Vision Science seminars

Current computational models of visual salience accurately predict the distribution of fixations on isolated visual stimuli. It is not known, however, whether the global salience of a stimulus, that is its effectiveness in the competition for attention with other stimuli, is a function of the local salience or an independent measure. Further, do task and familiarity with the competing images influence eye movements? In this talk, I will present the analysis of a computational model of the global salience of natural images. We trained a machine learning algorithm to learn the direction of the first saccade of participants who freely observed pairs of images. The pairs balanced the combinations of new and already seen images, as well as task and task-free trials. The coefficients of the model provided a reliable measure of the likelihood of each image to attract the first fixation when seen next to another image, that is their global salience. For example, images of close-up faces and images containing humans were consistently looked first and were assigned higher global salience. Interestingly, we found that global salience cannot be explained by the feature-driven local salience of images, the influence of task and familiarity was rather small and we reproduced the previously reported left-sided bias. This computational model of global salience allows to analyse multiple other aspects of human visual perception of competing stimuli. In the talk, I will also present our latest results from analysing the saccadic reaction time as a function of the global salience of the pair of images.

Outside the foveola, visual acuity and other visual functions gradually deteriorate with increasing eccentricity. Humans compensate for these limitations by relying on a tight link between perception and action; rapid gaze shifts (saccades) occur 2-3 times every second, separating brief “fixation” intervals in which visual information is acquired and processed. During fixation, however, the eye is not immobile. Small eye movements incessantly shift the image on the retina even when the attended stimulus is already foveated, suggesting a much deeper coupling between visual functions and oculomotor activity. Thanks to a combination of techniques allowing for high-resolution recordings of eye position, retinal stabilization, and accurate gaze localization, we examined how attention and eye movements are controlled at this scale. We have shown that during fixation, visual exploration of fine spatial detail unfolds following visuomotor strategies similar to those occurring at a larger scale. This behavior compensates for non-homogenous visual capabilities within the foveola and is finely controlled by attention, which facilitates processing at selected foveal locations. Ultimately, the limits of high acuity vision are greatly influenced by the spatiotemporal modulations introduced by fixational eye movements. These findings reveal that, contrary to common intuition, placing a stimulus within the foveola is necessary but not sufficient for high visual acuity; fine spatial vision is the outcome of an orchestrated synergy of motor, cognitive, and attentional factors.

The long-term goal of my research is to study the mammalian retina as a model for the central nervous system (CNS) -- to understand how it functions in physiological conditions, how it is formed, how it breaks down in pathological conditions, and how it can be repaired. I have focused on two research themes: 1) Photoreceptor structure, synapse, circuits, and development, 2) Hibernation and metabolic adaptations in the retina and beyond. As the first neuron of the visual system, photoreceptors are vital for photoreception and transmission of visual signals. I am particularly interested in cone photoreceptors, as they mediate our daylight vision with high resolution color information. Diseases affecting cone photoreceptors compromise visual functions in the central macular area of the human retina and are thus most detrimental to our vision. However, because cones are much less abundant compared to rods in most mammals, they are less well studied. We have used the ground squirrel (GS) as a model system to study cone vision, taking advantage of their unique cone-dominant retina. In particular, we have focused on short-wavelength sensitive cones (S-cones), which are not only essential for color vision, but are also an important origin of signals for biological rhythm, mood and cognitive functions, and the growth of the eye during development. We are studying critical cone synaptic structures – synaptic ribbons, the synaptic connections of S-cones, and the development of S-cones with regard to their specific connections. These works will provide knowledge of normal retinal development and function, which can also be extended to the rest of CNS; for example, the mechanisms of synaptic targeting during development. In addition, such knowledge will benefit the development of optimal therapeutic strategies for regeneration and repair in cases of retinal degenerative disease. Many neurodegenerative diseases, including retinal diseases, are rooted in metabolic stress in neurons and/or glial cells. Using the same GS model, we aim to learn from this hibernating mammal, which possesses an amazing capability to adapt to the extreme metabolic conditions during hibernation. By exploring the mechanisms of such adaptation, we hope to discover novel therapeutic tactics for neurodegenerative diseases.

