fMRI reveals a common neural substrate of illusory and real contours in V1 after perceptual learning

Perceptual learning involves the specific and relatively permanent modification of perception following a sensory experience. In psychophysical experiments, the specificity of the learning effects to the trained stimulus attributes (e.g., visual field position or stimulus orientation) is often attributed to assumed neural modifications at an early cortical site within the visual processing hierarchy. We directly investigated a neural correlate of perceptual learning in the primary visual cortex using fMRI. Twenty volunteers practiced a curvature discrimination on Kanizsa-type illusory contours in the MR scanner. Practice-induced changes in the BOLD response to illusory contours were compared between the pretraining and the posttraining block in those areas of the primary visual cortex (V1) that, in the same session, had been identified to represent real contours at corresponding visual field locations. A retinotopically specific BOLD signal increase to illusory contours was observed as a consequence of the training, possibly signaling the formation of a contour representation, which is necessary for performing the curvature discrimination. The effects of perceptual training were maintained over a period of about 10 months, and they were specific to the trained visual field position. The behavioral specificity of the learning effects supports an involvement of V1 in perceptual learning, and not in unspecific attentional effects

Change blindness: eradication of gestalt strategies

Arrays of eight, texture-defined rectangles were used as stimuli in a one-shot change blindness (CB) task where there was a 50% chance that one rectangle would change orientation between two successive presentations separated by an interval. CB was eliminated by cueing the target rectangle in the first stimulus, reduced by cueing in the interval and unaffected by cueing in the second presentation. This supports the idea that a representation was formed that persisted through the interval before being 'overwritten' by the second presentation (Landman et al, 2003 Vision Research 43149–164]. Another possibility is that participants used some kind of grouping or Gestalt strategy. To test this we changed the spatial position of the rectangles in the second presentation by shifting them along imaginary spokes (by ±1 degree) emanating from the central fixation point. There was no significant difference seen in performance between this and the standard task [F(1,4)=2.565, p=0.185]. This may suggest two things: (i) Gestalt grouping is not used as a strategy in these tasks, and (ii) it gives further weight to the argument that objects may be stored and retrieved from a pre-attentional store during this task

Retinotopic Activation in Response to Subjective Contours in Primary Visual Cortex

Objects in our visual environment are arranged in depth and hence there is a considerable amount of overlap and occlusion in the image they generate on the retina. In order to properly segment the image into figure and background, boundary interpolation is required even across large distances. Here we study the cortical mechanisms involved in collinear contour interpolation using fMRI. Human observers were asked to discriminate the curvature of interpolated boundaries in Kanizsa figures and in control configurations, which contained identical physical information but did not generated subjective shapes. We measured a spatially precise spin-echo BOLD signal and found stronger responses to subjective shapes than non-shapes at the subjective boundary locations, but not at the inducer locations. The responses to subjective contours within primary visual cortex were retinotopically specific and analogous to that to real contours, which is intriguing given that subjective and luminance-defined contours are physically fundamentally different. We suggest that in the absence of retinal stimulation, the observed activation changes in primary visual cortex are driven by intracortical interactions and feedback, which are revealed in the absence of a physical stimulus

Illusory Contours over Pathological Retinal Scotomas

Our visual percepts are not fully determined by physical stimulus inputs. Thus, in visual illusions such as the Kanizsa figure, inducers presented at the corners allow one to perceive the bounding contours of the figure in the absence of luminance-defined borders. We examined the discrimination of the curvature of these illusory contours that pass across retinal scotomas caused by macular degeneration. In contrast with previous studies with normal-sighted subjects that showed no perception of these illusory contours in the region of physiological scotomas at the optic nerve head, we demonstrated perfect discrimination of the curvature of the illusory contours over the pathological retinal scotoma. The illusion occurred despite the large scar around the macular lesion, strongly reducing discrimination of whether the inducer openings were acute or obtuse and suggesting that the coarse information in the inducers (low spatial frequency) sufficed. The result that subjective contours can pass through the pathological retinal scotoma suggests that the visual cortex, despite the loss of bottom-up input, can use low-spatial frequency information from the inducers to form a neural representation of new complex geometrical shapes inside the scotoma

