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Gregory C DeAngelis

Publications and source records attributed to Gregory C DeAngelis.

12 recordsLinked to original sources

Linking neural representation to function in stereoscopic depth perception: roles of the middle temporal area in coarse versus fine disparity discrimination.

Neurons selective for binocular disparity form the neural substrate for stereoscopic depth perception and are found in several areas of primate visual cortex. Presumably, multiple representations of disparity exist to serve different functions, but the specific contributions of different visual areas to depth perception remain poorly understood. We examine this issue by comparing the contributions of the middle temporal (MT) area to performance of two depth discrimination tasks: a "coarse" task that involves discrimination between absolute disparities in the presence of noise, and a "fine" task that involves discrimination of very small differences in relative disparity between two stimuli in the absence of noise. In the fine task, we find that electrical microstimulation of MT does not affect perceptual decisions, although many individual MT neurons have sufficient sensitivity to account for behavioral performance. In contrast, microstimulation at the same recording sites does bias depth percepts in the coarse task. We hypothesized that these results may be explained by the fact that MT neurons do not represent relative disparity signals that are thought to be essential for the fine task. This hypothesis was supported by single-unit recordings that show that MT neurons signal absolute, but not relative, disparities in a stimulus configuration similar to that used in the fine task. This work establishes a link between the neural representation of disparity in MT and the functional contributions of this area to depth perception.

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Visual and nonvisual contributions to three-dimensional heading selectivity in the medial superior temporal area.

Robust perception of self-motion requires integration of visual motion signals with nonvisual cues. Neurons in the dorsal subdivision of the medial superior temporal area (MSTd) may be involved in this sensory integration, because they respond selectively to global patterns of optic flow, as well as translational motion in darkness. Using a virtual-reality system, we have characterized the three-dimensional (3D) tuning of MSTd neurons to heading directions defined by optic flow alone, inertial motion alone, and congruent combinations of the two cues. Among 255 MSTd neurons, 98% exhibited significant 3D heading tuning in response to optic flow, whereas 64% were selective for heading defined by inertial motion. Heading preferences for visual and inertial motion could be aligned but were just as frequently opposite. Moreover, heading selectivity in response to congruent visual/vestibular stimulation was typically weaker than that obtained using optic flow alone, and heading preferences under congruent stimulation were dominated by the visual input. Thus, MSTd neurons generally did not integrate visual and nonvisual cues to achieve better heading selectivity. A simple two-layer neural network, which received eye-centered visual inputs and head-centered vestibular inputs, reproduced the major features of the MSTd data. The network was trained to compute heading in a head-centered reference frame under all stimulus conditions, such that it performed a selective reference-frame transformation of visual, but not vestibular, signals. The similarity between network hidden units and MSTd neurons suggests that MSTd may be an early stage of sensory convergence involved in transforming optic flow information into a (head-centered) reference frame that facilitates integration with vestibular signals.

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A logarithmic, scale-invariant representation of speed in macaque middle temporal area accounts for speed discrimination performance.

Human speed discrimination thresholds follow Weber's law over a large range of reference (i.e., pedestal) speeds, that is, the just-noticeable-difference in speed scales in proportion to the reference speed. We analyzed the neural representation of speed information in macaque middle temporal visual area (MT) to determine whether this representation can account for the basic form of psychophysical data. Based on theoretical considerations, we hypothesized: (1) that the speed tuning curves of MT neurons should be bell-shaped (Gaussian) as a function of the logarithm of speed, (2) that the set of speed-tuning curves should be approximately scale-invariant, (3) that the distribution of speed preferences should be approximately uniform in log speed, and (4) that response variability should be independent of speed preference. Our quantitative analysis of data from 501 MT neurons shows that the neural representation of speed approximately obeys these constraints, with modest deviations particularly at slow speeds. We then used the MT data to predict how speed discrimination thresholds should depend on pedestal speed. The shape of this prediction matches very closely to that of human psychophysical data, accounting for constant Weber fractions over a large range of intermediate speeds as well as a marked departure from Weber's law at slow speeds. Moreover, we show that deviations of the MT representation from the above constraints are important for predicting how psychophysical thresholds depart from Weber's law at slow speeds. These findings support the notion that a logarithmic, approximately scale-invariant representation of speed in area MT limits perceptual speed discrimination.

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Does neuronal synchrony underlie visual feature grouping?

Previous research suggests that synchronous neural activity underlies perceptual grouping of visual image features. The generality of this mechanism is unclear, however, as previous studies have focused on pairs of neurons with overlapping or collinear receptive fields. By sampling more broadly and employing stimuli that contain partially occluded objects, we have conducted a more incisive test of the binding by synchrony hypothesis in area MT. We find that synchrony in spiking activity shows little dependence on feature grouping, whereas gamma band synchrony in field potentials can be significantly stronger when features are grouped. However, these changes in gamma band synchrony are small relative to the variability of synchrony across recording sites and do not provide a robust population signal for feature grouping. Moreover, these effects are reduced when stimulus differences nearby the receptive fields are eliminated using partial occlusion. Our findings suggest that synchrony does not constitute a general mechanism of visual feature binding.