Figure-ground organisation and perceptual grouping are classic topics in Gestalt and perceptual psychology. They often appear alongside one another in introductory textbook chapters on perception and have a long history of investigation. However, they are typically discussed as separate processes of perceptual organisation with their own distinct phenomena and mechanisms. Here, I will propose that perceptual grouping and figure-ground organisation are strongly linked. In particular, perceptual grouping can provide a basis for, and may share mechanisms with, a wide range of figure-ground principles. To support this claim, I will describe a new class of figure-ground principles based on perceptual grouping between edges and demonstrate that this inter-edge grouping (IEG) is a powerful influence on figure-ground organisation. I will also draw support from our other results showing that grouping between edges and regions (i.e., edge-region grouping) can affect figure-ground organisation (Palmer & Brooks, 2008) and that contextual influences in figure-ground organisation can be gated by perceptual grouping between edges (Brooks & Driver, 2010). In addition to these modern observations, I will also argue that we can describe some classic figure-ground principles (e.g., symmetry, convexity, etc.) using perceptual grouping mechanisms. These results suggest that figure-ground organisation and perceptual grouping have more than a mere association under the umbrella topics of Gestalt psychology and perceptual organisation. Instead, perceptual grouping may provide a mechanism underlying a broad class of new and extant figure-ground principles.

Emotion processing is thought to be impaired in autism and linked to atypical visual exploration and arousal modulation to others faces and gaze, yet evidence is equivocal. We propose that, where observed, atypical socioemotional processing is due to alexithymia, a distinct but frequently co-occurring condition which affects emotional self-awareness and Interoception. In study 1 (N = 80), we tested this hypothesis by studying the spatio-temporal dynamics and entropy of eye-gaze during emotion processing tasks. Evidence from traditional and novel methods revealed that atypical eye-gaze and emotion recognition is best predicted by alexithymia in both autistic and non-autistic individuals. In Study 2 (N = 70), we assessed interoceptive and autonomic signals implicated in socioemotional processing, and found evidence for alexithymia (not autism) driven effects on gaze and arousal modulation to emotions. We also conducted two large-scale studies (N = 1300), using confirmatory factor-analytic and network modelling and found evidence that Alexithymia and Autism are distinct at both a latent level and their intercorrelations. We argue that: 1) models of socioemotional processing in autism should conceptualise difficulties as intrinsic to alexithymia, and 2) assessment of alexithymia is crucial for diagnosis and personalised interventions in autism.

n natural vision, active vision refers to the changes in visual input resulting from self-initiated eye movements. In this talk, I will present studies that show that the stimulus-related activity during active vision differs substantially from that occurring during classical flashed-stimuli paradigms. Our results uncover novel and efficient mechanisms that improve visual perception. In a general way, the nervous system appears to engage in sensory modulation mechanisms, precisely timed to self-initiated stimulus changes, thus coordinating neural activity across different cortical areas and serving as a general mechanism for the global coordination of visual perception.

It has long been known that when viewing a set of images, we misjudge individual elements as being closer to the mean than they are (Hollingworth, 1910) and recall seeing the (absent) set mean (Deese, 1959; Roediger & McDermott (1995). Recent studies found that viewing sets of images, simultaneously or sequentially, leads to perception of set statistics (mean, range) with poor memory for individual elements. Ensemble perception was found for sets of simple images (e.g. circles varying in size or brightness; lines of varying orientation), complex objects (e.g. faces of varying emotion), as well as for objects belonging to the same category. When the viewed set does not include its mean or prototype, nevertheless, observers report and act as if they have seen this central image or object – a form of false memory. Physiologically, detailed sensory information at cortical input levels is processed hierarchically to form an integrated scene gist at higher levels. However, we are aware of the gist before the details. We propose that images and objects belonging to a set or category are represented as their gist, mean or prototype, plus individual differences from that gist. Under constrained viewing conditions, only the gist is perceived and remembered. This theory also provides a basis for compressed neural representation. Extending this theory to scenes and episodes supplies a generalized basis for false memories. They seem right, match generalized expectations, so are believable without challenging examination. This theory could be tested by analyzing the typicality of false memories, compared to rejected alternatives.

