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B G Cumming

Publications and source records attributed to B G Cumming.

At least 19 recordsLinked to original sources

Comparing perceptual signals of single V5/MT neurons in two binocular depth tasks.

Neurons in the extrastriate visual area V5/MT show perceptually relevant signals in binocular depth tasks, which can be measured as a choice probability (CP) for the neuron. The presence of a CP in a particular paradigm may be an indicator that the neuron is generally part of the substrate for the perception of binocular depth. We compared the responses of those single neurons that show CPs in one stereoscopic depth task with their responses in another stereo task. Each neuron was tested for the presence of 1) CPs during a task in which macaques responded to the sign of binocular depth in a structure-from-motion stimulus, to judge its direction of three-dimensional rotation and 2) a consistent response to the stereo disparity of binocularly anti-correlated stimuli. Previous work, confirmed here, shows that changing the disparity of these binocularly anti-correlated stimuli often fails to yield a coherent change in the depth percept. For each test alone, there are V5/MT neurons that carry signals that are congruent with the perceptual effects. However, on comparing tests, there is no fixed pool of neurons that can account for the binocular depth percept. Excitation of neurons with a measurable CP does not necessarily lead to a change in perception. The cortical circuitry must be able to make dynamic changes in the pools of neurons that underlie perceptual judgments according to the demands of the task.

Action Potentials↗

An unexpected specialization for horizontal disparity in primate primary visual cortex.

The horizontal separation of the eyes means that objects nearer or farther than the fixation point project to different locations on the two retinae, differing principally in their horizontal coordinates (horizontal binocular disparity). Disparity-selective neurons have generally been studied with disparities applied in only one direction (often horizontal), which cannot determine whether the encoding is specialized for processing disparities along the horizontal axis. It is therefore unclear if disparity selectivity represents a specialization for naturally occurring disparities. I used random dot stereograms to study disparity-selective neurons from the primary visual cortex (V1) of awake fixating monkeys. Many combinations of vertical and horizontal disparity were used, characterizing the surface of responses as a function of two-dimensional disparity. Here I report that the response surface usually showed elongation along the horizontal disparity axis, despite the isotropic stimulus. Thus these neurons modulated their firing rate over a wider range of horizontal disparity than vertical disparity. This demonstrates that disparity-selective cells are specialized for processing horizontal disparity, and that existing models of disparity selectivity require substantial revision.

Action Potentials↗

A specialization for relative disparity in V2.

Stereoscopic depth perception relies on binocular disparities, or small geometric differences between the retinal images of each eye. The most reliable binocular depth judgments are those that are based on relative disparities between two simultaneously visible features in a scene. Many cortical areas contain neurons that are sensitive to disparity, but it is unclear whether any areas show a specific sensitivity to relative disparity. We recorded from neurons in the early cortical visual area V2 of the awake macaque during presentation of random-dot patterns. The depth of a central region ('center'), and that of an annular surrounding region ('surround'), were manipulated independently in these stimuli. Some cells were fully selective for the resulting relative disparities. Most showed partial selectivity, which nonetheless indicated a sensitivity for the depth relationship between center and surround. Both types of neural response could support psychophysical judgments of relative depth.

Animals↗

Quantitative analysis of the responses of V1 neurons to horizontal disparity in dynamic random-dot stereograms.

Horizontal disparity tuning for dynamic random-dot stereograms was investigated for a large population of neurons (n = 787) in V1 of the awake macaque. Disparity sensitivity was quantified using a measure of the discriminability of the maximum and minimum points on the disparity tuning curve. This measure and others revealed a continuum of selectivity rather than separate populations of disparity- and nondisparity-sensitive neurons. Although disparity sensitivity was correlated with the degree of direction tuning, it was not correlated with other significant neuronal properties, including preferred orientation and ocular dominance. In accordance with the Gabor energy model, tuning curves for horizontal disparity were adequately described by Gabor functions when the neuron's orientation preference was near vertical. For neurons with orientation preferences near to horizontal, a Gaussian function was more frequently sufficient. The spatial frequency of the Gabor function that described the disparity tuning was weakly correlated with measurements of the spatial frequency and orientation preference of the neuron for drifting sinusoidal gratings. Energy models make several predictions about the relationship between the response rates to monocular and binocular dot patterns. Few of the predictions were fulfilled exactly, although the observations can be reconciled with the energy model by simple modifications. These same modifications also provide an account of the observed continuum in strength of disparity selectivity. A weak correlation between the disparity sensitivity of simultaneously recorded single- and multiunit data were revealed as well as a weak tendency to show similar disparity preferences. This is compatible with a degree of local clustering for disparity sensitivity in V1, although this is much weaker than that reported in area MT.

Animals↗

Range and mechanism of encoding of horizontal disparity in macaque V1.

