Tilt Aftereffect Research Articles

Tactile adaptation to orientation produces a robust tilt aftereffect and exhibits crossmodal transfer when tested in vision

Orientation processing is one of the most fundamental functions in both visual and somatosensory perception. Converging findings suggest that orientation processing in both modalities is closely linked: somatosensory neurons share a similar orientation organisation as visual neurons, and the visual cortex has been found to be heavily involved in tactile orientation perception. Hence, we hypothesized that somatosensation would exhibit a similar orientation adaptation effect, and this adaptation effect would be transferable between the two modalities, considering the above-mentioned connection. The tilt aftereffect (TAE) is a demonstration of orientation adaptation and is used widely in behavioural experiments to investigate orientation mechanisms in vision. By testing the classic TAE paradigm in both tactile and crossmodal orientation tasks between vision and touch, we were able to show that tactile perception of orientation shows a very robust TAE, similar to its visual counterpart. We further show that orientation adaptation in touch transfers to produce a TAE when tested in vision, but not vice versa. Additionally, when examining the test sequence following adaptation for serial effects, we observed another asymmetry between the two conditions where the visual test sequence displayed a repulsive intramodal serial dependence effect while the tactile test sequence exhibited an attractive serial dependence. These findings provide concrete evidence that vision and touch engage a similar orientation processing mechanism. However, the asymmetry in the crossmodal transfer of TAE and serial dependence points to a non-reciprocal connection between the two modalities, providing further insights into the underlying processing mechanism.

Stronger tilt aftereffects in individuals diagnosed with schizophrenia spectrum disorders but not bipolar disorder

An altered use of context and experience to interpret incoming information has been posited to explain schizophrenia symptoms. The visual system can serve as a model system for examining how context and experience guide perception and the neural mechanisms underlying putative alterations. The influence of prior experience on current perception is evident in visual aftereffects, the perception of the “opposite” of a previously viewed stimulus. Aftereffects are associated with neural adaptation and concomitant change in strength of lateral inhibitory connections in visually responsive neurons. In a previous study, we observed stronger aftereffects related to orientation (tilt aftereffects) but not luminance (negative afterimages) in individuals diagnosed with schizophrenia, which we interpreted as potentially suggesting altered cortical (but not subcortical) adaptability and local changes in excitatory-inhibitory interactions. Here, we tested whether stronger tilt aftereffects were specific to individuals with schizophrenia or extended to individuals with bipolar disorder. We measured tilt aftereffects and negative afterimages in 32 individuals with bipolar disorder, and compared aftereffect strength to a previously reported group of 36 individuals with schizophrenia and 22 healthy controls. We observed stronger tilt aftereffects, but not negative afterimages, in individuals with schizophrenia as compared to both controls and individuals with bipolar disorder, who did not differ from each other. These results mitigate concerns that stronger tilt aftereffects in schizophrenia are a consequence of medication or of the psychosocial consequences of a severe mental illness.

Distinct early and late neural mechanisms regulate feature-specific sensory adaptation in the human visual system

A canonical feature of sensory systems is that they adapt to prolonged or repeated inputs, suggesting the brain encodes the temporal context in which stimuli are embedded. Sensory adaptation has been observed in the central nervous systems of many animal species, using techniques sensitive to a broad range of spatiotemporal scales of neural activity. Two competing models have been proposed to account for the phenomenon. One assumes that adaptation reflects reduced neuronal sensitivity to sensory inputs over time (the "fatigue" account); the other posits that adaptation arises due to increased neuronal selectivity (the "sharpening" account). To adjudicate between these accounts, we exploited the well-known "tilt aftereffect", which reflects adaptation to orientation information in visual stimuli. We recorded whole-brain activity with millisecond precision from human observers as they viewed oriented gratings before and after adaptation, and used inverted encoding modeling to characterize feature-specific neural responses. We found that both fatigue and sharpening mechanisms contribute to the tilt aftereffect, but that they operate at different points in the sensory processing cascade to produce qualitatively distinct outcomes. Specifically, fatigue operates during the initial stages of processing, consistent with tonic inhibition of feedforward responses, whereas sharpening occurs ~200 ms later, consistent with feedback or local recurrent activity. Our findings reconcile two major accounts of sensory adaptation, and reveal how this canonical process optimizes the detection of change in sensory inputs through efficient neural coding.

