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Annual Review of Vision Science - Volume 7, 2021
Volume 7, 2021
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Coming of Age in Science: Just Look?
Vol. 7 (2021), pp. 1–17More LessWith Professor Patrick Cavanagh, I started the Harvard Vision Sciences Laboratory in 1990. Blessed with the largesse of a wealthy university, we occupied a very large common space. Here, students pursued their own projects in a uniquely cooperative and exciting scientific environment. The times were just right in the emerging and expanding field of vision science. With good thesis projects under their belt, most of the students went on to successful careers. However, my own coming of age in science did not have such a promising start. It only started well into my thirties when I joined the Smith Kettlewell Eye Research Institute in San Francisco. Providentially, it was there that I had the rare and unique opportunity to work closely and essentially only with peers (not students). Through these intense collaborations, I found my way as a scientist. Most of this account describes these formative years.
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The Diversity of Eyes and Vision
Vol. 7 (2021), pp. 19–41More LessEvery aspect of vision, from the opsin proteins to the eyes and the ways that they serve animal behavior, is incredibly diverse. It is only with an evolutionary perspective that this diversity can be understood and fully appreciated. In this review, I describe and explain the diversity at each level and try to convey an understanding of how the origin of the first opsin some 800 million years ago could initiate the avalanche that produced the astonishing diversity of eyes and vision that we see today. Despite the diversity, many types of photoreceptors, eyes, and visual roles have evolved multiple times independently in different animals, revealing a pattern of eye evolution strictly guided by functional constraints and driven by the evolution of gradually more demanding behaviors. I conclude the review by introducing a novel distinction between active and passive vision that points to uncharted territories in vision research.
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Generating and Using Transcriptomically Based Retinal Cell Atlases
Vol. 7 (2021), pp. 43–72More LessIt has been known for over a century that the basic organization of the retina is conserved across vertebrates. It has been equally clear that retinal cells can be classified into numerous types, but only recently have methods been devised to explore this diversity in unbiased, scalable, and comprehensive ways. Advances in high-throughput single-cell RNA sequencing (scRNA-seq) have played a pivotal role in this effort. In this article, we outline the experimental and computational components of scRNA-seq and review studies that have used them to generate retinal atlases of cell types in several vertebrate species. These atlases have enabled studies of retinal development, responses of retinal cells to injury, expression patterns of genes implicated in retinal disease, and the evolution of cell types. Recently, the inquiry has expanded to include the entire eye and visual centers in the brain. These studies have enhanced our understanding of retinal function and dysfunction and provided tools and insights for exploring neural diversity throughout the brain.
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Morphology, Molecular Characterization, and Connections of Ganglion Cells in Primate Retina
Vol. 7 (2021), pp. 73–103More LessThe eye sends information about the visual world to the brain on over 20 parallel signal pathways, each specialized to signal features such as spectral reflection (color), edges, and motion of objects in the environment. Each pathway is formed by the axons of a separate type of retinal output neuron (retinal ganglion cell). In this review, we summarize what is known about the excitatory retinal inputs, brain targets, and gene expression patterns of ganglion cells in humans and nonhuman primates. We describe how most ganglion cell types receive their input from only one or two of the 11 types of cone bipolar cell and project selectively to only one or two target regions in the brain. We also highlight how genetic methods are providing tools to characterize ganglion cells and establish cross-species homologies.
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Impact of Photoreceptor Loss on Retinal Circuitry
Vol. 7 (2021), pp. 105–128More LessOur sense of sight relies on photoreceptors, which transduce photons into the nervous system's electrochemical interpretation of the visual world. These precious photoreceptors can be disrupted by disease, injury, and aging. Once photoreceptors start to die, but before blindness occurs, the remaining retinal circuitry can withstand, mask, or exacerbate the photoreceptor deficit and potentially be receptive to newfound therapies for vision restoration. To maximize the retina's receptivity to therapy, one must understand the conditions that influence the state of the remaining retina. In this review, we provide an overview of the retina's structure and function in health and disease. We analyze a collection of observations on photoreceptor disruption and generate a predictive model to identify parameters that influence the retina's response. Finally, we speculate on whether the retina, with its remarkable capacity to function over light levels spanning nine orders of magnitude, uses these same adaptational mechanisms to withstand and perhaps mask photoreceptor loss.
