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Feasibility of extraocular stimulation for a retinal prosthesis.

BACKGROUND: We present a new approach to developing a retinal prosthesis for blind patients based on extraocular stimulation of the eye with disc electrodes. METHODS: Experiments to assess the feasibility of using extraocular stimulation in a retinal prosthesis were carried out in anaesthetised adult cats (n=6). A craniotomy and lateral orbital dissection were performed. Ball or disc electrodes were placed on the posterior scleral surface of the eye after incision of the periorbita. Cortical potentials evoked by electrical stimulation with these electrodes were recorded at the primary visual cortex. The viability of adapting the Nucleus 24 auditory brainstem implant (ABI) as an extraocular retinal prosthesis was also investigated. RESULTS: Electrodes placed on the exterior of the eye could reliably evoke visual cortex responses for a variety of configurations. Threshold currents for eliciting an evoked response were lower than 100 microA with single pulses. Strength-duration curves and cortical activation maps were obtained for different stimulus paradigms. It was possible to excite the retina to evoke a cortical response using the electrodes and stimulus capabilities in a standard Nucleus 24 ABI. INTERPRETATION: It is possible to electrically stimulate the retina with electrodes placed in an extraocular location. Threshold currents required to elicit a response were low, and comparable to epiretinal implants. Prototype electrodes, and a potential implant, were found to be effective at retinal stimulation.

Animals↗

Preserved imagery for colours in a patient with cerebral achromatopsia.

We report the case of a patient who, after sequential bilateral strokes in the occipital regions sparing the primary visual cortex, developed a severe deficit of colour perception. At variance with other reports of acquired achromatopsic patients, she showed a perfectly vivid visual imagery for colours. These findings, together with similar data in domains other than colour processing, challenge the theories which posit that the same cognitive processes are involved in both the perception and the retrieval from memory of a given stimulus.

Aged↗

Neural response to emotional faces with and without awareness: event-related fMRI in a parietal patient with visual extinction and spatial neglect.

This study examined whether differential neural responses are evoked by emotional stimuli with and without conscious perception, in a patient with visual neglect and extinction. Stimuli were briefly shown in either right, left, or both fields during event-related fMRI. On bilateral trials, either a fearful or neutral left face appeared with a right house, and it could either be extinguished from awareness or perceived. Seen faces in left visual field (LVF) activated primary visual cortex in the damaged right-hemisphere and bilateral fusiform gyri. Extinguished left faces increased activity in striate and extrastriate cortex, compared with right houses only. Critically, fearful faces activated the left amygdala and extrastriate cortex both when seen and when extinguished; as well as bilateral orbitofrontal and intact right superior parietal areas. Comparison of perceived versus extinguished faces revealed no difference in amygdala for fearful faces. Conscious perception increased activity in fusiform, parietal and prefrontal areas of the left-hemisphere, irrespective of emotional expression; while a differential emotional response to fearful faces occurring specifically with awareness was found in bilateral parietal, temporal, and frontal areas. These results demonstrate that amygdala and orbitofrontal cortex can be activated by emotional stimuli even without awareness after parietal damage; and that substantial unconscious residual processing can occur within spared brain areas well beyond visual cortex, despite neglect and extinction.

Aged↗

Vision for spatial perception and vision for action: a dissociation between the left-right and near-far dimensions.

Neuropsychological and psychophysical studies have suggested that two distinct visual sub-systems are responsible for perception and action. One of the main psychophysical arguments for this is based on visual illusion such as the Induced Roelofs Effect (IRE), where the location of a visual target presented with an off-centre frame is misperceived when evaluated verbally, but not with a reaching response. This dissociated effect suggests the existence of two independent representations of visual space devoted, respectively, to categorisation and to egocentric localisation of reachable objects. These "cognitive" and "sensorimotor" representations have been assumed to be produced through specific anatomical pathways stemming from the primary visual cortex (respectively, the ventral and dorsal streams). To account for the dissociation found with the IRE, it has been suggested that only the cognitive system is sensitive to contextual information. However this view has been challenged by recent psychophysical studies demonstrating the influence of environmental cues on distance perception and the guiding of movement. In the present study, the IRE is re-evaluated but the near-far and right-left dimensions were dissociated. In agreement with previous findings, our results showed that the IRE in the right-left dimension gives rise to a perceptual misperception of target position with no effect on motor performance. Conversely, when the IRE was induced in the near-far dimension a misperception of the target position affected both perceptual and motor responses. This dissociation indicates that the spatial constraints of the task, and not only the nature of the response, interfere with sensitivity to contextual information leading to visual illusions. It is thus likely that the action system (imputed to the dorsal stream) can be sensitive to contextual information, at least when depth processing is emphasised.