Tilt aftereffect spreads across the visual field

The tilt aftereffect (TAE) is observed when adaptation to a tilted contour alters the perceived tilt of a subsequently presented contour. Thus far, TAE has been treated as a local aftereffect observed only at the location of the adapter. Whether and how TAE spreads to other locations in the visual field has not been systematically studied. Here, we sought an answer to this question by measuring TAE magnitudes at locations including but not limited to the adapter location. The adapter was a tilted grating presented at the same peripheral location throughout an experimental session. In a single trial, participants indicated the perceived tilt of a test grating presented after the adapter at one of fifteen locations in the same visual hemifield as the adapter. We found non-zero TAE magnitudes in all locations tested, showing that the effect spreads across the tested visual hemifield. Next, to establish a link between neuronal activity and behavioral results and to predict the possible neuronal origins of the spread, we built a computational model based on known characteristics of the visual cortex. The simulation results showed that the model could successfully capture the pattern of the behavioral results. Furthermore, the pattern of the optimized receptive field sizes suggests that mid-level visual areas, such as V4, could be critically involved in TAE and its spread across the visual field.

Tilt adaptation aftereffects reveal fundamental perceptual characteristics of tactile orientation processing on the hand.

Orientation information contributes substantially to our tactile perception, such as feeling an object's shape on the skin. For vision, a perceptual adaptation aftereffect (tilt aftereffect; TAE), which is well explained by neural orientation selectivity, has been used to reveal fundamental perceptual properties of orientation processing. Neural orientation selectivity has been reported in somatosensory cortices. However, little research has investigated the perceptual characteristics of the tactile TAE. The aim of the current study was to provide the first demonstration of a tactile TAE on the hand and investigate the perceptual nature of tactile TAE on the hand surface. We used a 2-point stimulation with minimal input for orientation. We found clear TAEs on the hand surface: Adaptation induced shifts in subjective vertical sensation toward the orientation opposite to the adapted orientation. Further, adaptation aftereffects were purely based on orientation processing given that the effects transferred between different lengths across adaptor and test stimuli and type of stimuli. Finally, adaptation aftereffects were anchored to the hand: tactile TAE occurred independently of hand rotation and transferred from palm to dorsum sides of the hand, while the effects did not transfer between hands. Our findings demonstrate the existence of hand-centered perceptual processing for basic tactile orientation information. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

The role of lateral modulation in orientation-specific adaptation effect.

Center-surround modulation in visual processing reflects a normalization process of contrast gain control in the responsive neurons. Prior adaptation to a clockwise (CW) tilted grating, for example, leads to the percept of counterclockwise tilt in a vertical grating, referred to as the tilt-aftereffect (TAE). We previously reported that the magnitude of the TAE is modulated by adding a same-orientation annular surround to an adapter, suggesting inhibitory lateral modulation. To further examine the property of this lateral modulation effect on the perception of a central target, we here used center-surround sinusoidal patterns as adapters and varied the adapter surround and center orientations independently. The target had the same spatial extent as the adapter center with no physical overlap with the adapter surround. Participants were asked to judge the target orientation as tilted either CW or counterclockwise from vertical after adaptation. Results showed that, when the surround orientation was held constant, the TAE magnitude was determined by the adapter center, peaking between 10° and 20° of tilt. More important, the adapter surround orientation modulated the adaptation effect such that the TAE magnitude first decreased and then increased as the surround orientation became increasingly more different from that of the center, suggesting that the surround modulation effect was indeed orientation specific. Our data can be accounted for by a divisive inhibition model, in which (1) the adaptation effect is represented by increasing the normalizing constant and (2) the surround modulation is captured by two multiplicative sensitivity parameters determined by the adapter surround orientation.

Functional Interactions between Sensory and Memory Networks for Adaptive Behavior.