The Developmental Trajectory of Contour Integration in Autism Spectrum Disorders

Sensory input is inherently ambiguous and complex, so perception is believed to be achieved by combining incoming sensory information with prior knowledge. One model envisions the grouping of sensory features (the local dimensions of stimuli) to be the outcome of a predictive process relying on prior experience (the global dimension of stimuli) to disambiguate possible configurations those elements could take. Contour integration, the linking of aligned but separate visual elements, is one example of perceptual grouping. Kanizsa-type illusory contour (IC) stimuli have been widely used to explore contour integration processing. Consisting of two conditions which differ only in the alignment of their inducing elements, one induces the experience of a shape apparently defined by a contour and the second does not. This contour has no counterpart in actual visual space – it is the visual system that fills-in the gap between inducing elements. A well-tested electrophysiological index associated with this process (the IC-effect) provided us with a metric of the visual system’s contribution to contour integration. Using visually evoked potentials (VEP), we began by probing the limits of this metric to three manipulations of contour parameters previously shown to impact subjective experience of illusion strength. Next we detailed the developmental trajectory of contour integration processes over childhood and adolescence. Finally, because persons with autism spectrum disorders (ASDs) have demonstrated an altered balance of global and local processing, we hypothesized that contour integration may be atypical. We compared typical development to development in persons with ASDs to reveal possible mechanisms underlying this processing difference. Our manipulations resulted in no differences in the strength of the IC-effect in adults or children in either group. However, timing of the IC-effect was delayed in two instances: 1) peak latency was delayed by increasing the extent of contour to be filled-in relative to overall IC size and 2) onset latency was delayed in participants with ASDs relative to their neurotypical counterparts

The integration of bottom-up and top-down signals in human perception in health and disease

To extract a meaningful visual experience from the information falling on the retina, the visual system must integrate signals from multiple levels. Bottom-up signals provide input relating to local features while top-down signals provide contextual feedback and reflect internal states of the organism. In this thesis I will explore the nature and neural basis of this integration in two key areas. I will examine perceptual filling-in of artificial scotomas to investigate the bottom-up signals causing changes in perception when filling-in takes place. I will then examine how this perceptual filling-in is modified by top-down signals reflecting attention and working memory. I will also investigate hemianopic completion, an unusual form of filling-in, which may reflect a breakdown in top-down feedback from higher visual areas. The second part of the thesis will explore a different form of top-down control of visual processing. While the effects of cognitive mechanisms such as attention on visual processing are well-characterised, other types of top-down signal such as reward outcome are less well explored. I will therefore study whether signals relating to reward can influence visual processing. To address these questions, I will employ a range of methodologies including functional MRI, magnetoencephalography and behavioural testing in healthy participants and patients with cortical damage. I will demonstrate that perceptual filling-in of artificial scotomas is largely a bottom-up process but that higher cognitive functions can modulate the phenomenon. I will also show that reward modulates activity in higher visual areas in the absence of concurrent visual stimulation and that receiving reward leads to enhanced activity in primary visual cortex on the next trial. These findings reveal that integration occurs across multiple levels even for processes rooted in early retinotopic regions, and that higher cognitive processes such as reward can influence the earliest stages of cortical visual processing

Cue-dependent circuits for illusory contours in humans.

Objects' borders are readily perceived despite absent contrast gradients, e.g. due to poor lighting or occlusion. In humans, a visual evoked potential (VEP) correlate of illusory contour (IC) sensitivity, the "IC effect", has been identified with an onset at ~90ms and generators within bilateral lateral occipital cortices (LOC). The IC effect is observed across a wide range of stimulus parameters, though until now it always involved high-contrast achromatic stimuli. Whether IC perception and its brain mechanisms differ as a function of the type of stimulus cue remains unknown. Resolving such will provide insights on whether there is a unique or multiple solutions to how the brain binds together spatially fractionated information into a cohesive perception. Here, participants discriminated IC from no-contour (NC) control stimuli that were either comprised of low-contrast achromatic stimuli or instead isoluminant chromatic contrast stimuli (presumably biasing processing to the magnocellular and parvocellular pathways, respectively) on separate blocks of trials. Behavioural analyses revealed that ICs were readily perceived independently of the stimulus cue-i.e. when defined by either chromatic or luminance contrast. VEPs were analysed within an electrical neuroimaging framework and revealed a generally similar timing of IC effects across both stimulus contrasts (i.e. at ~90ms). Additionally, an overall phase shift of the VEP on the order of ~30ms was consistently observed in response to chromatic vs. luminance contrast independently of the presence/absence of ICs. Critically, topographic differences in the IC effect were observed over the ~110-160ms period; different configurations of intracranial sources contributed to IC sensitivity as a function of stimulus contrast. Distributed source estimations localized these differences to LOC as well as V1/V2. The present data expand current models by demonstrating the existence of multiple, cue-dependent circuits in the brain for generating perceptions of illusory contours

