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).
During perceptual decisions, the activity of sensory neurons correlates with a subject's percept, even when the physical stimulus is identical 1 -9 . The origin of this correlation is unknown. Current theory proposes a causal effect of noise in sensory neurons on perceptual decisions 10 -12 , but it could result from different brain-states associated with the perceptual choice 13 (top-down). These two schemes have very different implications for the role played by sensory neurons in forming decisions 14 . Here, we used white-noise analysis 15 to measure tuning-functions of V2 neurons associated with choice and simultaneously measure how the variation in the stimulus affects subjects' (two macaques) perceptual decisions 16 -18 . In causal models stronger effects of the stimulus upon decisions, mediated by sensory neurons, are associated with stronger choice-related activity. However, we find that over the timecourse of the trial, these measures change in different directions-at odds with causal models. An analysis of effect of reward size supports the same conclusion. Finally, choice was associated with changes in neuronal gain that are incompatible with causal models. All three results are readily explained if choice is associated with changes in neuronal gain caused by top-down phenomena that closely resemble attention 19 . We conclude that top-down processes contribute to choice-related activity. Thus even forming simple sensory decisions involves complex interactions between cognitive processes and sensory neurons.Considerable progress has been made towards explaining the neuronal mechanisms underlying decision making 12 -a major goal in systems neuroscience. For simple perceptual decisions, recent theory proposes that sensorimotor areas accumulate sensory evidence about the physical world, delivered by sensory neurons 10 , 11 , 20 -22 . Noise in the sensory neurons causes variability in the behavioral response 10 -12 , resulting in a co-variation between the neuronal activity and behavior 1 -9 . (Note that this causal effect of noise in the sensory representation has only been invoked for sensory areas, not for sensorimotor areas.) However, this co-variation could also arise from top-down effects 13 in which brain states 23 that are associated with one behavioral response, also alter the response of the sensory neurons. A third (bottom-up) possibility is that sensory neurons that themselves have no Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#termsCorrespondence and requests for materials should be addressed to H.N. (hnienb@gmail.com). Supplementary Information accompanies the paper.Author contributions: H.N. collected the data, performed the analyses and wrote the paper. B.G.C. supervised the project. HHS Public Access Author ManuscriptAuthor Manuscript Author ManuscriptAuthor Manuscript causal effect on th...
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.
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.
Quantitative analysis of the responses of V1 neurons to horizontal disparity in dynamic random-dot stereograms. J Neurophysiol 87: 191-208, 2002; 10.1152/jn.00465.2000. Horizontal disparity tuning for dynamic random-dot stereograms was investigated for a large population of neurons (n ϭ 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. I N T R O D U C T I O NSelectivity for binocular disparity was initially demonstrated using elongated bar stimuli in cat area 17 (Barlow et al. 1967;Pettigrew et al. 1968) and V1 of the awake monkey (Poggio and Fischer 1977). Subsequently, Poggio and colleagues (Poggio 1995;Poggio et al. 1985Poggio et al. , 1988 examined the sensitivity to horizontal disparity in random-dot stereograms (RDS) in macaque V1. None of the studies using RDS has attempted to describe the disparity tuning quantitatively. Consequently, there has been no quantitative analysis of the relationship between disparity selectivity to RDS and other fundamental properties of V1 neurons, such as orientation tuning and ocular dominance.There are several reasons why it is important to study these issues with RDS. First, a change in the disparity of a bar stimulus also generates changes in the monocular images, which by themselves may influence neuronal firing. By contrast the monocular images of random-dot stimuli are spatially homogeneous. There...
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.
Neurons in early sensory cortex show weak but systematic correlations with perceptual decisions when trained animals perform at psychophysical threshold. These correlations are observed across repeated presentations of identical stimuli and cannot be explained by variation in external factors. The relationship between the activity of individual sensory neurons and the animal's behavioral choice means that even neurons in early sensory cortex carry information about an upcoming decision. This relationship, termed choice probability, may reflect the effect of fluctuations in neuronal firing rate on the animal's decision, but it can also reflect modulation of sensory responses by cognitive factors, or network properties such as variability that is shared among populations of neurons. Here, we review recent work clarifying the relationship among fluctuations in the responses of individual neurons, correlated variability, and behavior in a variety of tasks and cortical areas. We also discuss the possibility that choice probability may in part reflect the influence of cognitive factors on sensory neurons and explore the situations in which choice probability can be used to make inferences about the role of particular sensory neurons in the decision-making process.
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.
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