The brain’s capacity to adapt to sensory inputs is key for processing sensory information efficiently and interacting in new environments. Following repeated exposure to the same sensory input, brain activity in sensory areas is known to decrease as inputs become familiar, a process known as adaptation. Yet, the brain-wide mechanisms that mediate adaptive processing remain largely unknown. Here, we combine multimodal brain imaging (functional magnetic resonance imaging [fMRI], magnetic resonance spectroscopy) with behavioral measures of orientation-specific adaptation (i.e., tilt aftereffect) to investigate the functional and neurochemical mechanisms that support adaptive processing. Our results reveal two functional brain networks: 1) a sensory-adaptation network including occipital and dorsolateral prefrontal cortex regions that show decreased fMRI responses for repeated stimuli and 2) a perceptual-memory network including regions in the parietal memory network (PMN) and dorsomedial prefrontal cortex that relate to perceptual bias (i.e., tilt aftereffect). We demonstrate that adaptation relates to increased occipito-parietal connectivity, while decreased connectivity between sensory-adaptation and perceptual-memory networks relates to GABAergic inhibition in the PMN. Thus, our findings provide evidence that suppressive interactions between sensory-adaptation (i.e., occipito-parietal) and perceptual-memory (i.e., PMN) networks support adaptive processing and behavior, proposing a key role of memory systems in efficient sensory processing.

Working Memory Load Effects on the Tilt Aftereffect.

Prolonged exposure to an oriented stimulus causes a subsequent test stimulus to be perceived as tilted in the opposite direction, a phenomenon referred to as the tilt aftereffect (TAE). Previous studies have demonstrated that high-level cognitive functions such as attention can modulate the TAE, which is generally well-known as a low-level perceptual process. However, it is unclear whether working memory load, another high-level cognitive function, could modulate the TAE. To address this issue, here we developed a new paradigm by combining a working memory load task with a TAE task. Participants firstly remembered a stream of digits (Experiment 1) or four color-shape conjunctions (Experiment 2) under high/low load conditions, and then recognized the probe stimuli (digits or a color-shape conjunction), which were presented at the center of an adapting grating. After the recognition task (i.e., the adaptation stage), participants performed an orientation judgment task to measure their TAEs. The result of Experiment 1, where the load stimuli were digits, showed that the magnitude of the TAEs were reduced under the condition of the high working memory load compared to that of the low working memory load. However, we failed to replicate the finding in Experiment 2, where the load stimuli were color-shape conjunctions. Together, our two experiments provided mixed evidence regarding the working memory load effects on the TAE and further replications are needed in future work.

Interaction of surface pattern and contour shape in the tilt after effects evoked by symmetry

Integration of multiple properties of an object is a fundamental function of the visual cortex in object recognition. For instance, surface patterns and contour shapes are thought to be crucial characteristics that jointly contribute to recognition. However, the mechanisms of integration and corresponding cortical representations have not been fully clarified. We investigated the integration of surfaces and shapes by examining the tilt after effects (TAEs) evoked by the symmetry of patterns and contours. As symmetry in both pattern and contour evokes TAEs, we can directly measure the interaction between the two. The measured TAEs exhibited mutual transfer between the symmetry of the pattern (SP) and that of the contour shape (SS), i.e., adaptation by SP (SS) evoked TAEs when tested by SS (SP), suggesting the existence of an integrated representation. Next, we examined the interaction between SP and SS when both were simultaneously presented in adaptation. Congruent adaptors wherein their symmetry axes aligned evoked compressive interaction, whereas incongruent adaptors wherein the axes of SP and SS tilted to the opposite directions evoked subtractive interaction. These results suggest the existence of a cortical representation that integrates the properties of the surface and shape with suppressive interactions, which can provide crucial insights into the formation of object representation as well as the integration of visual information in the cortex.

Spatial and Temporal Selectivity of Translational Glass Patterns Assessed With the Tilt After-Effect.

Glass patterns (GPs) have been widely employed to investigate the mechanisms underlying processing of global form from locally oriented cues. The current study aimed to psychophysically investigate the level at which global orientation is extracted from translational GPs using the tilt after-effect (TAE) and manipulating the spatiotemporal properties of the adapting pattern. We adapted participants to translational GPs and tested with sinewave gratings. In Experiment 1, we investigated whether orientation-selective units are sensitive to the temporal frequency of the adapting GP. We used static and dynamic translational GPs, with dynamic GPs refreshed at different temporal frequencies. In Experiment 2, we investigated the spatial frequency selectivity of orientation-selective units by manipulating the spatial frequency content of the adapting GPs. The results showed that the TAE peaked at a temporal frequency of ∼30 Hz, suggesting that orientation-selective units responding to translational GPs are sensitive to high temporal frequencies. In addition, TAE from translational GPs peaked at lower spatial frequencies than the dipoles’ spatial constant. These effects are consistent with form-motion integration at low and intermediate levels of visual processing.

