Plasticity of the human visual brain after an early cortical lesion.

In adults, partial damage to V1 or optic radiations abolishes perception in the corresponding part of the visual field, causing a scotoma. However, it is widely accepted that the developing cortex has superior capacities to reorganize following an early lesion to endorse adaptive plasticity. Here we report a single patient case (G.S.) with near normal central field vision despite a massive unilateral lesion to the optic radiations acquired early in life. The patient underwent surgical removal of a right hemisphere parieto-temporal-occipital atypical choroid plexus papilloma of the right lateral ventricle at four months of age, which presumably altered the visual pathways during in utero development. Both the tumor and surgery severely compromised the optic radiations. Residual vision of G.S. was tested psychophysically when the patient was 7 years old. We found a close-to-normal visual acuity and contrast sensitivity within the central 25° and a great impairment in form and contrast vision in the far periphery (40-50°) of the left visual hemifield. BOLD response to full field luminance flicker was recorded from the primary visual cortex (V1) and in a region in the residual temporal-occipital region, presumably corresponding to the middle temporal complex (MT+), of the lesioned (right) hemisphere. A population receptive field analysis of the BOLD responses to contrast modulated stimuli revealed a retinotopic organization just for the MT+ region but not for the calcarine regions. Interestingly, consistent islands of ipsilateral activity were found in MT+ and in the parieto-occipital sulcus (POS) of the intact hemisphere. Probabilistic tractography revealed that optic radiations between LGN and V1 were very sparse in the lesioned hemisphere consistently with the post-surgery cerebral resection, while normal in the intact hemisphere. On the other hand, strong structural connections between MT+ and LGN were found in the lesioned hemisphere, while the equivalent tract in the spared hemisphere showed minimal structural connectivity. These results suggest that during development of the pathological brain, abnormal thalamic projections can lead to functional cortical changes, which may mediate functional recovery of vision.

Perception during double-step saccades.

How the visual system achieves perceptual stability across saccadic eye movements is a long-standing question in neuroscience. It has been proposed that an efference copy informs vision about upcoming saccades, and this might lead to shifting spatial coordinates and suppressing image motion. Here we ask whether these two aspects of visual stability are interdependent or may be dissociated under special conditions. We study a memory-guided double-step saccade task, where two saccades are executed in quick succession. Previous studies have led to the hypothesis that in this paradigm the two saccades are planned in parallel, with a single efference copy signal generated at the start of the double-step sequence, i.e. before the first saccade. In line with this hypothesis, we find that visual stability is impaired during the second saccade, which is consistent with (accurate) efference copy information being unavailable during the second saccade. However, we find that saccadic suppression is normal during the second saccade. Thus, the second saccade of a double-step sequence instantiates a dissociation between visual stability and saccadic suppression: stability is impaired even though suppression is strong.

Visual BOLD Response in Late Blind Subjects with Argus II Retinal Prosthesis.

Retinal prosthesis technologies require that the visual system downstream of the retinal circuitry be capable of transmitting and elaborating visual signals. We studied the capability of plastic remodeling in late blind subjects implanted with the Argus II Retinal Prosthesis with psychophysics and functional MRI (fMRI). After surgery, six out of seven retinitis pigmentosa (RP) blind subjects were able to detect high-contrast stimuli using the prosthetic implant. However, direction discrimination to contrast modulated stimuli remained at chance level in all of them. No subject showed any improvement of contrast sensitivity in either eye when not using the Argus II. Before the implant, the Blood Oxygenation Level Dependent (BOLD) activity in V1 and the lateral geniculate nucleus (LGN) was very weak or absent. Surprisingly, after prolonged use of Argus II, BOLD responses to visual input were enhanced. This is, to our knowledge, the first study tracking the neural changes of visual areas in patients after retinal implant, revealing a capacity to respond to restored visual input even after years of deprivation.

Effects of adaptation on numerosity decoding in the human brain.

