Advanced computational model of rod ERG kinetics.

PURPOSE: The electroretinogram (ERG) is the summed response from all levels of the retinal processing of light, and exhibits several profound nonlinearities in the underlying processing pathways. Accurate computational models of the ERG are important, both for understanding the multifold processes of light transduction to ecologically useful signals by the retina, and for their diagnostic capabilities for the identification and characterization of retinal disease mechanisms. There are, however, very few computational models of the ERG waveform, and none that account for the full extent of its features over time. METHODS: This study takes the neuroanalytic approach to modeling the ERG waveform, defined as a computational model based on the main features of the transmitter kinetics of the retinal neurons. RESULTS: The present neuroanalytic model of the human rod ERG is elaborated from the same general principles as that of Hood and Birch (Vis Neurosci 8(2):107-126, 1992), but incorporates the more recent understanding of the early nonlinear stages of ERG generation by Robson and Frishman (Prog Retinal Eye Res 39:1-22, 2014). As a result, it provides a substantially better match than previous models of rod responses in six different waveform features of the ERG flash intensity series on which the Hood and Birch model was based. CONCLUSION: The neuroanalytic approach extends previous models of the component waves of the ERG, and can be structured to provide an accurate characterization of the full timecourse of the ERG waveform. The approach thus holds promise for advancing the theoretical understanding of the retinal kinetics of the light response.

Suprathreshold length summation.

To investigate the mechanisms underlying elongated spatial summation with a pattern-masking paradigm, we measured the contrast detection thresholds for elongated Gabor targets situated at 3° eccentricity to either the left or right of the fixation and elongated along an arc of the same radius to access homogeneous retinal sensitivity. The mask was a ring with a Gabor envelope of the same 3° center radius containing either a concentric (iso-orientation mask) or a radial (orthogonal mask) modulation. The task of the observer was to indicate whether the target in each trial was on the left or the right of the fixation. With orthogonal or low contrast iso-orientation masks, target thresholds first decreased with size with slope -1 on log-log coordinates until the target length reached 45' (specified as the half-height full-width of the Gabor envelope) and then further decreased according to a slope of -1/2, the latter being the signature of an ideal summation process. When the contrast of the iso-orientation mask was sufficiently high, however, the target thresholds, while still showing a -1 slope up to ∼10', asymptoted up to about 50' length, suggesting that the presence of the mask eliminated the ideal summation regime. Beyond about 50', the data approximated another -1 slope decrease in threshold, suggesting the existence of an extra-long channel that is not revealed by the conventional spatial summation paradigm. The full results could be explained by a divisive inhibition model, in which second-order filters sum responses across local oriented channels, combined with a single extra-long filter at least 300' in extent. In this model, the local filter response is given by the linear excitation of the local channels raised to a power, and scaled by divisive inhibition from all channels in the neighborhood. With the high-contrast iso-orientation masks, such divisive inhibition swamps the response to eliminate the ideal summation regime until the stimulus is long enough to activate the extra-long filter.

Brain trauma impacts retinal processing: photoreceptor pathway interactions in traumatic light sensitivity.

BACKGROUND: Concussion-induced light sensitivity, or traumatic photalgia, is a lifelong debilitating problem for upwards of 50% of mild traumatic brain injury (mTBI) cases, though of unknown etiology. We employed spectral analysis of electroretinographic (ERG) responses to assess retinal changes in mTBI as a function of the degree of photalgia. METHODS: The design was a case-control study of the changes in the ERG waveform as a function of level of light sensitivity in individuals who had suffered incidents of mild traumatic brain injury. The mTBI participants were categorized into non-, mild-, and severe-photalgic groups based on their spectral nociophysical settings. Light-adapted ERG responses were recorded from each eye for 200 ms on-off stimulation of three spectral colors (R:red, G:green, and B:blue) and their sum (W:white) at the highest pain-free intensity level for each participant. The requirement of controls for testing hypersensitive individuals at lower light levels was addressed by recording a full light intensity series in the control group. RESULTS: Both the b-wave and the photopic negative response (PhNR) were significantly reduced in the non-photalgic mTBI group relative to controls. In the photalgic groups, the main b-wave peak shifted to the timing of the rod b-wave, with reduced amplitude at the timing of the cone response. CONCLUSION: These results suggest the interpretation that the primary etiology of the painful light sensitivity in mTBI is release of the rod pathway from cone-mediated inhibition at high light levels, causing overactivation of the rod pathway.

