Gene R. Stoner

Object-based attention determines dominance in binocular rivalry

A question of long-standing interest to philosophers, psychologists and neuroscientists is how the brain selects which signals enter consciousness. Binocular rivalry and attention both involve selection of visual stimuli, but affect perception quite differently. During binocular rivalry, awareness alternates between two different stimuli presented to the two eyes. In contrast, attending to one of two different stimuli impairs discrimination of the ignored stimulus, but without causing it to disappear from consciousness. Here we show that despite this difference, attention and rivalry rely on shared object-based selection mechanisms. We cued attention to one of two superimposed transparent surfaces and then deleted the image of one surface from each eye, resulting in rivalry. Observers usually reported seeing only the cued surface. They were also less accurate in judging unpredictable changes in the features of the uncued surface. Our design ensured that selection of the cued surface could not have resulted from spatial, ocular or feature-based mechanisms. Rather, attention was drawn to one surface, and this caused the other surface to be perceptually suppressed during rivalry. These results raise the question of how object representations compete during these two forms of perceptual selection, even as the features of those objects change unpredictably over time.

Neuronal synchrony does not correlate with motion coherence in cortical area MT

Natural visual scenes are cluttered with multiple objects whose individual features must somehow be selectively linked (or ‘bound’) if perception is to coincide with reality. Recent neurophysiological evidence supports a ‘binding-by-synchrony’ hypothesis: neurons excited by features of the same object fire synchronously, while neurons excited by features of different objects do not. Moving plaid patterns offer a straightforward means to test this idea. By appropriate manipulations of apparent transparency, the component gratings of a plaid pattern can be seen as parts of a single coherently moving surface or as two non-coherently moving surfaces. We examined directional tuning and synchrony of area-MT neurons in awake, fixating primates in response to perceptually coherent and non-coherent plaid patterns. Here we show that directional tuning correlated highly with perceptual coherence, which is consistent with an earlier study. Although we found stimulus-dependent synchrony, coherent plaids elicited significantly less synchrony than did non-coherent plaids. Our data therefore do not support the binding-by-synchrony hypothesis as applied to this class of motion stimuli in area MT.

Image segmentation cues in motion processing: Implications for modularity in vision

The problem of processing visual motion is underconstrainedmany possible real world motions are compatible with any given dynamic retinal image. Recent psychophysical and neurophysiological experiments have shown that the primate visual systems normally veridical interpretation of moving patterns is attained through utilization of image segmentation cues unrelated to motion per se. These findings challenge notions of modularity in which it is assumed that the processing of specific scene properties, such as motion, can be studied in isolation from other visual processes. We discuss the implications of these findings with regard to both experimental and computational approaches to the study of visual motion.

Nonhuman primate model of schizophrenia using a noninvasive EEG method

There is growing evidence that impaired sensory-processing significantly contributes to the cognitive deficits found in schizophrenia. For example, the mismatch negativity (MMN) and P3a event-related potentials (ERPs), neurophysiological indices of sensory and cognitive function, are reduced in schizophrenia patients and may be used as biomarkers of the disease. In agreement with glutamatergic theories of schizophrenia, NMDA antagonists, such as ketamine, elicit many symptoms of schizophrenia when administered to normal subjects, including reductions in the MMN and the P3a. We sought to develop a nonhuman primate (NHP) model of schizophrenia based on NMDA-receptor blockade using subanesthetic administration of ketamine. This provided neurophysiological measures of sensory and cognitive function that were directly comparable to those recorded from humans. We first developed methods that allowed recording of ERPs from humans and rhesus macaques and found homologous MMN and P3a ERPs during an auditory oddball paradigm. We then investigated the effect of ketamine on these ERPs in macaques. As found in humans with schizophrenia, as well as in normal subjects given ketamine, we observed a significant decrease in amplitude of both ERPs. Our findings suggest the potential of a pharmacologically induced model of schizophrenia in NHPs that can pave the way for EEG-guided investigations into cellular mechanisms and therapies. Furthermore, given the established link between these ERPs, the glutamatergic system, and deficits in other neuropsychiatric disorders, our model can be used to investigate a wide range of pathologies.

The interpretation of visual motion: Evidence for surface segmentation mechanisms