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Imaging the Retinal Vasculature
Vol. 7 (2021), pp. 129–153More LessAdvances in retinal imaging are enabling researchers and clinicians to make precise noninvasive measurements of the retinal vasculature in vivo. This includes measurements of capillary blood flow, the regulation of blood flow, and the delivery of oxygen, as well as mapping of perfused blood vessels. These advances promise to revolutionize our understanding of vascular regulation, as well as the management of retinal vascular diseases. This review provides an overview of imaging and optical measurements of the function and structure of the ocular vasculature. We include general characteristics of vascular systems with an emphasis on the eye and its unique status. The functions of vascular systems are discussed, along with physical principles governing flow and its regulation. Vascular measurement techniques based on reflectance and absorption are briefly introduced, emphasizing ways of generating contrast. One of the prime ways to enhance contrast within vessels is to use techniques sensitive to the motion of cells, allowing precise measurements of perfusion and blood velocity. Finally, we provide a brief introduction to retinal vascular diseases.
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The Mechanism of Macular Sparing
Vol. 7 (2021), pp. 155–179More LessPatients with homonymous hemianopia sometimes show preservation of the central visual fields, ranging up to 10°. This phenomenon, known as macular sparing, has sparked perpetual controversy. Two main theories have been offered to explain it. The first theory proposes a dual representation of the macula in each hemisphere. After loss of one occipital lobe, the back-up representation in the remaining occipital lobe is postulated to sustain ipsilateral central vision in the blind hemifield. This theory is supported by studies showing that some midline retinal ganglion cells project to the wrong hemisphere, presumably driving neurons in striate cortex that have ipsilateral receptive fields. However, more recent electrophysiological recordings and neuroimaging studies have cast doubt on this theory by showing only a minuscule ipsilateral field representation in early visual cortical areas. The second theory holds that macular sparing arises because the occipital pole, where the macula is represented, remains perfused after occlusion of the posterior cerebral artery because it receives collateral flow from the middle cerebral artery. An objection to this theory is that it cannot account for reports of macular sparing in patients after loss of an entire occipital lobe. On close scrutiny, such reports turn out to be erroneous, arising from inadequate control of fixation during visual field testing. Patients seem able to detect test stimuli on their blind side within the macula or along the vertical meridian because they make surveillance saccades. A purported treatment for hemianopia, called vision restoration therapy, is based on this error. The dual perfusion theory is supported by anatomical studies showing that the middle cerebral artery perfuses the occipital pole in many individuals.In patients with hemianopia from stroke, neuroimaging shows preservation of the occipital pole when macular sparing is present. The frontier dividing the infarcted territory of the posterior cerebral artery and the preserved territory of the middle cerebral artery is variable, but always falls within the representation of the macula, because the macula is so highly magnified. For physicians, macular sparing was an important neurological sign in acute hemianopia because it signified a posterior cerebral artery occlusion. Modern neuroimaging has supplanted the importance of that clinical sign but at the same time confirmed its validity. For patients, macular sparing remains important because it mitigates the impact of hemianopia and preserves the ability to read fluently.
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Neuromodulatory Control of Early Visual Processing in Macaque
Vol. 7 (2021), pp. 181–199More LessVisual processing is dynamically controlled by multiple neuromodulatory molecules that modify the responsiveness of neurons and the strength of the connections between them. In particular, modulatory control of processing in the lateral geniculate nucleus of the thalamus, V1, and V2 will alter the outcome of all subsequent processing of visual information, including the extent to and manner in which individual inputs contribute to perception and decision making and are stored in memory. This review addresses five small-molecule neuromodulators—acetylcholine, dopamine, serotonin, noradrenaline, and histamine—considering the structural basis for their action, and the effects of their release, in the early visual pathway of the macaque monkey. Traditionally, neuromodulators are studied in isolation and in discrete circuits; this review makes a case for considering the joint action of modulatory molecules and differences in modulatory effects across brain areas as a better means of understanding the diverse roles that these molecules serve.