Psychophysical studies have shown that numerosity is a sensory attribute susceptible to adaptation. Neuroimaging studies have reported that, at least for relatively low numbers, numerosity can be accurately discriminated in the intra-parietal sulcus. Here we developed a novel rapid adaptation paradigm where adapting and test stimuli are separated by pauses sufficient to dissociate their BOLD activity. We used multivariate pattern recognition to classify brain activity evoked by non-symbolic numbers over a wide range (20-80), both before and after psychophysical adaptation to the highest numerosity. Adaptation caused underestimation of all lower numerosities, and decreased slightly the average BOLD responses in V1 and IPS. Using support vector machine, we showed that the BOLD response of IPS, but not in V1, classified numerosity well, both when tested before and after adaptation. However, there was no transfer from training pre-adaptation responses to testing post-adaptation, and vice versa, indicating that adaptation changes the neuronal representation of the numerosity. Interestingly, decoding was more accurate after adaptation, and the amount of improvement correlated with the amount of perceptual underestimation of numerosity across subjects. These results suggest that numerosity adaptation acts directly on IPS, rather than indirectly via other low-level stimulus parameters analysis, and that adaptation improves the capacity to discriminate numerosity.

A low-cost and versatile system for projecting wide-field visual stimuli within fMRI scanners.

We have constructed and tested a custom-made magnetic-imaging-compatible visual projection system designed to project on a very wide visual field (~80°). A standard projector was modified with a coupling lens, projecting images into the termination of an image fiber. The other termination of the fiber was placed in the 3-T scanner room with a projection lens, which projected the images relayed by the fiber onto a screen over the head coil, viewed by a participant wearing magnifying goggles. To validate the system, wide-field stimuli were presented in order to identify retinotopic visual areas. The results showed that this low-cost and versatile optical system may be a valuable tool to map visual areas in the brain that process peripheral receptive fields.

BOLD human responses to chromatic spatial features.

Animal physiological and human psychophysical studies suggest that an early step in visual processing involves the detection and identification of features such as lines and edges, by neural mechanisms with even- and odd-symmetric receptive fields. Functional imaging studies also demonstrate mechanisms with even- and odd-receptive fields in early visual areas, in response to luminance-modulated stimuli. In this study we measured fMRI BOLD responses to 2-D stimuli composed of only even or only odd symmetric features, and to an amplitude-matched random noise control, modulated in red-green equiluminant colour contrast. All these stimuli had identical power but different phase spectra, either highly congruent (even or odd symmetry stimuli) or random (noise). At equiluminance, V1 BOLD activity showed no preference between congruent- and random-phase stimuli, as well as no preference between even and odd symmetric stimuli. Areas higher in the visual hierarchy, both along the dorsal pathway (caudal part of the intraparietal sulcus, dorsal LO and V3A) and the ventral pathway (V4), responded preferentially to odd symmetry over even symmetry stimuli, and to congruent over random phase stimuli. Interestingly, V1 showed an equal increase in BOLD activity at each alternation between stimuli of different symmetry, suggesting the existence of specialised mechanisms for the detection of edges and lines such as even- and odd-chromatic receptive fields. Overall the results indicate a high selectivity of colour-selective neurons to spatial phase along both the dorsal and the ventral pathways in humans.

The lowest spatial frequency channel determines brightness perception.

This study investigates the role played by individual spatial scales in determining the apparent brightness of greyscale patterns. We measured the perceived difference in brightness across an edge in the presence of notch filtering and high-pass filtering for two stimulus configurations, one that elicits the perception of transparency and one that appears opaque. For both stimulus configurations, the apparent brightness of the surfaces delimited by the border decreased monotonically with progressive (ideal) high-pass filtering, with a critical cut-off at 1 c/deg. Using two octave ideal notch filtering, the maximum detrimental effect on apparent brightness was observed at about 1c/deg. Critical frequencies for apparent brightness did not vary with contrast, viewing distance, or surface size, suggesting that apparent brightness is determined by the channel tuned at 1 c/deg. Modelling the data with the local energy model [Morrone, M. C., & Burr, D. C. (1988). Feature detection in human vision: a phase dependent energy model. Proceedings of the Royal Society (London), B235, 221-245] at 1c/deg confirmed the suggestion that this channel mediates apparent brightness for both opaque and transparent borders, with no need for pooling or integration across spatial channels.

Different attentional resources modulate the gain mechanisms for color and luminance contrast.