The independent motions of objects in a visual scene are commonly manifest as overlapping retinal motions. A consequence of this overlap is the creation of spurious retinal image features--such as corners and terminated contours--that bear no direct relation to the motions of the objects that give rise to them. To reconstruct object motions, these emergent features must be distinguished from the retinal motions of real object features. This process can be studied using visual stimuli known as plaid patterns, which provide a laboratory archetype for the ubiquitous real-world circumstance of two surfaces with overlapping retinal projections. By adjusting luminance relationships in a plaid pattern it is possible to influence the perceptual interpretation of image features, such that they are seen as either an emergent consequence of occlusion or as real variations in surface reflectance. In the former case, the plaid is most likely to be to perceived as two independently moving surfaces, whereas the latter generally elicits a percept of a single moving surface. This dependence of motion perception on luminance configuration can be viewed as evidence for the involvement of surface segmentation mechanisms, which distinguish between real and emergent image features by promoting a depth-ordered neural representation of surfaces. An alternative interpretation, which does not demand such depth-ordering and feature classification, asserts that the effect of luminance configuration can be accounted for by attendant variations in the distribution of moving Fourier components. To evaluate these two proposed mechanisms, we designed novel plaid stimuli in which surface segmentation cues could be varied independently of changes in the distribution of Fourier components. Perceived motion was found to be highly correlated with the presence of appropriate segmentation cues and uncorrelated with the distribution of Fourier components. These results refute the Fourier components hypothesis, and they support our proposal that surface segmentation plays a critical role in the interpretation of visual motion signals.

Optogenetics through windows on the brain in the nonhuman primate

Optogenetics combines optics and genetics to control neuronal activity with cell-type specificity and millisecond temporal precision. Its use in model organisms such as rodents, Drosophila, and Caenorhabditis elegans is now well-established. However, application of this technology in nonhuman primates (NHPs) has been slow to develop. One key challenge has been the delivery of viruses and light to the brain through the thick dura mater of NHPs, which can only be penetrated with large-diameter devices that damage the brain. The opacity of the NHP dura prevents visualization of the underlying cortex, limiting the spatial precision of virus injections, electrophysiological recordings, and photostimulation. Here, we describe a new optogenetics approach in which the native dura is replaced with an optically transparent artificial dura. This artificial dura can be penetrated with fine glass micropipettes, enabling precisely targeted injections of virus into brain tissue with minimal damage to cortex. The expression of optogenetic agents can be monitored visually over time. Most critically, this optical window permits targeted, noninvasive photostimulation and concomitant measurements of neuronal activity via intrinsic signal imaging and electrophysiological recordings. We present results from both anesthetized-paralyzed (optical imaging) and awake-behaving NHPs (electrophysiology). The improvements over current methods made possible by the artificial dura should enable the widespread use of optogenetic tools in NHP research, a key step toward the development of therapies for neuropsychiatric and neurological diseases in humans.

Stimulus-dependent variability and noise correlations in cortical MT neurons

Population codes assume that neural systems represent sensory inputs through the firing rates of populations of differently tuned neurons. However, trial-by-trial variability and noise correlations are known to affect the information capacity of neural codes. Although recent studies have shown that stimulus presentation reduces both variability and rate correlations with respect to their spontaneous level, possibly improving the encoding accuracy, whether these second order statistics are tuned is unknown. If so, second-order statistics could themselves carry information, rather than being invariably detrimental. Here we show that rate variability and noise correlation vary systematically with stimulus direction in directionally selective middle temporal (MT) neurons, leading to characteristic tuning curves. We show that such tuning emerges in a stochastic recurrent network, for a set of connectivity parameters that overlaps with a single-state scenario and multistability. Information theoretic analysis shows that second-order statistics carry information that can improve the accuracy of the population code.

Exogenously cued attention triggers competitive selection of surfaces

It has been reported that when an endogenous cue directs attention to a brief translation of one of two superimposed surfaces, observers reliably report the direction of that translation as well as the direction of a second translation of the cued surface. In contrast, if the uncued surface translates second, direction judgments are severely impaired for several hundred milliseconds. We replicated this result, but found that the impairment survived the removal of the endogenous cue. The impairment is therefore not due to endogenously cued attention. Instead, a brief translation of one surface acts as an exogenous cue that triggers an automatic selection mechanism, which suppresses processing of the other surface. This study provides a clear case of exogenous cueing of surface-based attention. We relate these results to identified competitive selection mechanisms in visual cortex.

Adaptation of gender derived from biological motion

Human observers adapted to complex biological motions that distinguish males from females: viewing the gait of one gender biased judgments of subsequent gaits toward the opposite gender. This adaptation was not simply due to local features of the stimuli but instead relied upon the global motion of the figures. These results suggest the existence of neurons selective for gender and demonstrate that gender-from-motion judgments are not fixed but depend upon recent viewing history.

Stimulus-specific competitive selection in macaque extrastriate visual area V4.

Macaque visual area V4 has been implicated in the selective processing of stimuli. Prior studies of selection in area V4 have used spatially separate stimuli, thus confounding selection of retinotopic location with selection of the stimulus at that location. We asked whether V4 neurons can selectively respond to one of two differently colored stimuli even when they are spatially superimposed. We find that delaying one of the two stimuli leads to selective processing of the delayed stimulus by area V4 neurons. This selective processing persists when the stimuli move together across the visual field, thereby successively activating different populations of neurons. We also find that this effect is not a spatially global form of feature-based selection. We conclude that selective processing in area V4 is neither exclusively spatial nor feature-based and may thus be surface- or object-based.