Stronger tilt aftereffects in persons with schizophrenia.

Individuals with schizophrenia may fail to appropriately use temporal context and apply past environmental regularities to the interpretation of incoming sensory information. Here we use the visual system as a test bed for investigating how prior experience shapes perception in individuals with schizophrenia. Specifically, we use visual aftereffects, illusory percepts resulting from prior exposure to visual input, to measure the influence of prior events on current processing. At a neural level, visual aftereffects arise due to attenuation in the responses of neurons that code the features of the prior stimulus (neuronal adaptation) and subsequent disinhibition of neurons signaling activity at the opposite end of the feature dimension. In the current study, we measured tilt aftereffects and negative afterimages, 2 types of aftereffects that reflect, respectively, adaptation of cortical orientation-coding neurons and adaptation of subcortical and retinal luminance-coding cells in persons with schizophrenia (PSZ; n = 36) and demographically matched healthy controls (HC; n = 22). We observed stronger tilt aftereffects in PSZ compared to HC, but no difference in negative afterimages. Stronger tilt aftereffects were related to more severe negative symptoms. These data suggest oversensitivity to recent regularities, in the form of stronger visual adaptation, at cortical, but not subcortical, levels in schizophrenia. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

A decision-time account of individual variability in context-dependent orientation estimation

Following exposure to an oriented stimulus, the perceived orientation is slightly shifted, a phenomenon termed the tilt aftereffect (TAE). This estimation bias, as well as other context-dependent biases, is speculated to reflect statistical mechanisms of inference that optimize visual processing. Importantly, although measured biases are extremely robust in the population, the magnitude of individual bias can be extremely variable. For example, measuring different individuals may result in TAE magnitudes that differ by a factor of 5. Such findings appear to challenge the accounts of bias in terms of learned statistics: is inference so different across individuals? Here, we found that a strong correlation exists between reaction time and TAE, with slower individuals having much less TAE. In the tilt illusion, the spatial analogue of the TAE, we found a similar, though weaker, correlation. These findings can be explained by a theory predicting that bias, caused by a change in the initial conditions of evidence accumulation (e.g., priors), decreases with decision time (*Communications Biology 3 (2020) 1–12). We contend that the context-dependence of visual processing is more homogeneous in the population than was previously thought, with the measured variability of perceptual bias explained, at least in part, by the flexibility of decision-making. Homogeneity in processing might reflect the similarity of the learned statistics.

Lateral modulation of orientation perception in center-surround sinusoidal stimuli: Divisive inhibition in perceptual filling-in.

The perception of a target stimulus may be altered by its context. Perceptual filling-in is thought to be one example of lateral modulation, in which the percept of a central blank area is replaced by that of the surround. We investigated the mechanisms in eccentric vision underlying filling-in by selectively adapting the center (pedestal adapter), surround (annulus adapter), or both (disk adapter) in a sinusoidal grating and observed how the adaptation influences the orientation percept of a subsequently presented Gabor target, located at the same position as the adapter center. In a binary choice task, observers were to judge the orientation (clockwise or counterclockwise) of the target after adaptation. The tilt aftereffect (TAE), corresponding to an illusory tilt of a physically vertical Gabor target, depended both on the adapter orientation and the adapter type. The TAE, peaked between 10 degrees and 20 degrees adapter orientation, was strongest in the pedestal, followed by the disk, and weakest in the annulus adapter conditions. The difference between the disk and pedestal conditions implies lateral inhibition from the surround. Lacking physical overlap with the target, the annulus adapter nonetheless induced a small but significant TAE in the central area. The effect of filling-in on the TAE was estimated by comparing the results from trials with and without subjectively reported filling-in during adaptation to the annulus adapter. The TAE was greater when filling-in occurred during adaptation, suggesting a stronger lateral modulation effect on trials where filling-in was induced. The data were fit by a variant of a divisive inhibition model, in which the adaptation effect is captured by the increase of an additive constant in the denominator of the response function, whereas the surround modulation in the adapter is modeled by an excitatory sensitivity in the numerator.