We used an interference paradigm to investigate whether attention is attribute-specific at early levels of visual processing. We show that the peripheral increment thresholds for luminance contrast deteriorate when the observer is currently performing another luminance (form or contrast) discrimination task in central view, but not when he or she is performing a color discrimination task. Similar results were obtained for color increment thresholds, indicating that the interference is specific to contrast modality. The effects are strong and robust over primary task difficulties and perceptual learning levels. Modeling suggests that attention improves contrast sensitivity by modulating the gain of the neuronal response to contrast. These results suggest that attention is parceled in independent resources for luminance and color contrast.

Automatic gain control contrast mechanisms are modulated by attention in humans: evidence from visual evoked potentials.

This study investigated the effect of attention on the contrast response curves of steady-state visual evoked potentials (VEPs) to counter-phased sinusoidal gratings. The 1 cyc/deg gratings were modulated either in luminance or chromaticity (equiluminant red-green). The luminance grating counter-phased at 9 Hz (to favour activation of the magno-cellular system), and the chromatic grating at 2.5 Hz (to favour activation of the parvo-cellular system). Attention was directed towards the gratings (displayed in the left visual field) by requiring subjects to detect and respond to randomly occurring changes in contrast. In the control condition, attention towards the grating was minimised by requiring subjects to detect a target letter amongst distracters briefly flashed in the contra-lateral visual field. Attention increased VEP amplitudes for both luminance and chromatic stimuli, more so at high than at low contrasts, increasing the slope of the contrast amplitude curves (over the non-saturating range of contrasts). The estimates of contrast threshold from extrapolation of amplitudes were unaffected by attention. Attention also changed the VEP phases, but only for luminance gratings, where it acted to reduce the magnitude of phase advance with contrast. Attention had no effect on the average phases for chromatic gratings. The results are consistent with the notion that attention acts on cortical gain control mechanisms, which are known to be different for the magno- and parvo-cellular systems.

Separate visual representations for perception and action revealed by saccadic eye movements.

Some 30 years ago, Trevarthen [1] introduced the idea of two separate visual systems, a focal system for fine motor acts and an ambient system for gross body movements such as ambulation. More recent developments indicating anatomically and physiologically separate pathways in primate vision [2] have led to a different idea of separate visual systems, one for conscious perception and one for action [3]. It has received empirical support from several studies showing that pointing, reaching, and grasping can remain accurate while the perceived position or size of objects is subject to illusory distortion [4-6]. However, much of this evidence has been challenged on the grounds of methodological flaws, particularly failure to match perfectly the conditions for verbal and motor tasks and failure to replicate results [7-10]. Here we take advantage of the strong compression of perceived position that occurs around the time of saccadic eye movements [11, 12]. Under normal lighting conditions, stimuli flashed briefly over a wide range of spatial positions just before saccadic onset are neither seen nor reached for in their veridical positions, but are compressed toward the saccadic target. We validate the idea of separate systems by showing that, in the dark, subjects are able to point accurately to the correct target position, even though their verbal reports are still subject to compression.

Changes in visual perception at the time of saccades.

We frequently reposition our gaze by making rapid ballistic eye movements that are called saccades. Saccades pose problems for the visual system, because they generate rapid, large-field motion on the retina and change the relationship between the object position in external space and the image position on the retina. The brain must ignore the one and compensate for the other. Much progress has been made in recent years in understanding the effects of saccades on visual function and elucidating the mechanisms responsible for them. Evidence suggests that saccades trigger two distinct neural processes: (1) a suppression of visual sensitivity, specific to the magnocellular pathway, that dampens the sensation of motion and (2) a gross perceptual distortion of visual space in anticipation of the repositioning of gaze. Neurophysiological findings from several laboratories are beginning to identify the neural substrates involved in these effects.

A cortical area that responds specifically to optic flow, revealed by fMRI.

The continuously changing optic flow on the retina provides information about direction of heading and about the three-dimensional structure of the environment. Here we use functional magnetic resonance imaging (fMRI) to demonstrate that an area in human cortex responds selectively to components of optic flow, such as circular and radial motion. This area is within the region commonly referrred to as V5/MT complex, but is distinct from the part of this region that responds to translation. The functional properties of these two areas of the V5/MT complex are also different; the response to optic flow was obtained only with changing flow stimuli, whereas response to translation occurred during exposure to continuous motion.

Extraretinal control of saccadic suppression.