A Live Experience of Four-Dimensional Structure.

Selective attention is well known for 2D patterns and perceptual alternations are well established for 3D structures projected into 2D, such as the Necker cube. Here, these concepts are extended to the spatial fourth dimension in the form of the mathematical structure of the 4D hypercube. In orthographic projection, its 2D outline figure has multiple and highly dynamic percepts of up to 28 different 3D interpretations, which correspond to local 3D views of the 4D hypercube. Thus, the spontaneous operations of perceptual processing can provide direct insight into conceptual structure in the fourth dimension.

The Interstitial Pathways as the Substrate of Consciousness: A New Synthesis.

This paper considers three classes of analyses of the nature of consciousness: abstract theories of the functional organization of consciousness, and concrete proposals as to the neural substrate of consciousness, while providing a rationale for contesting non-neural and transcendental conceptualizations of consciousness. It indicates that abstract theories of the dynamic core of consciousness have no force unless they are grounded in the physiology of the brain, since the organization of dynamic systems, such as the Sun, could equally well qualify as conscious under such theories. In reviewing the wealth of studies of human consciousness since the mid-20th century, it concludes that many proposals for the particular neural substrate of consciousness are insufficient in various respects, but that the results can be integrated into a novel scheme that consciousness extends through a subcortical network of interlaminar structures from the brainstem to the claustrum. This interstitial structure has both the specificity and the extended connectivity to account for the array of reportable conscious experiences.

The Intersection of Visual Science and Art in Renaissance Italy.

In the time of the Renaissance, a major aspect of vision science was understanding how spatial information projected to the viewpoint of the observer, that is, visual perspective, which is one of the primary cues to depth perception. Perspective representation was thus an early form of virtual reality. Although accurate perspective representation was developed earlier in the 15th century, the first analytic perspective scheme was developed by Piero della Francesca, whose chef d'oeuvre is in the Church of San Francesco, Arezzo, in which the present lecture took place. The focus of the lecture was to evaluate some of the contributions of Piero della Francesca and his 15th-century contemporaries to the visual science, art and symbolism of his era, and its significance for the perception of depth structure from two-dimensional images.

Length summation in noise.

To investigate the effect of background noise on visual summation, we measured the contrast detection thresholds for targets with or without a white noise mask in luminance contrast. The targets were Gabor patterns placed at 3° eccentricity to either the left or right of the fixation and elongated along an arc of the same radius to ensure equidistance from fixation for every point along the long axis. The task was a spatial two-alternative forced-choice (2AFC) paradigm in which the observer had to indicate whether the target was on the left or the right of the fixation. The threshold was measured at 75% accuracy with a staircase procedure. The detection threshold decreased with target length with slope -1/2 on log-log coordinates for target lengths between 30' and 300' half-height full-width (HHFW), defining a range of ideal matched-filter summation extending up to about 200' (or about 16× the center width of the Gabor targets). The summation curves for different noise contrasts were shifted copies of each other. For the threshold versus mask contrast (TvN) functions, the target threshold was constant for noise levels up to about -22 dB, then increased with noise contrast to a linear asymptote on log-log coordinates. Since the "elbow" of the target threshold versus noise function is an index of the level of the equivalent noise experienced by the visual system during target detection, our results suggest that the signal-to-noise ratio was invariant with target length. We further show that a linear-nonlinear-linear gain-control model can fully account for these results with far fewer parameters than a matched-filter model.