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Contribution of area MT to stereoscopic depth perception: choice-related response modulations reflect task strategy.

Due to the diversity of tuning properties in sensory cortex, only a fraction of neurons are engaged in a particular task. Characterizing the tuning properties of neurons that are functionally linked to behavior is essential for understanding how activity is "read out" from sensory maps to guide decisions. We recorded from middle temporal (MT) neurons while monkeys performed a depth discrimination task, and we characterized the linkage between MT responses and behavioral choices. Trial-to-trial response fluctuations of MT neurons with odd-symmetric ("Near," "Far") disparity tuning were predictive of monkeys' choices, whereas responses of neurons with even-symmetric tuning were not. This result cannot be explained by neuronal sensitivity or any other response property of MT neurons that we examined but is simply explained by the task strategy that monkeys learned during training. We suggest that this approach provides a physiological means to explore how task strategies are implemented in the brain.

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Perceptual "read-out" of conjoined direction and disparity maps in extrastriate area MT.

Cortical neurons are frequently tuned to several stimulus dimensions, and many cortical areas contain intercalated maps of multiple variables. Relatively little is known about how information is "read out" of these multidimensional maps. For example, how does an organism extract information relevant to the task at hand from neurons that are also tuned to other, irrelevant stimulus dimensions? We addressed this question by employing microstimulation techniques to examine the contribution of disparity-tuned neurons in the middle temporal (MT) visual area to performance on a direction discrimination task. Most MT neurons are tuned to both binocular disparity and the direction of stimulus motion, and MT contains topographic maps of both parameters. We assessed the effect of microstimulation on direction judgments after first characterizing the disparity tuning of each stimulation site. Although the disparity of the stimulus was irrelevant to the required task, we found that microstimulation effects were strongly modulated by the disparity tuning of the stimulated neurons. For two of three monkeys, microstimulation of nondisparity-selective sites produced large biases in direction judgments, whereas stimulation of disparity-selective sites had little or no effect. The binocular disparity was optimized for each stimulation site, and our result could not be explained by variations in direction tuning, response strength, or any other tuning property that we examined. When microstimulation of a disparity-tuned site did affect direction judgments, the effects tended to be stronger at the preferred disparity of a stimulation site than at the nonpreferred disparity, indicating that monkeys can selectively monitor direction columns that are best tuned to an appropriate conjunction of parameters. We conclude that the contribution of neurons to behavior can depend strongly upon tuning to stimulus dimensions that appear to be irrelevant to the current task, and we suggest that these findings are best explained in terms of the strategy used by animals to perform the task.

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Do visual cues contribute to the neural estimate of viewing distance used by the oculomotor system?

Perceived shape and depth judgments that require knowledge of viewing distance are strongly influenced by both vergence angle and the pattern of vertical disparities across large visual fields. On the basis of this established contribution of visual cues to the neural estimate of viewing distance, we hypothesized that the oculomotor system would also make use of high-level visual cues to distance. To address this hypothesis, we investigated how compensatory eye movements during whole-body translation scale with viewing distance. Monkeys viewed large-field (85 x 68 degrees ) random-dot stereograms that were rear projected onto a fixed screen and simulated either a textured wall or pyramid at different viewing distances. In these stereograms, we independently manipulated vergence angle, horizontal and vertical disparity gradients, relative horizontal disparities, and textural cues to viewing distance. For comparison, random-dot patterns were also projected onto a moveable screen placed at different physical distances from the animal. Several cycles of left-right sinusoidal motion of the monkey at 5 Hz were interleaved with several cycles of motion in darkness, and the relationship between eye movement responses and viewing distance was quantified. As expected from previous work, the amplitude of compensatory eye movements depended strongly on vergence angle. Although visual cues to distance had a statistically significant effect on eye movements, these effects were approximately 20-fold weaker than the effect of vergence angle. We conclude that sensory and motor systems do not share a common neural estimate of viewing distance and that the oculomotor system relies far less on visual cues than the perceptual system.

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Macaque middle temporal neurons signal depth in the absence of motion.

The middle temporal (MT) visual area is widely accepted to play important roles in motion processing. It is unclear, however, whether MT contributes to visual perception during the viewing of static scenes, when there is little retinal image motion during the interval between saccades. Some previous studies suggest that MT neurons give little or no response to stationary stimuli that are flashed onto the receptive field, but no previous study has directly examined the fidelity with which MT neurons code visual information in moving versus stationary stimuli. In this study, we compare the ability of MT neurons to signal binocular disparity in moving versus stationary random-dot stereograms. Although responses to moving stimuli are typically stronger, many MT neurons give robust responses to stationary stereograms, and some MT neurons actually prefer stationary patterns to those moving at any tested speed. These responses to stationary stimuli are not caused by monitor refresh or microsaccades. Disparity tuning curves for moving and stationary stimuli are nearly identical in shape for most neurons. Although the disparity discriminability of MT neurons is generally higher for moving stereograms when responses are averaged over the entire 1.5 sec trial epoch, discriminability is comparable for moving and stationary stimuli during the first 200-300 msec of the response. Thus, in a normal time interval between saccades, MT neurons signal the binocular disparity of stationary stimuli with high fidelity. These findings show that MT can be a reliable source of visual information during the viewing of static scenes.

