Nearly half of the cerebral cortex of primates, including humans, is devoted to visual perception. This large proportion reflects the fact that our visual acuity, and the use of vision in our daily life, surpasses that of all other mammals. Why is so much of the brain required to interpret the images falling on the retina? One answer to that question is that vision is, by its nature, an interpretive process and a considerably more difficult problem than one might think. Consider a few moments in the life of a human or any other primate. As we walk or climb through our environment, we turn our heads and move our eyes. We glance three times per second from object to object, in some cases trying to understand the expression on a face, and in others deciding how to shape our hand in order to establish a correct grip. Our own movements cause our retinal image to flit about in a manner that would be impossible to understand if we were to see it on a computer monitor. Nonetheless, our brain is able to interpret this seemlingly incomprehensible sequence of retinal images and integrate it into a stable visual world: Indeed, the retina is only our visual sensor, controlled by the brain to sample data from our environment. It makes no sense to take each snapshot at face value instead the sequence of retinal images is, from the very beginning, interpreted within the context of the movements issued by the brain. Likewise, the brain makes an educated guess on the identity and use of objects, the distance to locations within the scene, the emotions and intentions of people, and a countless number of other features of the world. These qualities are not written into the visual signals themselves, but must be judged based on physical cues, experience, and intuition. In some cases the judgments are unconscious and automatic, whereas in others they are at the fore of our thought processes. In the this we focus on aspects of visual perception that are so immediate and intuitive to us that it is not at all obvious that there is a problem to be solved. In the past year, the laboratory has made headway on three studies related to visual perception. We have also published two studies and a major review in the Annual Review of Neuroscience entitled, Primary visual cortex, awareness and blindsight. In one study, we are investigating activity in a part of the thalamus called the pulvinar during spontaneous changes in visual perception. This project draws upon a phenomenon known as bistable perception, where a given physical stimulus is inherently ambiguous. The brain, seeing ambiguity as a dilemma, lapses into a sequence of spontaneous perceptual reversals. Our study in the pulvinar asks to what extent do visual thalamic neurons respond according to the subjective perception of an observer, even in cases when the stimulus is unchanging? This work follows on a series of previous studies investigating activity throughout the cortex and thalamus during a type of bistable perception called binocular rivalry. Those studies have shown that there is essentially a gradient of perception-related switching throughout the visual cortex, with early areas showing the weakest perceptual correlation and the later areas showing the strongest. The pulvinar receives input from the entire visual cortex, and this input shows some degree of regional segregation.
Our aim i s therefore to map the subregions of this nucleus during binocular rivalry, as well as other tasks, with the aim of understanding its functional organization with respect to visual perception. During the last year, we have made strong headway on this project, and have collected our first data from the pulvinar. Over the next year, we plan to continue this mapping process so that we will be able to understand the regional specificity of perceptual modulation. The larger goal of this project is to gain insights into the thalamocortical relationship more generally. In the last year, we have also completed two studies related to the contribution of a particular brain area, known as V4, to visual perception. In one project, we have asked investigated the basis of a visual illusion called subjective surface completion. Surface completion is a means by which the brain, upon seeing an array incomplete stimulus elements aligned in just the right way, creates the subjective impression of a surface even though no such surface is physically present. This process is thought to reflect automatic processes by which the brain routinely guesses what is present in a scene. Such guessing is critical in normal vision because, under normal conditions, objects and surfaces are occluded by scene elements. As an analogy, upon viewing a house whose middle portion is blocked by a large tree, the brain understands that the house is a complete and continuous structure that is partly obscured, rather than two half-houses. When certain illusions are optimized, this sort of perceptual completion can be extreme, and it is possible to visually perceive the part of the obscured stimulus that is being completed. This phenomenon raises the question: which neurons in the brain are responsible for this effect? Based on previous work, we gathered that an area known as V4 might contribute to this phenomenon. To address this, we implanted microelectrode arrays in area V4 in two trained monkeys who experienced this visual illusion. We found that V4 neurons exhibited an enhanced, and sometimes rhythmic, response during the illusion compared to similar conditions in which no such illusion was observed. We further discovered that, for a given neuron to participate in this enhancement, the spatial requirements were quite precise. Only when a neurons highest visual sensitivity was directly over the illusory surface was such a modulation observed. The results demonstrate that V4 neurons are directly involved in the interpolative processes involved in subjective surface completion. Moreover, they illustrate that this area, whose neurons normally cover a relatively broad range of visual space, is unexpectedly sensitive to the fine spatial details of the visual stimulus. In another V4 study, we have conducted a follow-up study to an earlier experiment related to the phenomenon of blindsight. We currently have a paper in submission in which we ask the question, to what extent does area V4 respond to visual stimuli when V1 is injured or absent? Under normal conditions, removal of area V1 leads to blindness, but is characterized by some residual, unconscious visual abilities known as blindsight. Our recent findings that fMRI responses in V4 can be observed during blindsight suggest that neurons in this area retain some visual responsiveness. Our present study demonstrates that not only do V4 neurons retain the ability to respond to visual stimuli, but that the residual responses are different in nature than the original responses. Specifically, although much weaker in amplitude, they are more movement sensitive, and to some degree more direction selective, than normal V4 responses. Our findings are in line with the view of the primary visual cortex as the major driver for neural activity in higher cortical areas. At the same time, the presence of weak responses to visual stimulation in the scotoma region supports the notion of V1-bypassing thalamic projections systems as alternative relays for the transmission of information to visual association cortex.
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