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Visual Signals in the Mammalian Auditory System
Vol. 7 (2021), pp. 201–223More LessCoordination between different sensory systems is a necessary element of sensory processing. Where and how signals from different sense organs converge onto common neural circuitry have become topics of increasing interest in recent years. In this article, we focus specifically on visual–auditory interactions in areas of the mammalian brain that are commonly considered to be auditory in function. The auditory cortex and inferior colliculus are two key points of entry where visual signals reach the auditory pathway, and both contain visual- and/or eye movement–related signals in humans and other animals. The visual signals observed in these auditory structures reflect a mixture of visual modulation of auditory-evoked activity and visually driven responses that are selective for stimulus location or features. These key response attributes also appear in the classic visual pathway but may play a different role in the auditory pathway: to modify auditory rather than visual perception. Finally, while this review focuses on two particular areas of the auditory pathway where this question has been studied, robust descending as well as ascending connections within this pathway suggest that undiscovered visual signals may be present at other stages as well.
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Population Models, Not Analyses, of Human Neuroscience Measurements
Vol. 7 (2021), pp. 225–255More LessSelectivity for many basic properties of visual stimuli, such as orientation, is thought to be organized at the scale of cortical columns, making it difficult or impossible to measure directly with noninvasive human neuroscience measurement. However, computational analyses of neuroimaging data have shown that selectivity for orientation can be recovered by considering the pattern of response across a region of cortex. This suggests that computational analyses can reveal representation encoded at a finer spatial scale than is implied by the spatial resolution limits of measurement techniques. This potentially opens up the possibility to study a much wider range of neural phenomena that are otherwise inaccessible through noninvasive measurement. However, as we review in this article, a large body of evidence suggests an alternative hypothesis to this superresolution account: that orientation information is available at the spatial scale of cortical maps and thus easily measurable at the spatial resolution of standard techniques. In fact, a population model shows that this orientation information need not even come from single-unit selectivity for orientation tuning, but instead can result from population selectivity for spatial frequency. Thus, a categorical error of interpretation can result whereby orientation selectivity can be confused with spatial frequency selectivity. This is similarly problematic for the interpretation of results from numerous studies of more complex representations and cognitive functions that have built upon the computational techniques used to reveal stimulus orientation. We suggest in this review that these interpretational ambiguities can be avoided by treating computational analyses as models of the neural processes that give rise to measurement. Building upon the modeling tradition in vision science using considerations of whether population models meet a set of core criteria is important for creating the foundation for a cumulative and replicable approach to making valid inferences from human neuroscience measurements.
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Visual Remapping
Vol. 7 (2021), pp. 257–277More LessOur visual system is fundamentally retinotopic. When viewing a stable scene, each eye movement shifts object features and locations on the retina. Thus, sensory representations must be updated, or remapped, across saccades to align presaccadic and postsaccadic inputs. The earliest remapping studies focused on anticipatory, presaccadic shifts of neuronal spatial receptive fields. Over time, it has become clear that there are multiple forms of remapping and that different forms of remapping may be mediated by different neural mechanisms. This review attempts to organize the various forms of remapping into a functional taxonomy based on experimental data and ongoing debates about forward versus convergent remapping, presaccadic versus postsaccadic remapping, and spatial versus attentional remapping. We integrate findings from primate neurophysiological, human neuroimaging and behavioral, and computational modeling studies. We conclude by discussing persistent open questions related to remapping, with specific attention to binding of spatial and featural information during remapping and speculations about remapping's functional significance.
