Biomedical subjects

Bruce G Cumming

Publications and source records attributed to Bruce G Cumming.

14 recordsLinked to original sources

PubMed2006

Does depth perception require vertical-disparity detectors?

Stereo depth perception depends on the fact that objects project to different positions in the two eyes. Because our eyes are offset horizontally, these retinal disparities are mainly horizontal, and horizontal disparity suffices to give an impression of depth. However, depending on eye position, there may also be small vertical disparities. These are significant because, given both vertical and horizontal disparities, the brain can deduce eye position from purely retinal information and, hence, derive the position of objects in space. However, we show here that, to achieve this, the brain need measure only the magnitude of vertical disparity; for physically possible stimuli, the sign then follows from the stereo geometry. The magnitude of vertical disparity--and hence eye position--can be deduced from the response of purely horizontal-disparity sensors because vertical disparity moves corresponding features off the receptive fields, reducing the effective binocular correlation. As proof, we demonstrate an algorithm that can accurately reconstruct gaze and vergence angles from the population activity of pure horizontal-disparity sensors and show that it is subject to the induced effect. Given that disparities experienced during natural viewing are overwhelmingly horizontal and that eye position measures require only horizontal-disparity sensors, this work raises two questions: Does the brain in fact contain sensors tuned to nonzero vertical disparities, and if so, why?

Algorithms↗

PubMed2006

Macaque V2 neurons, but not V1 neurons, show choice-related activity.

In the macaque extrastriate cortex, robust correlations between perceptual choice and neuronal response have been demonstrated, frequently quantified as choice probabilities (CPs). Such correlations are modest in early visual cortex, suggesting that CPs may depend on the position of a neuron in the hierarchy of visual processing. However, previous studies have not compared neurons with similar precision in equivalent tasks. We investigated the role of cortical hierarchy on CP using a task for which significant CPs have been described previously for middle temporal area (MT). We measured CPs in disparity-selective neurons from both V1 and V2. The stimulus was a dynamic random dot stereogram, presented with a near or a far disparity, masked by varying numbers of binocularly uncorrelated dots. Two macaque monkeys reported whether they perceived a circular patch in front or behind a surrounding annulus in a forced choice task. For V2 (n = 69), CP was on average 0.56, the first demonstration of systematic CPs in a visual area as early as V2. In V1 (n = 74), average CP was at chance level (0.51). The pattern was similar in a subgroup of neurons selected such that the statistical precision in the task was on average identical to that reported for MT (mean CP, 0.51 for V1, n = 33; 0.58 for V2, n = 54). This difference between V1 and V2 could not be explained by eye movements, stimulus size relative to the receptive field, or differences in disparity tuning. Rather, it seems to reflect a functional difference (at least in disparity processing) between striate and extrastriate cortex.

Action Potentials↗

PubMed2006

A simple account of cyclopean edge responses in macaque v2.

It has been shown recently that neurons in V2 respond selectively to the edges of figures defined only by disparity (cyclopean edges). These responses are orientation selective, often preferring similar orientations for cyclopean and luminance contours, suggesting that they may support a cue-invariant representation of contours. Here, we investigate the extent to which processing of purely local visual information (in the vicinity of the receptive field) might explain such results, using the most impoverished stimulus possible containing a cyclopean edge (a circular patch of random dots divided into two regions by a single edge). Many V2 cells responded better to the cyclopean edge than to uniform disparities, and most of these were at least broadly selective for the orientation of the cyclopean edge. Two characteristics argue against a cue-invariant contour representation: (1) the cyclopean edge response was frequently abolished by small changes to the component disparities; and (2) although V2 cells frequently responded to both signs of a cyclopean edge (defined by which side of the edge is in front), they did so at different edge locations. These characteristics are consistent with a simple feedforward scheme in which V2 neurons receive inputs from several V1 subunits with different disparity selectivity. We also found a correlation between the preferred orientations for cyclopean edges and contrast stimuli, suggesting that this feedforward wiring is not random. These characteristics suggest that V2 responses to cyclopean edges may be useful in supporting a cue-invariant contour representation higher in the visual pathway.

Animals↗

PubMed2005

All Pulfrich-like illusions can be explained without joint encoding of motion and disparity.