We measured the time course of saccadic suppression and tested whether suppression results entirely from retinal image motion or has an extraretinal source. We measured contrast thresholds for low-frequency gratings modulated either in luminance, at 17 cd/m(2) and 0.17 cd/m(2), or color at 17 cd/m(2). Gratings were flashed on a uniform background before, during, or after voluntary 12 degrees saccades and, additionally in the case of luminance modulated gratings, saccades simulated by mirror motion. A 10-fold decrease in contrast sensitivity was found for luminance-modulated gratings with saccades, but little suppression was found with simulated saccades. Adding high-contrast noise to the display increased the magnitude and the duration of the suppression during simulated saccades but had little effect on suppression produced by real saccades. Suppression anticipates saccades by 50 msec, is maximal at the moment of saccadic onset, and outlasts saccades by approximately 50 msec. At lower luminance, suppression is reduced, and its course is shallower than at higher luminance. Simulated saccades produce shallower suppression over a longer time course at both luminances. No suppression was found for chromatically modulated gratings. Differences between real and simulated saccades in the magnitude and time course of sensitivity loss suggest that saccadic suppression has an extraretinal component. We model the effects of saccades by adding a signal to the visual input, so as to saturate the nonlinear stage of visual processing and make detection of a test stimulus more difficult.

Developmental changes in optokinetic mechanisms in the absence of unilateral cortical control.

Animal models suggest that the asymmetry of monocular optokinetic nystagmus (OKN) in young infants can be explained by a direct pathway from retina to the midbrain nucleus of the optic tract. However, earlier studies with hemispherectomized infants showed no evidence for OKN responses towards the damaged cortex that could be ascribed to this subcortical pathway. In longitudinal testing of two infants with very extensive unilateral cortical damage, we have now shown that OKN responses in both directions do occur before 10 months of age. OKN towards the damaged cortex, indicating functioning of the direct pathways in the absence of cortical control, drops out in the later development. The neural circuitry responsible for OKN in humans appears to undergo a plastic reorganization.

Saccadic suppression precedes visual motion analysis.

There is now good evidence that perception of motion is strongly suppressed during saccades (rapid shifts of gaze), presumably to blunt the disturbing sense of motion that saccades would otherwise elicit. Other aspects of vision, such as contrast detection of high-frequency or equiluminant gratings, are virtually unaffected by saccades [1] [2] [3] [4] [5]. This has led to the suggestion that saccades may suppress selectively the magnocellular pathway (which is strongly implicated in motion perception), leaving the parvocellular pathway unaffected [5] [6]. Here, we investigate the neural level at which perception of motion is suppressed. We used a simple technique in which an impression of motion is generated from only two frames, allowing precise control over the stimulus [7] [8]. One frame has a certain fixed contrast, whereas the contrast of the other (the test frame) is varied to determine the threshold for motion discrimination (that is, the lowest test-frame contrast level at which the direction of motion can be correctly guessed). Contrast thresholds of the test depended strongly and non-monotonically on the contrast of the fixed-contrast frame, with a minimum at medium contrast. To study the effect of saccadic suppression, we triggered the two-frame sequence by a voluntary saccade. Thresholds during saccades increased in a way that suggested that saccadic suppression precedes motion analysis: when the test frame was first in the motion sequence there was a general depression of sensitivity, whereas when it was second, the contrast response curve was shifted to a higher contrast range, sometimes even resulting in higher sensitivity than without a saccade. The dependence on presentation order suggests that saccadic suppression occurs at an early stage of visual processing, on the single frames themselves rather than on the combined motion signal. As motion detection itself is thought to occur at an early stage, saccadic suppression must take place at a very early phenomenon.

Cardinal directions for visual optic flow.

As we move through our environment, the flow of deforming images on the retinae provides a rich source of information about the three-dimensional structure of the external world and how to navigate through it. Recent evidence from psychophysical [1] [2] [3] [4], electrophysiological [5] [6] [7] [8] [9] and imaging [10] [11] studies suggests that there are neurons in the primate visual system - in the medial superior temporal cortex - that are specialised to respond to this type of complex 'optic flow' motion. In principle, optic flow could be encoded by a small number of neural mechanisms tuned to 'cardinal directions', including radial and circular motion [12] [13]. There is little support for this idea at present, however, from either physiological [6] [7] or psychophysical [14] research. We have measured the sensitivity of human subjects for detection of motion and for discrimination of motion direction over a wide and densely sampled range of complex motions. Average sensitivity was higher for inward and outward radial movement and for both directions of rotation, consistent with the existence of detectors tuned to these four types of motion. Principle component analysis revealed two clear components, one for radial stimuli (outward and inward) and the other for circular stimuli (clockwise and counter-clock-wise). The results imply that the mechanisms that analyse optic flow in humans tend to be tuned to the cardinal axes of radial and rotational motion.