Adult↗

Correlates of figure-ground segregation in fMRI.

We investigated which correlates of figure-ground-segregation can be detected by means of functional magnetic resonance imaging (fMRI). Five subjects were scanned with a Siemens Vision 1.5 T system. Motion, colour, and luminance-defined checkerboards were presented with alternating control conditions containing one of the two features of the checkerboard. We find a segregation-specific activation in V1 for all subjects and all stimuli and conclude that neural mechanisms exist as early as in the primary visual cortex that are sensitive to figure-ground segregation.

Adult↗

Visual jitter: evidence for visual-motion-based compensation of retinal slip due to small eye movements.

When dynamic random noise is replaced by static noise after a period of adaptation, adjacent unadapted regions filled with static noise appear to 'jitter' coherently in random directions for several seconds, actually mirroring the observer's own eye movements of fixation [Murakami, I. & Cavanagh, P. (1998). Nature, 395, 798-801]. The present study aims at psychophysically locating two distinct stages underlying this visual jitter phenomenon: a monocular, adaptable stage that measures local retinal motion and a compensation stage that estimates a baseline motion minimum and subtracts it from motion vectors nearby. The first three experiments revealed that visual jitter has storage, directional selectivity, and spatial frequency selectivity, like the motion after-effect does. These results suggest some overlap in the adaptation mechanisms for the two effects, possibly at or below the level of primary visual cortex. The next two experiments revealed the transfer of the effect across the vertical meridian as well as the existence of a preferred stimulus size that is a linear increasing function of eccentricity, mimicking the RF size of the monkey MT neurons. These results suggest that some extrastriate motion area along the parietal pathway including MT mediates motion-based compensation of retinal slip.

Adaptation, Physiological↗

High-resolution spatio-temporal mapping of visual pathways using multi-electrode arrays.

The parallel processing of visual information was studied with penetrating microelectrode arrays. We studied the high-resolution visuotopic organization of cat primary visual cortex, and the encoding of simple visual stimuli by ensembles of ganglion cells in the isolated turtle retina. The high-resolution visuotopic organization of visual cortex is non-conformal. Regions of visual cortex separated by 400 mu may have receptive field centers that are separated by as much as 3 degrees, or they may superimpose. Ganglion cells are 'generalists', and are poor specifiers of the color of full field visual stimuli. Groups of 'luminosity' type ganglion cells can assist in the specification of stimulus color, but even individual 'chromatic' ganglion cells are not capable of quality color specification. These basic studies have relevance to the development of visual neuroprostheses based upon electrical stimulation of the retina and cortex.

Animals↗

A transition between eye and object rivalry determined by stimulus coherence.

Two orthogonal patterns presented to the two eyes, respectively, are perceived as alternating in time, a phenomenon often assumed to reflect competition between neuronal activities corresponding to the two eyes, presumably in the primary visual cortex. Recent evidence supports a competition between neuronal activities corresponding to the two patterns (objects) at some higher cortical processing stage after inputs from the two eyes have converged. Here, using textures made of Gabor signals, we present psychophysical data showing that the level of visual processing at which competition takes place and is resolved, is determined by the degree of stimulus coherence. Moreover, depending on stimulus parameters, competition may occur at several levels of processing at the same time.

Humans↗

The relatively small decline in orientation acuity as stimulus size decreases.

Orientation acuity was measured with circular patches of sinusoidal gratings of various sizes. Threshold estimates were lowest (acuity highest) for the largest size patch, and increased as the stimulus size was reduced, consistent with the results of many researchers using line stimuli. These results are compared with the predictions of a simple and widely accepted model of spatial vision whereby the output of independent feed-forward filters are combined to produce threshold estimates. Specifically, the rectified output of a number of independent filters (i.e. Gabors) spanning the stimulus space (i.e. orientation) are combined via Bayesian decision theory. This model cannot account quantitatively for the relatively low thresholds estimated for the small sized stimuli when compared to the thresholds measured with larger patches. Application of a comparable analysis, with preliminary measurements of neuronal responses from primary visual cortex replacing the response rectified Gabor filter's responses, provides a more reasonable account of behavioral acuity. This indicates a fundamental inadequacy of the feed-forward filter model in accounting for V1 neurons' role in perception.

Adult↗

Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients.