In the Pulfrich effect, an interocular time delay results in the perception of depth. Two modified versions, the stroboscopic Pulfrich effect and dynamic visual noise with a delay, are generally explained by postulating an early stage of space/time-inseparable filtering, encoding motion and disparity jointly. However, most disparity sensors in monkey V1 do not show joint motion/disparity encoding, and we recently showed that depth perception in the stroboscopic Pulfrich effect is equally compatible with space/time-separable filtering. Here, we demonstrate that this filtering can be implemented with a population of physiologically plausible energy model units. Similar results are obtained whether the neurons are pure disparity sensors (like most V1 neurons) or joint motion/disparity sensors (like MT). We also demonstrate that the dynamic noise stimulus produces correlations between the activity in pure disparity sensors, and in a separate population of pure motion sensors. These correlations are sufficient to explain the percept. Thus, joint encoding of motion and disparity is not required to explain depth perception in Pulfrich-like stimuli: a brain which encoded motion and disparity in entirely separate neuronal pathways could still experience all of these illusions.

Animals↗

PubMed2005

Neuronal computation of disparity in V1 limits temporal resolution for detecting disparity modulation.

The human ability to detect modulation of binocular disparity over time is poor compared with detection of luminance modulation. We examined the physiological origin of this limitation by analyzing neuronal responses to temporal modulation of binocular disparity in striate cortex of awake monkeys. When neurons were presented with random-dot stereograms in which disparity varied sinusoidally over time, their responses modulated at the stimulus temporal frequency, with little change in mean firing rate. We calculated modulation amplitude as a function of temporal frequency and compared this with the psychophysical performance of four human observers. Neuronal and psychophysical functions showed similar peak frequencies (2 Hz) and comparable high-cut frequencies (10 and 5.5 Hz, respectively). Thus, V1 (primary visual cortex) neurons appear to limit psychophysical performance. The temporal resolution of the same neurons for contrast modulation was approximately 2.5 times greater, which parallels the superior psychophysical performance for contrast. There is a simple mathematical explanation for this difference: it results from calculating cross-correlation between temporally broadband monocular images that are bandpass filtered before measuring correlation. The limit on temporal resolution is a direct consequence of the binocular energy model that adds to the list of properties of human stereoscopic performance that are explained by this simple model of disparity encoding in V1: the same neurons can account for the performance of psychophysical tasks that result in either high (contrast) or low (disparity) temporal resolution. Because this principle holds whenever a broadband input is bandpass filtered before computing correlation, it may limit the resolution of other neuronal systems.

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PubMed2005

The stroboscopic Pulfrich effect is not evidence for the joint encoding of motion and depth.

In the Pulfrich effect, an illusion of depth is produced by introducing differences in the times at which a moving object is presented to the two eyes. In the classic form of the illusion, there is a simple explanation for the depth percept: the interocular delay introduces a spatial disparity into the stimulus. However, when the moving object is viewed stroboscopically, this simple explanation no longer holds. In recent years, depth perception in the stroboscopic Pulfrich effect has been explained by invoking neurons that are sensitive both to stereo disparity and to direction of motion. With such joint motion/disparity encoders, interocular delay causes a perception of depth by causing a shift in each neuron's preferred disparity. This model has been implemented by N. Qian and R. A. Andersen (1997). Here we show that this model's predictions for perceived disparity are quantitatively at odds with psychophysical measures. The joint-encoding model predicts that the perceived disparity is the virtual disparity implied by the apparent motion; in fact, the perceived disparity is smaller. We show that the percept can be quantitatively explained on the basis of spatial disparities present in the stimulus, which could be extracted from pure disparity sensors. These results suggest that joint encoding of motion and depth is not the dominant neuronal basis of depth perception in this stimulus.

Computer Simulation↗

PubMed2005

Effect of interocular delay on disparity-selective v1 neurons: relationship to stereoacuity and the pulfrich effect.

The temporal properties of disparity-sensitive neurons place important temporal constraints on stereo matching. We examined these constraints by measuring the responses of disparity-selective neurons in striate cortex of awake behaving monkeys to random-dot stereograms that contained interocular delays. Disparity selectivity was gradually abolished by increasing interocular delay (when the delay exceeds the integration time, the inputs from the 2 eyes become uncorrelated). The amplitude of the disparity-selective response was a Gaussian function of interocular delay, with a mean of 16 ms (+/-5 ms, SD). Psychophysical measures of stereoacuity, in both monkey and human observers, showed a closely similar dependency on time, suggesting that temporal integration in V1 neurons is what determines psychophysical matching constraints over time. There was a slight but consistent asymmetry in the neuronal responses, as if the optimum stimulus is one in which the right stimulus leads by about 4 ms. Because all recordings were made in the left hemisphere, this probably reflects nasotemporal differences in conduction times; psychophysical data are compatible with this interpretation. In only a few neurons (5/72), interocular delay caused a change in the preferred disparity. Such tilted disparity/delay profiles have been invoked previously to explain depth perception in the stroboscopic version of the Pulfrich effect (and other variants). However, the great majority of the neurons did not show tilted disparity/delay profiles. This suggests that either the activity of these neurons is ignored when viewing Pulfrich stimuli, or that current theories relating neuronal properties to perception in the Pulfrich effect need to be reevaluated.