The effects of ageing on reaction times to motion onset.

We have measured reaction time (RT) to motion onset in two groups of subjects (average ages: 70 and 29 years), for horizontal gratings of 1 c deg-1, modulated in either luminance or colour (equiluminant red-green), for various contrasts and speeds. For both old and young subjects, RTs depended on both speed and contrast, being faster at high speeds and high contrasts, and showed a stronger contrast dependency for chromatic gratings. The older subjects were systematically slower than the younger subjects. The difference between old and young RTs varied with condition, being 30-40 ms more at the slow than at the fast speed. The relative difference in RTs in different stimulus conditions shows that at least some of the increase in response time with age has a sensory origin. The results relate well to previous work on visual evoked potentials.

Large receptive fields for optic flow detection in humans.

We used a psychophysical summation technique to study the properties of detectors tuned to radial, circular and translational motion, and to determine the spatial extent of their receptive fields. Signal-to-noise motion thresholds were measured for patterns curtailed spatially in various ways. Sensitivity for radial, circular and translational motion increased with stimulus area at a rate predicted by an ideal integrator. When sectors of noise were added to the stimulus, sensitivity decreased at a rate consistent with an ideal integrator. Summation was tested for large annular stimuli, and shown to hold up to 70 degrees in some cases, suggesting very large receptive fields for this type of motion (consistent with the physiology of neurones in the dorsal region of the medial superior temporal area (MSTd)). This is a far greater area than observed for summation of contrast sensitivity to gratings (Anderson SJ and Burr DC, Vis Res 1987;29:621-635, and to this type of stimuli (Morrone MC, Burr DC and Vaina LM, Nature 1995;376:507-509, consistent with the suggestion that the two techniques examine different levels of motion analysis.

Seeing biological motion.

One of the more stunning examples of the resourcefulness of human vision is the ability to see 'biological motion', which was first shown with an adaptation of earlier cinematic work: illumination of only the joints of a walking person is enough to convey a vivid, compelling impression of human animation, although the percept collapses to a jumble of meaningless lights when the walker stands still. The information is sufficient to discriminate the sex and other details of the walker, and can be interpreted by young infants. Here we measure the ability of the visual system to integrate this type of motion information over space and time, and compare this capacity with that for viewing simple translational motion. Sensitivity to biological motion increases rapidly with the number of illuminated joints, far more rapidly than for simple motion. Furthermore, this information is summed over extended temporal intervals of up to 3 seconds (eight times longer than for simple motion). The steepness of the summation curves indicates that the mechanisms that analyse biological motion do not integrate linearly over space and time with constant efficiency, as may occur for other forms of complex motion, but instead adapt to the nature of the stimulus.

Motion analysis by feature tracking.

We have developed a two-stage model of motion perception that identifies moving spatial features and computes their velocity, achieving both high spatial localisation and reliable estimates of velocity. Features are detected in each frame by locating the peaks of the spatial local energy functions, as for stationary images (Morrone MC and Burr DC. Proc R Soc Lond 1988;B235:221-245.). The energy functions are calculated for different scales and orientations, and integrated within a temporal Gaussian window. The velocity of features is determined by the direction of maximal elongation of the energy in space-time, evaluated by calculating the three characteristic curvatures of the energy at each feature point. To circumvent the aperture problem, the energy maps are blurred in space by various amounts, and velocity is computed separately for each spatial blur. The Weber fraction of the local curvatures (curvature contrast) describes the spatio-temporal energy elongation at each feature point, giving a reliability index for each velocity estimate. For each point, the velocity of the spatial blur that yielded the highest curvature contrast was selected, with no further constraints, such as rigidity of motion. Dynamic recruitment of operators of different size allows maximum flexibility of the analysis, allowing it to simulate human visual performance in the detection of noise images, transparent motion, some motion illusions, and second-order motion.