Measurement of saccadic eye movements by electrooculography for simultaneous EEG recording.

Eye movements are an important index of the neural functions of visual information processing, decision making, visuomotor coordination, sports performance, and so forth. However, the available optical tracking methods are impractical in many situations, such as the wearing of eyeglasses or the presence of ophthalmic disorders, and this can be overcome by accurate recording of eye movements by electrooculography (EOG). In this study we recorded eye movements by EOG simultaneously with high-density electroencephalogram (EEG) recording using a 128-channel EGI electrode net at a 500-Hz sampling rate, including appropriate facial electrodes. The participants made eye movements over a calibration target consisting of a 5×5 grid of stimulus targets. The results showed that the EOG methodology allowed accurate analysis of the amplitude and direction of the fixation locations and saccadic dynamics with a temporal resolution of 500 Hz, under both cued and uncued analysis regimes. Blink responses could be identified separately and were shown to have a more complex source derivation than has previously been recognized. The results also showed that the EOG signals recorded through the EEG net can achieve results as accurate as typical optical eye-tracking devices, and also allow for simultaneous assessment of neural activity during all types of eye movements. Moreover, the EOG method effectively avoids the technical difficulties related to eye-tracker positioning and the synchronization between EEG and eye movements. We showed that simultaneous EOG/EEG recording is a convenient means of measuring eye movements, with an accuracy comparable to that of many specialized eye-tracking systems.

Evidence of Stereoscopic Surface Disambiguation in the Responses of V1 Neurons.

For the important task of binocular depth perception from complex natural-image stimuli, the neurophysiological basis for disambiguating multiple matches between the eyes across similar features has remained a long-standing problem. Recurrent interactions among binocular disparity-tuned neurons in the primary visual cortex (V1) could play a role in stereoscopic computations by altering responses to favor the most likely depth interpretation for a given image pair. Psychophysical research has shown that binocular disparity stimuli displayed in 1 region of the visual field can be extrapolated into neighboring regions that contain ambiguous depth information. We tested whether neurons in macaque V1 interact in a similar manner and found that unambiguous binocular disparity stimuli displayed in the surrounding visual fields of disparity-selective V1 neurons indeed modified their responses when either bistable stereoscopic or uniform featureless stimuli were presented within their receptive field centers. The delayed timing of the response behavior compared with the timing of classical surround suppression and multiple control experiments suggests that these modulations are carried out by slower disparity-specific recurrent connections among V1 neurons. These results provide explicit evidence that the spatial interactions that are predicted by cooperative algorithms play an important role in solving the stereo correspondence problem.

Development and validation of a new glaucoma screening test using temporally modulated flicker.