Estimating the subjective perception of object size and position through brain imaging and psychophysics

Perception is subjective and context-dependent. Size and position perception are no exceptions. Studies have shown that apparent object size is represented by the retinotopic location of peak response in V1. Such representation is likely supported by a combination of V1 architecture and top-down driven retinotopic reorganisation. Are apparent object size and position encoded via a common mechanism? Using functional magnetic resonance imaging and a model-based reconstruction technique, the first part of this thesis sets out to test if retinotopic encoding of size percepts can be generalised to apparent position representation and whether neural signatures could be used to predict an individual’s perceptual experience. Here, I present evidence that static apparent position – induced by a dot-variant Muller-Lyer illusion – is represented retinotopically in V1. However, there is mixed evidence for retinotopic representation of motion-induced position shifts (e.g. curveball illusion) in early visual areas. My findings could be reconciled by assuming dual representation of veridical and percept-based information in early visual areas, which is consistent with the larger framework of predictive coding. The second part of the thesis sets out to compare different psychophysical methods for measuring size perception in the Ebbinghaus illusion. Consistent with the idea that psychophysical methods are not equally susceptible to cognitive factors, my experiments reveal a consistent discrepancy in illusion magnitude estimates between a traditional forced choice (2AFC) task and a novel perceptual matching (PM) task – a variant of a comparison-of-comparisons (CoC) task, a design widely seen as the gold standard in psychophysics. Further investigation reveals the difference was not driven by greater 2AFC susceptibility to cognitive factors, but a tendency for PM to skew illusion magnitude estimates towards the underlying stimulus distribution. I show that this dependency can be largely corrected using adaptive stimulus sampling

Dynamic and Integrative Properties of the Primary Visual Cortex

The ability to derive meaning from complex, ambiguous sensory input requires the integration of information over both space and time, as well as cognitive mechanisms to dynamically shape that integration. We have studied these processes in the primary visual cortex (V1), where neurons have been proposed to integrate visual inputs along a geometric pattern known as the association field (AF). We first used cortical reorganization as a model to investigate the role that a specific network of V1 connections, the long-range horizontal connections, might play in temporal and spatial integration across the AF. When retinal lesions ablate sensory information from portions of the visual field, V1 undergoes a process of reorganization mediated by compensatory changes in the network of horizontal collaterals. The reorganization accompanies the brain’s amazing ability to perceptually “fill-inâ€, or “seeâ€, the lost visual input. We developed a computational model to simulate cortical reorganization and perceptual fill-in mediated by a plexus of horizontal connections that encode the AF. The model reproduces the major features of the perceptual fill-in reported by human subjects with retinal lesions, and it suggests that V1 neurons, empowered by their horizontal connections, underlie both perceptual fill-in and normal integrative mechanisms that are crucial to our visual perception. These results motivated the second prong of our work, which was to experimentally study the normal integration of information in V1. Since psychophysical and physiological studies suggest that spatial interactions in V1 may be under cognitive control, we investigated the integrative properties of V1 neurons under different cognitive states. We performed extracellular recordings from single V1 neurons in macaques that were trained to perform a delayed-match-to-sample contour detection task. We found that the ability of V1 neurons to summate visual inputs from beyond the classical receptive field (cRF) imbues them with selectivity for complex contour shapes, and that neuronal shape selectivity in V1 changed dynamically according to the shapes monkeys were cued to detect. Over the population, V1 encoded subsets of the AF, predicted by the computational model, that shifted as a function of the monkeys’ expectations. These results support the major conclusions of the theoretical work; even more, they reveal a sophisticated mode of form processing, whereby the selectivity of the whole network in V1 is reshaped by cognitive state