Action Potentials↗

PubMed2004

Receptive field size in V1 neurons limits acuity for perceiving disparity modulation.

Disparity selectivity in the striate cortex has generally been studied with uniform disparity fields covering the receptive field (RF). In four awake behaving monkeys, we quantitatively characterized the spatial three-dimensional structure of 55 V1 RFs using random dot stereograms in which disparity varied as a sinusoidal function of vertical position ("corrugations"). At low spatial frequencies, this produced a modulation in neuronal firing at the temporal frequency of the stimulus. As the spatial frequency increased, the modulation reduced. The mean response rate changed little and was close to that produced by a uniform stimulus at the mean disparity of the corrugation. In 48 of 55 (91%) neurons, the modulation strength was a lowpass function of spatial frequency. These results are compatible with a response determined only by the weighted mean of the disparities of the dots (the weights being set by the RF envelope) and suggest that there is no disparity-based surround inhibition or selectivity for disparity gradients. This simple weighting scheme predicts a relationship between RF size and the high-frequency cutoff. Comparison with independent measurements of RF size was compatible with this. All of this behavior closely matches the binocular energy model. The mean cutoff frequency, 0.5 cycles per degree, is similar to equivalent measures of decline in human psychophysical sensitivity for such depth corrugations as a function of frequency (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004). This suggests that human cyclopean acuity for disparity modulations is limited by the selectivity of V1 neurons. This in turn is primarily limited by the RF size, because we find no sensitivity for disparity gradients or other disparity differences within the RFs.

Action Potentials↗

PubMed2004

Understanding the cortical specialization for horizontal disparity.

Because the eyes are displaced horizontally, binocular vision is inherently anisotropic. Recent experimental work has uncovered evidence of this anisotropy in primary visual cortex (V1): neurons respond over a wider range of horizontal than vertical disparity, regardless of their orientation tuning. This probably reflects the horizontally elongated distribution of two-dimensional disparity experienced by the visual system, but it conflicts with all existing models of disparity selectivity, in which the relative response range to vertical and horizontal disparities is determined by the preferred orientation. Potentially, this discrepancy could require us to abandon the widely held view that processing in V1 neurons is initially linear. Here, we show that these new experimental data can be reconciled with an initial linear stage; we present two physiologically plausible ways of extending existing models to achieve this. First, we allow neurons to receive input from multiple binocular subunits with different position disparities (previous models have assumed all subunits have identical position and phase disparity). Then we incorporate a form of divisive normalization, which has successfully explained many response properties of V1 neurons but has not previously been incorporated into a model of disparity selectivity. We show that either of these mechanisms decouples disparity tuning from orientation tuning and discuss how the models could be tested experimentally. This represents the first explanation of how the cortical specialization for horizontal disparity may be achieved.

Animals↗

PubMed2003

Ocular dominance predicts neither strength nor class of disparity selectivity with random-dot stimuli in primate V1.

We address two unresolved issues concerning the coding of binocular disparity in primary visual cortex. Experimental studies and theoretical models have suggested a relationship between a cell's ocular dominance, assessed with monocular stimuli, and its tuning to binocular disparity. First, the disparity energy model of disparity selectivity suggests that there should be a correlation between ocular dominance and the strength of disparity tuning. Second, several studies have reported a relationship between ocular dominance and the shape of the disparity tuning curve, with cells dominated by one eye more likely to have disparity tuning of the tuned-inhibitory type. We investigated both of these relationships in single neurons recorded from the primary visual cortex of awake fixating macaques, using dynamic random-dot patterns as a stimulus. To classify disparity tuning curves quantitatively, we develop a new measure of symmetry, which can be applied to any function. We find no evidence for any correlation between ocular dominance and the nature of disparity tuning. This places constraints on the circuitry underlying disparity tuning.

Algorithms↗

PubMed2003

Testing quantitative models of binocular disparity selectivity in primary visual cortex.