The responses of single cortical neurons were measured as a function of the binocular disparity of dynamic random dot stereograms for a large sample of neurons (n = 787) from V1 of the awake macaque. From this sample, we selected 180 neurons whose tuning curves were strongly tuned for disparity, well sampled and well described by one-dimensional Gabor functions. The fitted parameters of the Gabor functions were used to resolve three outstanding issues in binocular stereopsis. First, we considered whether tuning curves can be meaningfully divided into discrete tuning types. Careful examination of the distributions of the Gabor parameters that determine tuning shape revealed no evidence for clustering. We conclude that a continuum of tuning types is present. Second, we investigated the mechanism of disparity encoding for V1 neurons. The shape of the disparity tuning function can be used to distinguish between position-encoding (in which disparity is encoded by an interocular shift in receptive field position) and phase-encoding (in which disparity is encoded by a difference in the receptive field profile in the 2 eyes). Both position and phase encoding were found to be common. This was confirmed by an independent assessment of disparity encoding based on the measurement of disparity sensitivity for sinusoidal luminance gratings of different spatial frequencies. The contributions of phase and position to disparity encoding were compared by estimating a population average of the rate of change in firing rate per degree of disparity. When this was calculated separately for the phase and position contributions, they were found to be closely similar. Third, we investigated the range of disparity tuning in V1 as a function of eccentricity in the parafoveal range. We find few cells which are selective for disparities greater than +/-1 degrees even at the largest eccentricity of approximately 5 degrees. The preferred disparity was correlated with the spatial scale of the tuning curve, and for most units lay within a +/-pi radians phase limit. Such a size-disparity correlation is potentially useful for the solution of the correspondence problem.

Animals↗

Responses of macaque V1 neurons to binocular orientation differences.

Interocular differences in orientation occur during binocular viewing of a surface slanted in depth. These orientation disparities could be exploited by the visual system to provide information about surface slant, but gradients of positional disparity provide an equally effective means to the same end. We examined the encoding of orientation disparities in V1 neurons that were recorded from two awake fixating monkeys. Monocular orientation selectivity was measured separately in each eye. Although the preferred monocular orientation in the left and right eyes was highly correlated (r = 0.98), 19 of 61 cells showed a significant interocular difference in preferred orientation (IDPO). By itself, an IDPO does not imply a specific binocular selectivity for orientation differences. We therefore examined the response to 25 binocular combinations of orientations by pairing each of five orientations in one eye with five in the other. Forty-four of 64 neurons showed responses that reflected the monocular orientation tuning selectivity; the preferred orientation disparity changed when the monocular orientation was changed in either eye. The remaining third (20 of 64) responded to a consistent orientation disparity in a way that was not simply predictable from monocular orientation selectivity. However, nearly all of these neurons were selective for positional disparity, and several characteristics of the responses suggest that the apparent selectivity for orientation disparities was just a consequence of the positional disparity sensitivity. Neither the data presented here nor previous data from the cat (Blakemore et al., 1972; Nelson et al., 1977) support the idea that a population of neurons early in the visual system has a separate encoding scheme for orientation disparities.

Action Potentials↗

Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT.

The role of the primate middle temporal area (MT) in depth perception was examined by considering the trial-to-trial correlations between neuronal activity and reported depth sensations. A set of moving random dots portrayed a cylinder rotating about its principal axis. In this structure-from-motion stimulus, the direction of rotation is ambiguous and the resulting percept undergoes spontaneous fluctuations. The stimulus can be rendered unambiguous by the addition of binocular disparities. We trained monkeys to report the direction of rotation in a set of these stimuli, one of which had zero disparity. Many disparity-selective neurons in area MT are selective for the direction of rotation defined by disparity. Across repeated presentations of the ambiguous (zero-disparity) stimulus, there was a correlation between neuronal firing and the reported direction of rotation, as found by Bradley et al. (1998). Quantification of this effect using choice probabilities (Britten et al., 1996) allowed us to demonstrate that the correlation cannot be explained by eye movements, behavioral biases, or attention to spatial location. MT neurons therefore appear to be involved in the perceptual decision process. The mean choice probability (0.67) was substantially larger than that reported for MT neurons in a direction discrimination task (Britten et al., 1996). This implies that MT neurons make a different contribution to the two tasks. For the depth task, either the pool of neurons used is smaller or the correlation between neurons in the pool is larger.

Action Potentials↗

Cortical mechanisms of binocular stereoscopic vision.

The early neurophysiology of binocular vision is largely dominated by measurements of disparity selectivity in cortical neurons in various visual areas. Incisive progress has been made by the intensive study of the mechanism of disparity selectivity of V1 in cortical neurons and the development of a number of tests for the involvement of single neurons in the perception of stereoscopic depth. The picture that now emerges is that cortical area V1 must be a preliminary processing stage for the analysis of stereoscopic depth, whereas some of the extrastriate areas may actually be responsible for the generation of neuronal signals that underlie the perception of binocular depth.