Patients with lesions in the primary visual cortex (V1) may show processing of visual stimuli presented in their field of cortical blindness even when they report being unaware of the stimuli. To elucidate the neuroanatomical basis of their residual visual functions, we used functional magnetic resonance imaging in two hemianopic patients, FS and GY. In the first experiment, a rotating spiral stimulus was used to assess the responsiveness of dorsal stream areas. Although no response was detectable within denervated or destroyed early visual cortex, motion-sensitive areas (hMT+/V5) ipsilateral to the lesion showed a strong sustained hemodynamic response. In GY, this activation was at least as strong as that of his contralesional hMT+/V5 to the stimulus in the normal hemifield. In the second experiment, coloured images of natural objects were used to assess the responsiveness of ventral stream areas. Again, no activity was detectable in ipsilesional early visual areas, but extrastriate areas in the lateral occipital cortex (hMT+/V5 and LO) and within the posterior fusiform gyrus (V4/V8) showed a robust sustained hemodynamic response. In both experiments, we observed that ipsilesional areas responded to stimuli presented in either hemifield, whereas the normal hemisphere responded preferentially to stimuli in the sighted hemifield. As only one subject occasionally noticed the onset of stimulation in the impaired field, the unexpectedly strong sustained activity in ipsilesional dorsal and ventral cortical areas appears to be insufficient to generate conscious vision.

Adult↗

The relative sensitivities of sensory and motor fusion to small binocular disparities.

Horizontal binocular disparity is the fundamental stimulus for both fusional vergence and stereopsis, but whether common disparity-sensitive mechanisms are involved in both responses is unknown. To determine whether the sensitivities of motor and sensory fusion are interdependent, we studied vergence eye movements and depth discrimination, using stimuli with haplopic binocular disparities, in subjects with normal stereopsis and in subjects with mild to severe stereoanomalies. Our results showed that the subjects' disparity discrimination functions varied from nearly perfect discrimination to chance performance for all of the experimental stimuli. Their sensory functions did not necessarily predict the shape of their motor fusion functions, but in most cases were correlated with the subject's fixation disparities. The results support the conclusion that the stereoanomalies and vergence anomalies that previously have been described for coarse binocular disparities also extend to the small, haplopic binocular disparities. The independence of the response properties of sensory and motor fusion suggests that neural pathways for sensory and motor fusion separate after the initial disparity-selective mechanisms in primary visual cortex.

Depth Perception↗

Spatial scale of motion segmentation from speed cues.

For the accurate perception of multiple, potentially overlapping, surfaces or objects, the visual system must distinguish different local motion vectors and selectively integrate similar motion vectors over space to segment the retinal image properly. We recently showed that large differences in speed are required to yield a percept of motion transparency. In the present study, to investigate the spatial scale of motion segmentation from speed cues alone, we measured the speed-segmentation threshold (the minimum speed difference required for 75% performance accuracy) for 'corrugated' random-dot patterns, i.e. patterns in which dots with two different speeds were alternately placed in adjacent bars of variable width. In a first experiment, we found that, at large bar widths, a smaller speed difference was required to segment and perceive the corrugated pattern of moving dots, while at small bar-widths, a larger speed difference was required to segment the two speeds and perceive two transparent surfaces of moving dots. Both the perceptual and segmentation performance transitions occurred at a bar width of around 0.4 degrees. In a second experiment, speed-segmentation thresholds were found to increase sharply when dots with different speeds were paired within a local pooling area. The critical pairing distance was about 0.2 degrees in the fovea and increased linearly with stimulus eccentricity. However, across the range of eccentricities tested (up to 15 degrees ), the critical pairing distance did not change much and remained close to the receptive field size of neurons within the primate primary visual cortex. In a third experiment, increasing dot density changed the relationship between speed-segmentation thresholds and bar width. Thresholds decreased for large bar widths, but increased for small bar widths. All of these results are well fit by a simple stochastic model, which estimates the probabilities of having identical or different motion vectors within a local pooling area whose size is the same as that of primate V1 neurons. Altogether, these results demonstrate that speed-based segmentation can function well, even at small spatial scales (i.e. high-spatial frequencies of spatial corrugation) and thereby emphasizes the critical role of a local pooling process early in the cortical motion-processing pathway.

Cues↗

Better perception of global motion after monocular than after binocular deprivation.

We used random-dot kinematograms to compare the effects of early monocular versus early binocular deprivation on the development of the perception of the direction of global motion. Patients had been visually deprived by a cataract in one or both eyes from birth or later after a history of normal visual experience. The discrimination of direction of global motion was significantly impaired after early visual deprivation. Surprisingly, impairments were significantly worse after early binocular deprivation than after early monocular deprivation, and the sensitive period was very short. The unexpectedly good results after monocular deprivation suggest that the higher centers involved in the integration of global motion profit from input to the nondeprived eye. These findings suggest that beyond the primary visual cortex, competitive interactions between the eyes can give way to collaborative interactions that enable a relative sparing of some visual functions after monocular deprivation.