PURPOSE: Describing the psychometric characteristics and diagnostic accuracy of the Accelerator 4-Alternative Forced-Choice Flicker Test prototype (A4FTp) for detecting chronic open angle glaucoma (COAG). METHODS: A4FTp measures temporally-modulated flicker thresholds in regions of the visual field with high susceptibility to glaucomatous loss. We initially evaluated its psychometric properties on 20 normals (aged 33.8 ± 8.5 years) who were tested multiple times over a period of 3 months. All subjects underwent four repetitions for shorter (T8) and longer (T12) staircase termination criteria, to determine the most suitable threshold criterion. Four randomly selected subjects underwent a total of 10 repetitions to study test-retest repeatability and learning effects. To determine its diagnostic accuracy, one eye of 40 participants with COAG and 38 normal controls were tested with the A4FTp in comparison with the Frequency Doubling Technology (FDT; C20-5 programme) and iVue Spectral Domain Optical Coherence Tomography (SD-OCT). Tests were conducted in a random order with results masked to the clinician conducting the reference ophthalmic examination. The accuracy of each test was determined by analysis of the area under the receiver operator characteristic curve (AUROC). RESULTS: A4FTp flicker thresholds were stable, with standard deviations of only 0.52 decilog (dL) for T8, increasing to 1.32 dL for T12, and no significant flicker sensitivity threshold improvement over the 10 repeat runs. T8 was superior to T12 on several other measures, so it was used for the remaining comparisons. In terms of diagnostic accuracy, the mean AUROC for the three tests were A4FTp [T8 criterion; 0.82, 95% confidence interval (0.73-0.92)]; SD-OCT [any RNFL parameter p < 1% level; 0.90 (0.83-0.97)]; and FDT [one or more locations missed at p < 5% level; 0.91 (0.82-0.96)]. There was no statistical difference in AUROC between A4FTp and SD-OCT (p = 0.18) or FDT (p = 0.12). The A4FTp test duration averaged just over 2 min per eye, taking approximately one-third of the time for completion of the HFA SITA 24-2 algorithm (conducted as part of the reference examination) and twice the time for the suprathreshold FDT. CONCLUSION: Test accuracy for the A4FTp was comparable to those of the FDT and SD-OCT for the detection of COAG. Time taken to complete the A4FTp was relatively short and initial results are promising. With further refinement, the A4FTp could have a future role in glaucoma detection.

Improvement of contrast sensitivity with practice is not compatible with a sensory threshold account.

In forced-choice detection, incorrect responses are routinely ascribed to internal noise, because experienced psychophysical observers do not act as if they have a sensory threshold, below which all perceived intensities would be identical. To determine whether inexperienced observers have sensory thresholds, we examined psychometric functions (percent correct versus log contrast) for detection and detection in full-screen, dynamic visual noise. Over five days, neither type of psychometric function changed shape, but both shifted leftwards, indicating increased sensitivity. These results are not consistent with a lowered sensory threshold, which would decrease psychometric slope. Our results can be understood within the context of Dosher and Lu's "stochastic" perceptual template model [Vis. Res.40, 1269 (2000)], augmented to allow intrinsic uncertainty. Specifically, our results are consistent with a combination of reduced internal additive noise and improved filtering of external noise.

Studying the Retinal Source of Photophobia by Facial Electroretinography.

PURPOSE: Photophobia is a debilitating clinical condition that disrupts the ability to use vision for everyday tasks in bright lighting conditions. The goal of the study is to develop a methodology to study the neural basis of photophobia and the contribution of the melanopic pathway to its etiology with differential chromatic responses by means of standard electroencephalographic recording equipment. METHODS: We introduce and validate the approach of recording wavelength-specific electroretinographic (ERG) responses from the face electrodes of the high-density whole-head electroencephalography recording system under light-adapted conditions. RESULTS: ERGs recorded in this way to whole-field chromatic stimuli exhibit striking differences between the photophobic and non-photophobic groups. The control responses were consistent with photopic intensity in peak time, and in the ordering of peak times as a function of wavelength condition, indicating a predominantly cone source of the signals. The photophobic responses, on the other hand, were substantially slowed relative to controls, with the peak times conforming to a different order as a function of wavelength condition than controls, implying that the cone response has been suppressed and that the responses derived from a different photoreceptor system consistent with mediation by melanopic retinal ganglion cells. CONCLUSIONS: The results will be important for determining the neural pathways involved in photophobia and potential approaches to its treatment on the basis of this etiology.

The perceived depth from disparity as function of luminance contrast.

Does human vision show the contrast invariance expected of an ideal stereoscopic system for computing depth from disparity? We used random-dot stereograms to investigate the luminance contrast effect on perceived depth from disparity. The perceived depth of disparity corrugations was measured by adjusting the length of a horizontal line to match the perceived depth of the corrugations at various luminance contrasts. At each contrast, the perceived depth increased with disparity up to a critical value, decreasing with further increases in disparity. Both the maximum perceived depth and the disparity modulation level where this maximum occurred changed as a sigmoid function of luminance contrast. These results show that perceived depth from disparity depends in a complex manner on the luminance contrast in the image, providing significant limitations on depth perception at low contrasts in a lawful manner but that are incompatible with existing models of cortical disparity processing.