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Role of the Superior Colliculus in Guiding Movements Not Made by the Eyes
Vol. 7 (2021), pp. 279–300More LessThe superior colliculus (SC) has long been associated with the neural control of eye movements. Over seventy years ago, the orderly topography of saccade vectors and corresponding visual field locations were discovered in the cat SC. Since then, numerous high-impact studies have investigated and manipulated the relationship between visuotopic space and saccade vector across this topography to better understand the physiological underpinnings of the sensorimotor signal transformation. However, less attention has been paid to the other motor responses that may be associated with SC activity, ranging in complexity from concerted movements of skeletomotor muscle groups, such as arm-reaching movements, to behaviors that involve whole-body movement sequences, such as fight-or-flight responses in murine models. This review surveys these more complex movements associated with SC (optic tectum in nonmammalian species) activity and, where possible, provides phylogenetic and ethological perspective.
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Spatial Integration in Normal Face Processing and Its Breakdown in Congenital Prosopagnosia
Vol. 7 (2021), pp. 301–321More LessCongenital prosopagnosia (CP), a life-long impairment in face processing that occurs in the absence of any apparent brain damage, provides a unique model in which to explore the psychological and neural bases of normal face processing. The goal of this review is to offer a theoretical and conceptual framework that may account for the underlying cognitive and neural deficits in CP. This framework may also provide a novel perspective in which to reconcile some conflicting results that permits the expansion of the research in this field in new directions. The crux of this framework lies in linking the known behavioral and neural underpinnings of face processing and their impairments in CP to a model incorporating grid cell–like activity in the entorhinal cortex. Moreover, it stresses the involvement of active, spatial scanning of the environment with eye movements and implicates their critical role in face encoding and recognition. To begin with, we describe the main behavioral and neural characteristics of CP, and then lay down the building blocks of our proposed model, referring to the existing literature supporting this new framework. We then propose testable predictions and conclude with open questions for future research stemming from this model.
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Urgent Decision Making: Resolving Visuomotor Interactions at High Temporal Resolution
Vol. 7 (2021), pp. 323–348More LessMeasuring when exactly perceptual decisions are made is crucial for defining how the activation of specific neurons contributes to behavior. However, in traditional, nonurgent visuomotor tasks, the uncertainty of this temporal measurement is very large. This is a problem not only for delimiting the capacity of perception, but also for correctly interpreting the functional roles ascribed to choice-related neuronal responses. In this article, we review psychophysical, neurophysiological, and modeling work based on urgent visuomotor tasks in which this temporal uncertainty can be effectively overcome. The cornerstone of this work is a novel behavioral metric that describes the evolution of the subject's perceptual judgment moment by moment, allowing us to resolve numerous perceptual events that unfold within a few tens of milliseconds. In this framework, the neural distinction between perceptual evaluation and motor selection processes becomes particularly clear, as the conclusion of one is not contingent on that of the other.
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Remembering the Past to See the Future
Vol. 7 (2021), pp. 349–365More LessIn addition to the role that our visual system plays in determining what we are seeing right now, visual computations contribute in important ways to predicting what we will see next. While the role of memory in creating future predictions is often overlooked, efficient predictive computation requires the use of information about the past to estimate future events. In this article, we introduce a framework for understanding the relationship between memory and visual prediction and review the two classes of mechanisms that the visual system relies on to create future predictions. We also discuss the principles that define the mapping from predictive computations to predictive mechanisms and how downstream brain areas interpret the predictive signals computed by the visual system.
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Balancing Flexibility and Interference in Working Memory
Vol. 7 (2021), pp. 367–388More LessWorking memory is central to cognition, flexibly holding the variety of thoughts needed for complex behavior. Yet, despite its importance, working memory has a severely limited capacity, holding only three to four items at once. In this article, I review experimental and computational evidence that the flexibility and limited capacity of working memory reflect the same underlying neural mechanism. I argue that working memory relies on interactions between high-dimensional, integrative representations in the prefrontal cortex and structured representations in the sensory cortex. Together, these interactions allow working memory to flexibly maintain arbitrary representations. However, the distributed nature of working memory comes at the cost of causing interference between items in memory, resulting in a limited capacity. Finally, I discuss several mechanisms used by the brain to reduce interference and maximize the effective capacity of working memory.