Disparity-selective neurons in striate cortex (V1) probably implement the initial processing that supports binocular vision. Recently, much progress has been made in understanding the computations that these neurons perform on retinal inputs. The binocular energy model has been highly successful in providing a simple theory of these computations. A key feature of the energy model is that it is linear until after inputs from the two eyes are combined. Recently, however, a modified version of the energy model, incorporating threshold nonlinearities before binocular combination, has been proposed to account for the weaker disparity tuning observed with anticorrelated stimuli. In this study, we present new data needed for a critical assessment of these two models. We compare two key predictions of the models with responses of disparity-selective neurons recorded from V1 of awake fixating monkeys. We find that the original energy model, and a family of generalizations retaining linear binocular combination, are quantitatively inconsistent with the response of V1 neurons. In contrast, the modified version incorporating threshold nonlinearities can explain both sets of observations. We conclude that the energy model can be reconciled with experimental observations by adding a threshold before binocular combination. This gives us the clearest picture yet of the computation being carried out by disparity-selective V1 neurons.

Action Potentials↗

PubMed2003

Measuring V1 receptive fields despite eye movements in awake monkeys.

One difficulty with measuring receptive fields in the awake monkey is that even well-trained animals make small eye movements during fixation. These complicate the measurement of receptive fields by blurring out the region where a response is observed, causing underestimates of the ability of individual neurons to signal changes in stimulus position. In simple cells, this blurring may severely disrupt estimates of receptive field structure. An accurate measurement of eye movements would allow correction of this blurring. Scleral search coils have been used to provide such measurements, although little is known about their accuracy. We have devised a range of approaches to address this issue: implanting two coils into a single eye, exploiting the small size of V1 receptive fields and developing maximum-likelihood fitting techniques to extract receptive field parameters in the presence of eye movements. All our investigations lead to the same conclusion: our scleral search coils (which were not sutured to the globe) are subject to an error of approximately the same magnitude as the small eye movements which occur during fixation: SD approximately 0.1 degrees. This error is large enough to explain the SD of measured vergence in the absence of any real changes in vergence state. This, and a variety of other arguments, indicate that the real variation in vergence is much smaller than coil measurements suggest. These results suggest that monkeys, like humans, maintain very stable vergence. The error has a slower time course than fixational eye movements so that search coils report the difference in eye position between two consecutive trials more accurately than the eye position itself on either trial. Receptive field estimates are unlikely to be improved by assuming the coil record is veridical and correcting for eye position accordingly. However, receptive field parameters can reliably be determined by a fitting technique that allows for eye movements. It is possible that suturing coils to the globe reduces the artifacts, but no method has been available to demonstrate this. These receptive field measurements provide a general means by which the reliability of eye-position measurements can be assessed.

Animals↗

PubMed2002

Neuronal activity and its links with the perception of multi-stable figures.

In order to isolate the neuronal activity that relates to the making of perceptual decisions, we have made use of a perceptually ambiguous motion stimulus. This stimulus lies on the boundary between two perceptual categories that correspond to clockwise and counter-clockwise rotation of a three-dimensional figure. It consists of a two-dimensional pattern of moving dots that are capable of generating these two, distinct, three-dimensional percepts. We have studied the responses of neurons in cortical area V5/MT whilst macaque monkeys report judgements about the perceptual configuration of this stimulus. We extract a quantitative statistic called 'choice probability' that expresses the covariation of neuronal activity and perceptual choice. An analysis of choice probabilities shows that the pool of neurons involved in the perceptual decisions is a tightly constrained subset of the population of sensory neurons relevant to the perceptual task.

Animals↗

PubMedDate not supplied

A simple model accounts for the response of disparity-tuned V1 neurons to anticorrelated images.

Disparity-tuned cells in primary visual cortex (VI) are thought to play a significant role in the processing of stereoscopic depth. The disparity-specific responses of these neurons have been previously described by an energy model based on local, feedforward interactions. This model fails to predict the response to binocularly anticorrelated stimuli, in which images presented to left and right eyes have opposite contrasts. The original energy model predicts that anticorrelation should invert the disparity tuning curve (phase difference pi), with no change in the amplitude of the response. Experimentally, the amplitude tends to be reduced with anticorrelated stimuli and a spread of phase differences is observed, although phase differences near pi are the most common. These experimental observations could potentially reflect a modulation of the V1 signals by feedback from higher visual areas (because anticorrelated stimuli create a weaker or nonexistent stereoscopic depth sensation). This hypothesis could explain the effects on amplitude, but the spread of phase differences is harder to understand. Here, we demonstrate that changes in both amplitude and phase can be explained by a straightforward modification of the energy model that involves only local processing. Input from each eye is passed through a monocular simple cell, incorporating a threshold, before being combined at a binocular simple cell that feeds into the energy computation. Since this local feedforward model can explain the responses of complex cells to both correlated and anticorrelated stimuli, there is no need to invoke any influence of global stereoscopic matching.

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