Neuronal and behavioral mechanisms of Gestalt perception

Principles of Gestalt perception have fundamentally influenced our understanding of visual cognition. In the past century, Gestalt psychologists postulated that the human brain determines single elements with common features as a single entity rather than a sum of separate parts. The importance of Gestalt perception is emphasized by the neuropsychological syndrome simultanagnosia. Patients suffering from this condition have lost the ability to integrate single elements into a superior entity. Simultanagnosia is usually associated with bilateral posterior temporo-parietal brain lesions but the exact neuroanatomy of global Gestalt perception and functions of areas already associated with this perceptual quality are still a matter of lively debates. Further, not much is known about behavioral characteristics of wellexplored perceptual processes, like visual constancy, in the context of Gestalt perception. The present work aimed at investigating neuronal and behavioral properties of Gestalt perception applying psychophysical methods and functional magnetic resonance imaging (fMRI). In previous neuroimaging studies the temporoparietal junction (TPJ) was identified as a crucial brain structure involved in Gestalt perception. However, its specific role in Gestalt perception is still unclear. The functions attributed to this brain region range from attentional selection between the local and the global level of hierarchically organized stimuli to mere perceptual mechanisms of global processing. The neuroimaging studies included into this work explore mainly TPJ related perceptual functions. In the first study, neuronal properties of TPJ in Gestalt perception were investigated. Based on observations in simultanagnosia patients that are able to perceive familiar complex stimulus arrangements but fail in recognition of novel stimulus configurations, it was hypothesized that TPJ areas mainly contribute to processing of novel object arrangements. A training study was conducted where subjects had to learn the perception of complex stimulus arrangements in order to examine this hypothesis. Neuronal processes of Gestalt perception in bilateral TPJ regions were assessed pre- and posttraining. It was demonstrated that an anterior right hemispheric TPJ region responded to perceptual training with global stimuli. The results indicated fundamentally changed TPJ contributions with increasing familiarity suggesting a different strategy of the brain for processing of highly familiar object arrangements. In the second study, involvements of bilateral TPJ areas in global processing were investigated with an approach taking advantage of visual expertise. During presentation of specific chess arrangements TPJ signals of chess experts and novices were examined. As a consequence, it was possible to compare neuronal TPJ correlates for holistic perception in experts and serial perceptual strategies in novices. The result showed higher signals in bilateral TPJ areas for chess experts compared to novices while inspecting specific chess configurations. With this method a lot of the typical stimulus confounds in research about Gestalt perception, like size differences or differences in spatial frequencies between global/local stimulus levels, were avoided. Moreover, the nature of the stimuli and experimental tasks argues for a TPJ involvement during perception rather than for functions of attentional selection. In the third study perceptual properties of visual size constancy were investigated in the context of Gestalt perception. While size constancy is a well-known phenomenon for regular objects this visual mechanism has not been investigated for stimuli forming a global Gestalt. Therefore, the perceptual performance for a global stimulus arrangement placed on different locations of a visual scene containing a 3D perspective was tested. For the first time, influences of size constancy were demonstrated also for global stimuli. Effects of size constancy on Gestalt perception suggest a perceptual hierarchy of global scenes even on stimuli that have to be integrated themselves. Taken together the results show that the TPJ is involved in mere perceptual processes of Gestalt perception and that an anterior section of this structure has a specific role in processing of novel object arrangements. It was also demonstrated that Gestalt perception itself underlies visual top-down processes of visual constancy suggesting a superior role of global scene processing influencing even local grouping processes.Zu Beginn des letzten Jahrhunderts formulierte die Gestaltpsychologie bestimmte Gesetzmäßigkeiten, die der menschlichen Wahrnehmung zu Grunde liegen. Die sog. Gestaltgesetzte besagen, dass einzelne Elemente mit systematischen Gemeinsamkeiten eher als ganzheitliche Entität aufgefasst werden denn als Summe einzelner Teile. Die besondere Bedeutung der Gestaltwahrnehmung wird durch das