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Binocular Vision and Stereopsis Across the Animal Kingdom
Vol. 7 (2021), pp. 389–415More LessMost animals have at least some binocular overlap, i.e., a region of space that is viewed by both eyes. This reduces the overall visual field and raises the problem of combining two views of the world, seen from different vantage points, into a coherent whole. However, binocular vision also offers many potential advantages, including increased ability to see around obstacles and increased contrast sensitivity. One particularly interesting use for binocular vision is comparing information from both eyes to derive information about depth. There are many different ways in which this might be done, but in this review, I refer to them all under the general heading of stereopsis. This review examines the different possible uses of binocular vision and stereopsis and compares what is currently known about the neural basis of stereopsis in different taxa. Studying different animals helps us break free of preconceptions stemming from the way that stereopsis operates in human vision and provides new insights into the different possible forms of stereopsis.
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Lightness Perception in Complex Scenes
Vol. 7 (2021), pp. 417–436More LessLightness perception is the perception of achromatic surface colors: black, white, and shades of grey. Lightness has long been a central research topic in experimental psychology, as perceiving surface color is an important visual task but also a difficult one due to the deep ambiguity of retinal images. In this article, I review psychophysical work on lightness perception in complex scenes over the past 20 years, with an emphasis on work that supports the development of computational models. I discuss Bayesian models, equivalent illumination models, multidimensional scaling, anchoring theory, spatial filtering models, natural scene statistics, and related work in computer vision. I review open topics in lightness perception that seem ready for progress, including the relationship between lightness and brightness, and developing more sophisticated computational models of lightness in complex scenes.
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Quantifying Visual Image Quality: A Bayesian View
Vol. 7 (2021), pp. 437–464More LessImage quality assessment (IQA) models aim to establish a quantitative relationship between visual images and their quality as perceived by human observers. IQA modeling plays a special bridging role between vision science and engineering practice, both as a test-bed for vision theories and computational biovision models and as a powerful tool that could potentially have a profound impact on a broad range of image processing, computer vision, and computer graphics applications for design, optimization, and evaluation purposes. The growth of IQA research has accelerated over the past two decades. In this review, we present an overview of IQA methods from a Bayesian perspective, with the goals of unifying a wide spectrum of IQA approaches under a common framework and providing useful references to fundamental concepts accessible to vision scientists and image processing practitioners. We discuss the implications of the successes and limitations of modern IQA methods for biological vision and the prospect for vision science to inform the design of future artificial vision systems. (The detailed model taxonomy can be found at http://ivc.uwaterloo.ca/research/bayesianIQA/.)
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The Certainty of Ambiguity in Visual Neural Representations
Vol. 7 (2021), pp. 465–486More LessSome images evoke bistable percepts: two different visual experiences seen in alternation while continuously viewing an unchanged stimulus. The Necker Cube and Rubin's Vase are classic examples, each of which gives alternating percepts of different shapes. Other bistable percepts are alternating colors or directions of motion. Although stimuli that result in salient bistability are rare and sometimes cleverly constructed to emphasize ambiguity, they have been influential for over 150 years, since the work of von Helmholtz, who considered them to be evidence for perceptual visual processes that interpret retinal stimuli. While bistability in natural viewing is uncommon, the main point of this review is that implicit ambiguity in visual neural representations is pervasive. Resolving ambiguity, therefore, is a fundamental and ubiquitous process of vision that routinely affects what we see, not an oddity arising from cleverly crafted images. This review focuses on the causes of widespread ambiguity, historical perspectives on it, and modern knowledge and theory about resolving it.
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