The ability to encode the direction of image motion is fundamental to our sense of vision. Direction selectivity along the four cardinal directions is thought to originate in direction-selective ganglion cells (DSGCs), due to directionally-tuned GABAergic suppression by starburst cells. Here, by utilizing two-photon glutamate imaging to measure synaptic release, we reveal that direction selectivity along all four directions arises earlier than expected, at bipolar cell outputs. Thus, DSGCs receive directionally-aligned glutamatergic inputs from bipolar cell boutons. We further show that this bouton-specific tuning relies on cholinergic excitation and GABAergic inhibition from starburst cells. In this way, starburst cells are able to refine directional tuning in the excitatory visual pathway by modulating the activity of DSGC dendrites and their axonal inputs using two different neurotransmitters.

Neurons in the primary visual cortex (V1) encode the orientation and contrast of visual stimuli through changes in firing rate (Hubel and Wiesel, 1962). Their activity typically peaks at a preferred orientation and decays to zero at the orientations that are orthogonal to the preferred. This activity pattern is re-scaled by contrast but its shape is preserved, a phenomenon known as contrast invariance. Contrast-invariant selectivity is also observed at the population level in V1 (Carandini and Sengpiel, 2004). The mechanisms supporting the emergence of contrast-invariance at the population level remain unclear. How does the activity of different neurons with diverse orientation selectivity and non-linear contrast sensitivity combine to give rise to contrast-invariant population selectivity? Theoretical studies have shown that in the balance limit, the properties of single-neurons do not determine the population activity (van Vreeswijk and Sompolinsky, 1996). Instead, the synaptic dynamics (Mongillo et al., 2012) as well as the intracortical connectivity (Rosenbaum and Doiron, 2014) shape the population activity in balanced networks. We report that short-term plasticity can change the synaptic strength between neurons as a function of the presynaptic activity, which in turns modifies the population response to a stimulus. Thus, the same circuit can process a stimulus in different ways –linearly, sublinearly, supralinearly – depending on the properties of the synapses. We found that balanced networks with excitatory to excitatory short-term synaptic plasticity cannot be contrast-invariant. Instead, short-term plasticity modifies the network selectivity such that the tuning curves are narrower (broader) for increasing contrast if synapses are facilitating (depressing). Based on these results, we wondered whether balanced networks with plastic synapses (other than short-term) can support the emergence of contrast-invariant selectivity. Mathematically, we found that the only synaptic transformation that supports perfect contrast invariance in balanced networks is a power-law release of neurotransmitter as a function of the presynaptic firing rate (in the excitatory to excitatory and in the excitatory to inhibitory neurons). We validate this finding using spiking network simulations, where we report contrast-invariant tuning curves when synapses release the neurotransmitter following a power- law function of the presynaptic firing rate. In summary, we show that synaptic plasticity controls the type of non-linear network response to stimulus contrast and that it can be a potential mechanism mediating the emergence of contrast invariance in balanced networks with orientation-dependent connectivity. Our results therefore connect the physiology of individual synapses to the network level and may help understand the establishment of contrast-invariant selectivity.