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Disparity-based coding of three-dimensional surface orientation by macaque middle temporal neurons.

Gradients of binocular disparity across the visual field provide a potent cue to the three-dimensional (3-D) orientation of surfaces in a scene. Neurons selective for 3-D surface orientation defined by disparity gradients have recently been described in parietal cortex, but little is known about where and how this selectivity arises within the visual pathways. Because the middle temporal area (MT) has previously been implicated in depth perception, we tested whether MT neurons could signal the 3-D orientation (as parameterized by tilt and slant) of planar surfaces that were depicted by random-dot stereograms containing a linear gradient of horizontal disparities. We find that many MT neurons are tuned for 3-D surface orientation, and that tilt and slant generally have independent effects on MT responses. This separable coding of tilt and slant is reminiscent of the joint coding of variables in other areas (e.g., orientation and spatial frequency in V1). We show that tilt tuning remains unchanged when all coherent motion is removed from the visual stimuli, indicating that tilt selectivity is not a byproduct of 3-D velocity coding. Moreover, tilt tuning is typically insensitive to changes in the mean disparity (depth) of gradient stimuli, indicating that tilt tuning cannot be explained by conventional tuning for frontoparallel disparities. Finally, we explore the receptive field mechanisms underlying selectivity for 3-D surface orientation, and we show that tilt tuning arises through heterogeneous disparity tuning within the receptive fields of MT neurons. Our findings show that MT neurons carry high-level signals about 3-D surface structure, in addition to coding retinal image velocities.

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Contribution of middle temporal area to coarse depth discrimination: comparison of neuronal and psychophysical sensitivity.

Recent work suggests that the middle temporal (MT) area contributes to depth perception in addition to its well established roles in motion perception. To determine whether single MT neurons carry disparity signals with sufficient fidelity to account for depth perception, we have compared neuronal and psychophysical sensitivity to disparity while monkeys discriminated between two coarse disparities (near vs far) in the presence of noise. The strength of the visual stimulus was titrated around psychophysical threshold by varying the percentage of binocularly correlated dots in a random dot stereogram. We find that the average MT neuron has sensitivity equal to that of the monkey, as was reported previously for direction discrimination in MT. We further address some important factors that could bias the neuronal/psychophysical sensitivity comparison, including the possibility that monkeys reach a decision before the end of the stimulus presentation. Unlike the predictions of a simple model that uses Poisson spiking statistics, the sensitivity of many MT neurons has little dependence on the time interval over which spikes are counted to compute a neuronal threshold. Thus the response properties of many MT neurons appear to be adapted for rapid discrimination of depth, and we describe how temporal variations in both signal and noise contribute to this effect. We therefore predicted that psychophysical thresholds should exhibit little dependence on viewing duration in our task, and this was confirmed by additional behavioral experiments. Overall, our findings show that MT is well suited to provide sensory signals that form the basis for perceptual judgments of depth.

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Coding of horizontal disparity and velocity by MT neurons in the alert macaque.

We performed the first large-scale (n = 501), quantitative study of horizontal disparity tuning in the middle temporal (MT) visual area of alert, fixating macaque monkeys. Using random-dot stereograms, we quantified the direction tuning, speed tuning, horizontal disparity tuning, and size tuning of each neuron. The vast majority (93%) of MT neurons were significantly tuned for horizontal disparity. Although disparity tuning was generally quite robust, the average disparity sensitivity of MT neurons was significantly weaker than their direction or speed sensitivity as quantified using both an index of response modulation and an index of signal-to-noise ratio. Disparity tuning was not correlated with direction or size tuning but tended to be broader and weaker for neurons that preferred faster speeds of motion. By comparison with recent studies, we find that disparity selectivity in MT is substantially stronger than that seen in either primary visual cortex (V1) or area V4. In addition, MT neurons are more broadly tuned for disparity than V1 neurons at comparable eccentricities. Disparity tuning curves are very well described by Gabor functions for >80% of MT neurons. The distribution of Gabor phases shows clear bimodality, indicating that MT neurons tend to have odd-symmetric disparity tuning (unlike neurons in V1). The preferred disparities were more strongly correlated with the phase parameter of the Gabor function than with the positional offset parameter. In fact, for neurons with preferred disparities close to zero, the positional offset tended to oppose the phase shift in specifying the disparity preference. We suggest that this result reflects a strategy used to finely distribute the disparity preferences of MT neurons, given the predominance of odd-symmetry and broad tuning.

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Binocular vision: an orientation to disparity coding.

A new study has shown that neurons in the visual cortex are specialized to encode the larger range of horizontal - relative to vertical - disparities that occurs in central vision. These results challenge the established 'energy' model of disparity processing.

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