Inefficiency of orientation averaging: Evidence for hybrid serial/parallel temporal integration.

Intuition suggests that increased viewing time should allow for the accumulation of more visual information, but scant support for this idea has been found in studies of voluntary averaging, where observers are asked to make decisions based on perceived average size. In this paper we examine the dynamics of information accrual in an orientation-averaging task. With orientation (unlike intensive dimensions such as size), it is relatively safe to use an item's physical value as an approximation for its average perceived value. We displayed arrays containing eight iso-eccentric Gabor patterns, and asked six trained psychophysical observers to compare their average orientation with that of probe stimuli that were visible before, during, or only after the presentation of the Gabor array. From the relationship between orientation variance and human performance, we obtained estimates of effective set size, i.e., the number of items that an ideal observer would need to assess in order to estimate average orientation as well as our human observers did. We found that display duration had only a modest influence on effective set size. It rose from an average of ∼2 for 0.1-s displays to an average of ∼3 for 3.3-s displays. These results suggest that the visual computation is neither purely serial nor purely parallel. Computations of this nature can be made with a hybrid process that takes a series of subsamples of a few elements at a time.

Recurrent connectivity can account for the dynamics of disparity processing in V1.

Disparity tuning measured in the primary visual cortex (V1) is described well by the disparity energy model, but not all aspects of disparity tuning are fully explained by the model. Such deviations from the disparity energy model provide us with insight into how network interactions may play a role in disparity processing and help to solve the stereo correspondence problem. Here, we propose a neuronal circuit model with recurrent connections that provides a simple account of the observed deviations. The model is based on recurrent connections inferred from neurophysiological observations on spike timing correlations, and is in good accord with existing data on disparity tuning dynamics. We further performed two additional experiments to test predictions of the model. First, we increased the size of stimuli to drive more neurons and provide a stronger recurrent input. Our model predicted sharper disparity tuning for larger stimuli. Second, we displayed anticorrelated stereograms, where dots of opposite luminance polarity are matched between the left- and right-eye images and result in inverted disparity tuning in the disparity energy model. In this case, our model predicted reduced sharpening and strength of inverted disparity tuning. For both experiments, the dynamics of disparity tuning observed from the neurophysiological recordings in macaque V1 matched model simulation predictions. Overall, the results of this study support the notion that, while the disparity energy model provides a primary account of disparity tuning in V1 neurons, neural disparity processing in V1 neurons is refined by recurrent interactions among elements in the neural circuit.

Spatial summation for motion detection.

We used the psychophysical summation paradigm to reveal some spatial characteristics of the mechanism responsible for detecting a motion-defined visual target in central vision. There has been much previous work on spatial summation for motion detection and direction discrimination, but none has assessed it in terms of the velocity threshold or used velocity noise to provide a measure of the efficiency of the velocity processing mechanism. Motion-defined targets were centered within square fields of randomly selected gray levels. The motion was produced within the disk-shaped target region by shifting the pixels rightwards for 0.2 s. The uniform target motion was perturbed by Gaussian motion noise in horizontal strips of 16 pixels. Independent variables were field size, the diameter of the disk target, and the variance of an independent perturbation added to the (signed) velocity of each 16-pixel strip. The dependent variable was the threshold velocity for target detection. Velocity thresholds formed swoosh-shaped (descending, then ascending) functions of target diameter. Minimum values were obtained when targets subtended approximately 2 degrees of visual angle. The data were fit with a continuum of models, extending from the theoretically ideal observer through various inefficient and noisy refinements thereof. In particular, we introduce the concept of sparse sampling to account for the relative inefficiency of the velocity thresholds. The best fits were obtained from a model observer whose responses were determined by comparing the velocity profile of each stimulus with a limited set of sparsely sampled "DoG" templates, each of which is the product of a random binary array and the difference between two 2-D Gaussian density functions.