In this talk I will summarize some of our recent unpublished work on spectral coding in the larval zebrafish retina. Combining 2p imaging, hyperspectral stimulation, computational modeling and connectomics, we take a renewed look at the spectral tuning of cone photoreceptors in the live eye. We find that already cones optimally rotate natural colour space in a PCA-like fashion to disambiguate greyscale from "colour" information. We then follow this signal through the retinal layers and ultimately into the brain to explore the major spectral computations performed by the visual system at its consecutive stages. We find that by and large, zebrafish colour vision can be broken into three major spectral zones: long wavelength grey-scale-like vision, short-wavelength prey capture circuits, and spectrally diverse mid-wavelength circuits which possibly support the bulk of "true colour vision" in this tetrachromate vertebrate.

The Manookin lab is investigating the structure and function of neural circuits within the retina and developing techniques for treating blindness. Many blinding diseases, such as retinitis pigmentosa, cause death of the rods and cones, but spare other cell types within the retina. Thus, many techniques for restoring visual function following blindness are based on the premise that other cells within the retina remain viable and capable of performing their various roles in visual processing. There are more than 80 different neuronal types in the human retina and these form the components of the specialized circuits that transform the signals from photoreceptors into a neural code responsible for our perception of color, form, and motion, and thus visual experience. The Manookin laboratory is investigating the function and connectivity of neural circuits in the retina using a variety of techniques including electrophysiology, calcium imaging, and electron microscopy. This knowledge is being used to develop more effective techniques for restoring visual function following blindness.

We will start our talk with a short video of our research, illustrating methods (some old and new) and findings that have provided our current understanding of how visual capabilities develop in infancy and early childhood. However, our research poses some outstanding questions. We will briefly discuss three issues, which are linked by a common focus on the development of visual attentional processing: (1) How do recurrent cortical loops contribute to development? Cortical selectivity (e.g., to orientation, motion, and binocular disparity) develops in the early months of life. However, these systems are not purely feedforward but depend on parallel pathways, with recurrent feedback loops playing a critical role. The development of diverse networks, particularly for motion processing, may explain changes in dynamic responses and resolve developmental data obtained with different methodologies. One possible role for these loops is in top-down attentional control of visual processing. (2) Why do hyperopic infants become strabismic (cross-eyes)? Binocular interaction is a particularly sensitive area of development. Standard clinical accounts suppose that long-sighted (hyperopic) refractive errors require accommodative effort, putting stress on the accommodation-convergence link that leads to its breakdown and strabismus. Our large-scale population screening studies of 9-month infants question this: hyperopic infants are at higher risk of strabismus and impaired vision (amblyopia and impaired attention) but these hyperopic infants often under- rather than over-accommodate. This poor accommodation may reflect poor early attention processing, possibly a ‘soft sign’ of subtle cerebral dysfunction. (3) What do many neurodevelopmental disorders have in common? Despite similar cognitive demands, global motion perception is much more impaired than global static form across diverse neurodevelopmental disorders including Down and Williams Syndromes, Fragile-X, Autism, children with premature birth and infants with perinatal brain injury. These deficits in motion processing are associated with deficits in other dorsal stream functions such as visuo-motor co-ordination and attentional control, a cluster we have called ‘dorsal stream vulnerability’. However, our neuroimaging measures related to motion coherence in typically developing children suggest that the critical areas for individual differences in global motion sensitivity are not early motion-processing areas such as V5/MT, but downstream parietal and frontal areas for decision processes on motion signals. Although these brain networks may also underlie attentional and visuo-motor deficits , we still do not know when and how these deficits differ across different disorders and between individual children. Answering these questions provide necessary steps, not only increasing our scientific understanding of human visual brain development, but also in designing appropriate interventions to help each child achieve their full potential.

Vision starts in the retina where images are transformed and coded into neuronal activity relevant for the brain. These coding steps function optimally over a wide range of conditions: from bright day on the beach to a moonless night. Under these very different conditions, specific retinal mechanisms continue to select relevant aspects of the visual world and send this information to the brain. We are studying the neuronal processing involved in these selection and adaptation processes. This knowledge is essential for understanding how the visual system works and forms the basis for research dedicated to restoring vision in blind people.