neuropsychologische Störungsbild Simultanagnosie deutlich. Patienten, die an dieser Störung leiden, haben die Fähigkeit einzelne Elemente zu einer übergeordneten Einheit zu verbinden verloren. Normalerweise treten Symptome der Simultanagnosie nach bilateralen temporo-parietalen Gehirnläsionen auf. Die genaue Neuroanatomie der Gestaltwahrnehmung und klar definierte Funktionen von Gehirnarealen, die bereits mit globaler Wahrnehmung in Verbindung gebracht werden konnten, sind jedoch noch nicht eindeutig definiert. Darüber hinaus ist auf Verhaltensebene wenig über Funktionen der visuellen Wahrnehmung, z.B. hinsichtlich des Phänomens der Größenkonstanz, im Zusammenhang mit Gestaltwahrnehmung bekannt. Das Ziel der vorliegenden Arbeit ist die Erforschung neuronaler und behavioraler Mechanismen der Gestaltwahrnehmung mit Hilfe psychophysischer und bildgebender Methoden. In bisherigen Bildgebungsstudien konnte die temporo-parietale Übergangsregion (temporo-parietal junction, TPJ) als neuronales Korrelat der Gestaltwahrnehmung identifiziert werden. Die genaue Bedeutung dieser Hirnregion für die Gestaltwahrnehmung ist jedoch noch unklar, wobei bisher vor allem Aufmerksamkeits- und reine Wahrnehmungsfunktionen damit in Verbindung gebracht werden konnten. Die Bildgebungsstudien dieser Arbeit konzentrieren sich daher vornehmlich auf perzeptuelle Funktionen bilateraler TPJ-Areale. In der ersten Studie dieser Arbeit wurden spezifische Eigenschaften der temporo-parietalen Übergangsregion für die Gestaltwahrnehmung untersucht. Die Motivation für diese Studie wurde von Beobachtungen bei Simultanagnosie-Patienten abgeleitet, die vor allem Schwierigkeiten bei der Verarbeitung neuartiger komplexer Reizanordnungen haben, aber geläufige komplexe visuelle Inhalte erkennen können. Daher wurde die Hypothese untersucht, dass bilaterale TPJ-Regionen hauptsächlich in die Verarbeitung neuartiger komplexer Strukturen involviert sind. Zur Untersuchung dieser Hypothese wurde eine Lernstudie durchgeführt. Im Rahmen dieser Studie wurde die Wahrnehmung für komplexe Gestalt-Stimuli trainiert und die neuronalen Mechanismen der Gestaltwahrnehmung vor und nach dem Training mittels funktionaler Magnet Resonanztomographie (fMRT) gemessen. Es zeigte sich, dass hauptsächlich das anteriore rechtshemisphärische TPJ-Areal signifikant auf Wahrnehmungstraining reagierte. Dieses Ergebnis bestätigte die Hypothese, dass TPJ hauptsächlich für die Verarbeitung neuartiger Objekt-Arrangements zuständig ist bzw. komplexe Stimuli mit hohem Bekanntheitsgrad über andere neuronale Kanäle verarbeitet werden. In der zweiten Studie wurde der Beitrag bilateraler TPJ-Areale auf die Gestaltwahrnehmung durch die Untersuchung von Schach-Experten realisiert. Dabei wurden TPJ-Signale von Schach-Experten und Novizen bei der Betrachtung komplexer Schach-Arrangements mittels fMRT gemessen. Auf diese Weise war es möglich neuronale TPJ-Aktivierungen während einer ganzheitlichen Wahrnehmung in Experten und einer seriellen Strategie in Novizen zu vergleichen. Die Ergebnisse zeigten stärkere Signale in bilateralen TPJ-Regionen für Experten im Vergleich zu Novizen während der Betrachtung komplexer Schach-Arrangements. Mit Hilfe dieses Ansatzes konnten einige Störvariablen, die bei der Erforschung der Gestaltwahrnehmung auftreten, wie z.B. Unterschiede zwischen lokalen und globalen Stimuli hinsichtlich Größe oder räumlicher Frequenz, umgangen werden. Darüber hinaus weisen der Aufbau der Stimuli und die verwendeten Testparadigmen auf TPJ-Einflüsse während der perzeptuellen Verarbeitung komplexer Stimuli hin und sprechen gegen TPJ-gesteuerte Aufmerksamkeitsmechanismen der perzeptuellen Auswahl von globalen oder lokalen Ebenen. Die dritte Studie untersuchte perzeptuelle Eigenschaften der Größenkonstanz im Kontext der Gestaltwahrnehmung. Während die Größenkonstanz ein gut erforschtes Phänomen im Rahmen der Objektwahrnehmung darstellt, ist bisher nicht bekannt, ob dieser visuelle Mechanismus auch globale Gestalt-Stimuli betrifft. Diese Fragestellung wurde durch ein Experiment, in dem globale Gestalt-Stimuli in einer visuellen Szene mit 3D-Perspektive platziert wurden, untersucht. Es zeigte sich, dass auch die Verarbeitung globaler Stimuli Mechanismen der Größenkonstanz unterliegt. Effekte der Größenkonstanz auf die Wahrnehmung globaler Gestalt-Stimuli weisen auf eine Hierarchie der visuellen Verarbeitung hin, der zufolge eine übergeordnete globale Szene auch visuelle Inhalte beeinflusst, die selbst der Gestaltwahrnehmung unterliegen. Zusammenfassend zeigen die dargestellten Arbeiten, dass das TPJ-Areal hauptsächlich an der perzeptuellen Verarbeitung komplexer visueller Reizanordnungen beteiligt ist und dabei speziell für neuartige Reizkonfigurationen zuständig ist. Darüber hinaus konnte gezeigt werden, dass Gestaltwahrnehmung selbst Top-down-Prozessen der visuellen Größenkonstanz unterliegt und die globale Wahrnehmung einer visuellen Szene lokale Prozesse der Gestaltwahrnehmung beeinflussen kann