Success rates, near-response patterns, and learning trends with free-fusion stereograms.

Free-fusion stereograms are routinely used for demonstrating various stereoscopic effects. Yet, untrained observers find it challenging to perform this task. This study showed that only less than 1/3rd of sixty-one pre-presbyopic adults with normal binocular vision could successfully free-fuse random-dot image pairs and identify the stereoscopic shapes embedded in these patterns. Another one-third of participants performed the task with poor success rates, while the remaining could not perform the task. There was a clear dissociation of vergence and accommodative responses in participants who were successful with free-fusion, as recorded using a dynamic infrared eye tracker and photorefractor. Those in the unsuccessful cluster either showed strong vergence and accommodation or weak vergence and strong accommodation during the task. These response patterns, however, were specific to the free-fusion task because all these participants generated good convergence/accommodation to real-world targets and to conflicting vergence and accommodative demands stimulated with prisms or lenses. Task performance of the unsuccessful cluster also improved significantly following pharmacological paralysis of accommodation and reached the performance levels of the successful cluster. A minority of participants also appeared to progressively learn to dissociate one of the two directions of their vergence and accommodation crosslinks with repeated free-fusion trials. These results suggest that successful free-fusion might depend upon how well participants generate a combination of volitional and reflex vergence responses to large differences in disparity with conflicting static accommodative demands. Such responses would require that only one direction of the vergence-accommodation crosslinks be active at any given time. The sequence of near-responses could also be learnt through repeated trials to optimize task performance.

Comparison of Depth-Related Visuomotor Task Performance in Uniocular Individuals and in Binocular Controls With and Without Temporary Monocular Occlusion.

Purpose: Do one-eyed (uniocular) humans use monocular depth cues differently from those with intact binocularity to perform depth-related visuomotor tasks that emulate complex activities of daily living? If so, does performance depend on the participant's age, duration of uniocularity and head movements? Methods: Forty-five uniocular cases (age range 6-37 years; 2.4 months-31.0 years of uniocularity) and 46 age-similar binocular controls performed a task that required them to pass a hoop around an electrified wire convoluted in depth multiple times, while avoiding contact as indicated by auditory feedback. The task was performed with and without head restraint, in random order. The error rate and speed were calculated from the frequency of contact between the hoop and wire and the total task duration (adjusting for error time), respectively, all determined from video recordings of the task. Head movements were analyzed from the videos using face-tracking software. Results: Error rate decreased with age (P < 0.001) until the late teen years while speed revealed no such trend. Across all ages, the error rate increased and speed decreased in the absence of binocularity (P < 0.001). There was no additional error reduction with duration of uniocularity (P = 0.16). Head movements provided no advantage to task performance, despite generating parallax disparities comparable to binocular viewing. Conclusions: Performance in a dynamic, depth-related visuomotor task is reduced in the absence of binocular viewing, independent of age-related performance level. This study finds no evidence for a prolonged experience with monocular depth cues being advantageous for such tasks over transient loss of binocularity.

A simpler structure for local spatial channels revealed by sustained perifoveal stimuli.

A new evaluation of the local structure of spatial channels with sustained stimuli in perifoveal retina employs the masking sensitivity approach to minimize analytic assumptions. The stimuli were designed to address the range of channel tunings of the predominantly sustained response system in the near periphery. Under these conditions, the range of identifiable channels spanned a narrow range of spatial frequencies, from roughly 2-8 cpd at 2° eccentricity to 1-4 cpd at 8° eccentricity. The analysis showed that there are no sustained channels tuned below 2 cpd for the central visual field. This two-octave range of channel tuning is much narrower than is conventionally assumed. For local sustained stimuli, human peripheral spatial processing therefore appears to be based on a simpler channel structure than is often supposed.