Animals↗

The integration of orientation information in the motion correspondence problem.

We examine how differently oriented components contribute to the discrimination of motion direction along a horizontal axis. Stimuli were two-frame random-dot kinematograms that were narrowband filtered in spatial frequency. On each trial, subjects had to state whether motion was to the left or the right. For each stimulus condition, Dmax (the largest displacement supporting 80% correct direction discrimination performance) was measured. In experiment 1, Dmax was measured for orientationally narrowband stimuli as a function of their mean orientation. Dmax was found to increase as the orientation of the stimuli became closer to the axis of motion. Experiment 2 used isotropic stimuli in which some orientation bands contained a coherent motion signal, and some contained only noise. When the noise band started at vertical orientations and increased until only horizontal orientations contained a coherent motion signal, Dmax increased slightly. This suggests that near-vertical orientations interfere with motion perception at large displacements when they contain a coherent motion signal. When the noise band started at horizontal and increased until only vertical orientations contained the motion signal, Dmax decreased steadily. This implies that Dmax depends at least partly on the most horizontal motion signal in the stimulus. These results were contrasted with two models. In the first, the visual system utilises the most informative orientations (nearest horizontal). In the second, all available orientations are used equally. Results supported an intermediate interpretation, in which all orientations are used but more informative ones are weighted more heavily.

Discrimination, Psychological↗

The physiology of stereopsis.

Binocular disparity provides the visual system with information concerning the three-dimensional layout of the environment. Recent physiological studies in the primary visual cortex provide a successful account of the mechanisms by which single neurons are able to signal disparity. This work also reveals that additional processing is required to make explicit the types of signal required for depth perception (such as the ability to match features correctly between the two monocular images). Some of these signals, such as those encoding relative disparity, are found in extrastriate cortex. Several other lines of evidence also suggest that the link between perception and neuronal activity is stronger in extrastriate cortex (especially MT) than in the primary visual cortex.

Animals↗

Local disparity not perceived depth is signaled by binocular neurons in cortical area V1 of the Macaque.

Binocular neurons that are closely related to depth perception should respond selectively for stimuli eliciting an appropriate depth sensation. To separate perceived depth from local disparity within the receptive field, sinusoidal luminance gratings were presented within a circular aperture. The disparity of the aperture was coupled to that of the grating, thereby rendering unambiguous the psychophysical matching between repeating cycles of the grating. In cases in which the stimulus disparity differs by one horizontal period of the grating, the portion of the grating that locally covers a receptive field is binocularly identical, but the depth sensation is very different because of the aperture. For 117 disparity-selective V1 neurons tested in two monkeys, the overwhelming majority responded equally well to configurations that were locally identical but led to different perceptions of depth. Because the psychophysical sensation is not reflected in the firing rate of V1 neurons, the signals that make stereo matches explicit are most likely elaborated in extrastriate cortex.

Animals↗

The precision of single neuron responses in cortical area V1 during stereoscopic depth judgments.

The performance of single neurons in cortical area V1 of alert macaque monkeys was compared against the animals' psychophysical performance during a binocular disparity discrimination task. Performance was assessed with stimuli that consisted of a patch of dynamic random dots, whose disparity varied from trial to trial, surrounded by an annulus of similar dots at a fixed disparity. On each trial, the animals indicated whether the depth of the central patch was in front of or behind the annulus. For each disparity of the center patch, neural performance was assessed by calculating the probability that the response of the neuron was greater or less than the response when the center disparity was the same as that of the annulus. Initially the animals performed the task simultaneously with the neural recording. However, the range of disparities used, which was appropriate for the neuronal recording, may have affected performance, because the thresholds were substantially lower (2.6x) when the psychophysical measurements were repeated later. Average neuronal thresholds were approximately 4x poorer than these behavioral thresholds, although the best neurons were marginally better than the animals' behavior. Thus, the well known precision of relative depth judgments can be supported with signals from a small number of V1 neurons. Interference with the relative depth information in the stimulus profoundly affected behavioral thresholds, which were approximately 10x poorer when the surround was absent or contained binocularly uncorrelated dots. In this case, single V1 neurons consistently outperform the observer: presumably here, psychophysical thresholds are limited by other factors (such as uncertainty about vergence eye position).

Animals↗

Binocular neurons in V1 of awake monkeys are selective for absolute, not relative, disparity.

