two eyes. Our results confirm some strong differences between first- and second-order processing, in accordance with the classical filter-rectify-filter model. They suggest a common contrast detection mechanism but different second-order mechanisms.

Properties of spatial channels underlying the detection of orientation-modulations

Orientation-modulated stimuli are thought to be processed via a two-stage process, the first stage involving the detection of the carrier by mechanisms in striate cortex and the second stage involving the detection of the modulation by way of integration of carrier-based information by mechanisms in extra-striate cortex. Much is known about the spatial properties of the channels underlying carrier detection but less is known about the properties of the channels involved in modulation detection. Using a discrimination at detection paradigm, we show that the mechanisms underlying modulation detection are tuned for envelope spatial frequency and orientation. The tuning of these channels is not substantially different from that previously described for carrier mechanisms, namely 1–2 octaves for spatial frequency and 30° for orientation. For orientation, these stimuli exhibit an oblique effect that is dependent on absolute carrier orientation, suggesting facilitative interactions between first- and second-stage processes.Orientation-modulated stimuli are thought to be processed via a two-stage process, the first stage involving the detection of the carrier by mechanisms in striate cortex and the second stage involving the detection of the modulation by way of integration of carrier-based information by mechanisms in extra-striate cortex. Much is known about the spatial properties of the channels underlying carrier detection but less is known about the properties of the channels involved in modulation detection. Using a discrimination at detection paradigm, we show that the mechanisms underlying modulation detection are tuned for envelope spatial frequency and orientation. The tuning of these channels is not substantially different from that previously described for carrier mechanisms, namely 1–2 octaves for spatial frequency and 30° for orientation. For orientation, these stimuli exhibit an oblique effect that is dependent on absolute carrier orientation, suggesting facilitative interactions between first- and second-stage processes.

A normative dataset on human global stereopsis using the quick Disparity Sensitivity Function (qDSF)

Global stereopsis results from the lateral displacement of distributed textured elements between the eyes. In this study, we investigate how the key parameters of the disparity sensitivity function such as its peak sensitivity and spatial bandwidth are distributed across a pool of normal observers and how large the individual differences are. For this purpose, we adapted the quick Contrast Sensitivity Function (qCSF, Lesmes et al., 2010) to the quick Disparity Sensitivity Function (qDSF). We show that this new method is accurate and allows a rapid measurement of disparity sensitivity for a range of different disparity spatial frequencies. Our results confirm that there is a greater variability in human disparity sensitivity tuning compared to other common visual features, for example, 1st or 2nd order contrast sensitivity.