Adolescent↗

A multi-layer sparse coding network learns contour coding from natural images.

An important approach in visual neuroscience considers how the function of the early visual system relates to the statistics of its natural input. Previous studies have shown how many basic properties of the primary visual cortex, such as the receptive fields of simple and complex cells and the spatial organization (topography) of the cells, can be understood as efficient coding of natural images. Here we extend the framework by considering how the responses of complex cells could be sparsely represented by a higher-order neural layer. This leads to contour coding and end-stopped receptive fields. In addition, contour integration could be interpreted as top-down inference in the presented model.

Cerebral Cortex↗

Sensitivity to global form in glass patterns after early visual deprivation in humans.

To compare the effects of early monocular versus early binocular deprivation on the perception of global form, we assessed sensitivity to global concentric structure in Glass patterns with varying ratios of paired signal dots to noise dots. Children who had been deprived by dense congenital cataracts in one (n=10) or both (n=8) eyes performed significantly worse than comparably aged children without eye problems. Consistent with previous results on sensitivity to global motion [Vision Research 42 (2002) 169], thresholds in the deprived eyes were significantly better after monocular deprivation than after binocular deprivation of comparable duration, even when there had been little patching of the nondeprived eye after monocular deprivation. Together, the results indicate that the competitive interactions between a deprived and nondeprived eye evident in the primary visual cortex can co-occur with complementary interactions in extrastriate cortex that enable a relative sparing of some visual functions after early monocular deprivation.

Adolescent↗

Texture segmentation performance related to cortical geometry.

There are two prevailing explanations for the foveal deficit in texture segmentation reported in previous works. One is based on the spatial and temporal properties of the stimuli, which means in terms of physiology a strong contribution of the Magno-channel. The other one is purely spatial and assigns filters of different bandwidths to each eccentricity in the visual field. We have challenged the first explanation experimentally by using isoluminant stimuli. The central performance drop persisted although the Magno-channel is known to respond weakly to stimuli with low luminance contrast. Therefore, we agreed with the spatial explanation. But instead of the abstract filter theories from previous works we propose a computational neural model assuming local lateral interactions in a cortical map model. The psychophysical performance measures could be directly related to geometric properties of the primary visual cortex concerning its mapping geometry and its intrinsic interaction width. Our model accounts quantitatively for our own psychophysical data as well as for others from literature. In general, we claim that the high foveal retino-cortical magnification maps texture elements too far away from each other for being compared by local processes.

Contrast Sensitivity↗

The role of complex cells in object recognition.

Primate's primary visual cortex (V1) is dominated by complex cells. This choice of nature seems puzzling, as complex cells are insensitive to spatial phase--information which is generally believed to be essential for perceptual characterization and recognition of images. Modeling complex cells as Gabor wavelet magnitudes, we have mathematically and empirically examined the information content of their responses. Our results show that in spite of phase insensitivity of individual complex cell responses, population responses contain sufficient information to capture the perceptual essence of images. A complex cell type representation seems to be not only sufficiently discriminating for object identification, but also--due to its inherent ambiguities--robust to changes in background, lighting, and small deformations.

Form Perception↗

Reading a population code: a multi-scale neural model for representing binocular disparity.

Although binocular neurons in the primary visual cortex are sensitive to retinal disparity, their activity does not constitute an unambiguous disparity signal. A multi-spatial-scale neural model for disparity computation is developed to examine how population activity might be interpreted to overcome ambiguities at the single neuron level. The model incorporates a front end that encodes disparity by a family of complex cell-like energy units and a second stage that reads the population activity. Disparity is recovered by matching the population response to a set of canonical templates, derived from the mean response to white noise stimuli at a range of disparities. Model predictions are qualitatively consistent with a variety of psychophysical results in the literature, including the effects of spatial frequency on stereoacuity and bias in perceived depths, and the effect of standing disparity on increment thresholds. Model predictions are also consistent with data on qualitative appearance of complex stimuli, including depth averaging, transparency, and corrugation. The model also accounts for the non-linear interaction of disparities in compound grating stimuli. These results show that a template-match approach reduces ambiguities in individual and pooled neuronal responses, and allows for a broader range of percepts, consistent with psychophysics, than other models. Thus, the pattern of neural population activity across spatial scales is a better candidate for the neural correlate of depth perception than the activity of single neurons or the pooled activity of multiple neurons.

Depth Perception↗