Most neurophysiological accounts of disparity selectivity in neurons of the primary visual cortex (V1) imply that they are selective for absolute retinal disparities. By contrast, a number of psychophysical observations indicate that relative disparities play a more important role in depth perception. During recordings from disparity selective neurons in area V1 of awake behaving monkeys, we used a disparity feedback loop () to add controlled amounts of absolute disparity to a display containing both absolute and relative disparities. This manipulation changed the absolute disparity of all the visible features in the display but left unchanged the relative disparities signalled by these features. The addition of absolute disparities produced clear changes in the neural responses to unchanged external stimuli, which were well predicted by the measured change in absolute disparity: in 45/53 cases, the neuron maintained a consistent firing pattern with respect to absolute disparity so that the manipulation created no significant change in the absolute disparity preferred by the neuron. No neuron in V1 maintained a consistent relationship with relative disparity. We conclude that the relative disparity signals used in primate depth perception are constructed outside area V1.

Action Potentials↗

Cortical area MT and the perception of stereoscopic depth.

Stereopsis is the perception of depth based on small positional differences between images formed on the two retinae (known as binocular disparity). Neurons that respond selectively to binocular disparity were first described three decades ago, and have since been observed in many visual areas of the primate brain, including V1, V2, V3, MT and MST. Although disparity-selective neurons are thought to form the neural substrate for stereopsis, the mere existence of disparity-selective neurons does not guarantee that they contribute to stereoscopic depth perception. Some disparity-selective neurons may play other roles, such as guiding vergence eye movements. Thus, the roles of different visual areas in stereopsis remain poorly defined. Here we show that visual area MT is important in stereoscopic vision: electrical stimulation of clusters of disparity-selective MT neurons can bias perceptual judgements of depth, and the bias is predictable from the disparity preference of neurons at the stimulation site. These results show that behaviourally relevant signals concerning stereoscopic depth are present in MT.

Animals↗

Disparity detection in anticorrelated stereograms.

Recent physiological observations in which stimuli with opposite contrast signs in the two eyes have been used (anticorrelated stereograms) show that these stimuli evoke responses in primary visual cortex which are the reverse of responses to correlated stimuli. Psychophysical investigations reveal no such reversals: reversed-contrast bars with crossed disparities are seen in front of those with uncrossed disparities. For anticorrelated random-dot stereograms human subjects perceive no depth at all, except at low dot densities. However, these human studies were carried out with stimuli that differed in several ways from those used in physiological studies. We therefore reexamined psychophysical responses using stimuli similar to those used for physiological recordings. Our results confirm the previous findings: there is no evidence of a reversed depth sensation for bar stereograms (crossed disparities are never seen behind uncrossed disparities), and subjects are unable to detect depth in anticorrelated random-dot stereograms at the densities used for the physiological recordings. The discrepancy between the psychophysical data and the responses of single neurons in primary visual cortex suggests that further processing outside area V1 is necessary to provide the signals that produce the sensation of stereoscopic depth.

Computer Graphics↗

The direction of retinal motion facilitates binocular stereopsis.

Visual information from binocular disparity and from relative motion provide information about three-dimensional structure and layout of the world. Although the mechanisms that process these cues have typically been studied independently, there is now a substantial body of evidence that suggests that they interact in the visual pathway. This paper investigates one advantage of such an interaction: whether retinal motion can be used as a matching constraint in the binocular correspondence process. Stimuli that contained identical disparity and motion signals but which differed in their fine-scale correlation were created to establish whether the direction, or the speed, of motion could enhance performance in a psychophysical task in which binocular matching is a limiting factor. The results of these experiments provide clear evidence that different directions of motion, but not different speeds, are processed separately in stereopsis. The results fit well with properties of neurons early in the cortical visual pathway which are thought to be involved in determining local matches between features in the two eyes' images.

Depth Perception↗

Responses of primary visual cortical neurons to binocular disparity without depth perception.

The identification of brain regions that are associated with the conscious perception of visual stimuli is a major goal in neuroscience. Here we present a test of whether the signals on neurons in cortical area V1 correspond directly to our conscious perception of binocular stereoscopic depth. Depth perception requires that image features on one retina are first matched with appropriate features on the other retina. The mechanisms that perform this matching can be examined by using random-dot stereograms, in which the left and right eyes view randomly positioned but binocularly correlated dots. We exploit the fact that anticorrelated random-dot stereograms (in which dots in one eye are matched geometrically to dots of the opposite contrast in the other eye) do not give rise to the perception of depth because the matching process does not find a consistent solution. Anti-correlated random-dot stereograms contain binocular features that could excite neurons that have not solved the correspondence problem. We demonstrate that disparity-selective neurons in V1 signal the disparity of anticorrelated random-dot stereograms, indicating that they do not unambiguously signal stereoscopic depth. Hence single V1 neurons cannot account for the conscious perception of stereopsis, although combining the outputs of many V1 neurons could solve the matching problem. The accompanying paper suggests an additional function for disparity signals from V1: they may be important for the rapid involuntary control of vergence eye movements (eye movements that bring the images on the two foveae into register).

Animals↗