Interaction of contexts in context-dependent orientation estimation

The processing of a visual stimulus is known to be influenced by the statistics in recent visual history and by the stimulus' visual surround. Such contextual influences lead to perceptually salient phenomena, such as the tilt aftereffect and the tilt illusion. Despite much research on the influence of an isolated context, it is not clear how multiple, possibly competing sources of contextual influence interact. Here, using psychophysical methods, we compared the combined influence of multiple contexts to the sum of the isolated context influences. The results showed large deviations from linear additivity for adjacent or overlapping contexts, and remarkably, clear additivity when the contexts were sufficiently separated. Specifically, for adjacent or overlapping contexts, the combined effect was often lower than the sum of the isolated component effects (sub-additivity), or was more influenced by one component than another (selection). For contexts that were separated in time (600 ms), the combined effect measured the exact sum of the isolated component effects (in degrees of bias). Overall, the results imply an initial compressive transformation during visual processing, followed by selection between the processed parts.

Perceptual bias is reduced with longer reaction times during visual discrimination

Fast and slow decisions exhibit distinct behavioral properties, such as the presence of decision bias in faster but not slower responses. This dichotomy is currently explained by assuming that distinct cognitive processes map to separate brain mechanisms. Here, we suggest an alternative single-process account based on the stochastic properties of decision processes. Our experimental results show perceptual biases in a variety of tasks (specifically: learned priors, tilt aftereffect, and tilt illusion) that are much reduced with increasing reaction time. To account for this, we consider a simple yet general explanation: prior and noisy decision-related evidence are integrated serially, with evidence and noise accumulating over time (as in the standard drift diffusion model). With time, owing to noise accumulation, the prior effect is predicted to diminish. This illustrates that a clear behavioral separation—presence vs. absence of bias—may reflect a simple stochastic mechanism.

Short-Term Attractive Tilt Aftereffects Predicted by a Recurrent Network Model of Primary Visual Cortex.

Adaptation is a multi-faceted phenomenon that is of interest in terms of both its function and its potential to reveal underlying neural processing. Many behavioral studies have shown that after exposure to an oriented adapter the perceived orientation of a subsequent test is repulsed away from the orientation of the adapter. This is the well-known Tilt Aftereffect (TAE). Recently, we showed that the dynamics of recurrently connected networks may contribute substantially to the neural changes induced by adaptation, especially on short time scales. Here we extended the network model and made the novel behavioral prediction that the TAE should be attractive, not repulsive, on a time scale of a few 100 ms. Our experiments, using a novel adaptation protocol that specifically targeted adaptation on a short time scale, confirmed this prediction. These results support our hypothesis that recurrent network dynamics may contribute to short-term adaptation. More broadly, they show that understanding the neural processing of visual inputs that change on the time scale of a typical fixation requires a detailed analysis of not only the intrinsic properties of neurons, but also the slow and complex dynamics that emerge from their recurrent connectivity. We argue that this is but one example of how even simple recurrent networks can underlie surprisingly complex information processing, and are involved in rudimentary forms of memory, spatio-temporal integration, and signal amplification.

A new visual illusion of aspect-ratio context

Perception of local properties of the visual field is influenced by aftereffects of adaptation. The tilt aftereffect describes repulsion of the perceived orientation of a line from the orientation of an adapting line. Analogous effects of spatial context are often called illusions. Repulsion of the perceived orientation of a grating from the orientation of a surrounding grating is referred to as the tilt illusion. In the same manner, the size aftereffect and Ebbinghaus illusion form a complementary pair of temporal and spatial context effects of size. Here we report psychophysical evidence for a previously unknown aspect-ratio illusion which causes the perceived aspect-ratio of a rectangle to be repelled from the aspect-ratio of rectangles surrounding it. This illusion provides a spatial analogue to the aspect-ratio aftereffect.

Effects of Number and Duration of Adaptation Events on Tilt and Motion Aftereffects in Central and Peripheral Vision

Effects of Number and Duration of Adaptation Events on Tilt and Motion Aftereffects in Central and Peripheral Vision

Phase specific shape aftereffects explained by the tilt aftereffect.

Aftereffects of adaptation are frequently used to infer mechanisms of human visual perception. Commonly, the properties of stimuli are repelled from properties of the adaptor. For example, in the tilt aftereffect a line is repelled in orientation from a previously experienced line. Perceived orientation is predicted by the centroid of the responses of a population of mechanisms individually tuned to limited ranges of orientation but collectively sensitive to the whole possible range. Aftereffects are also predictable if the mechanisms are allowed to adapt. Adaptation across radial frequency patterns, patterns deformed from circular by a sinusoidal modulation of radius, causes repulsive aftereffects, sensitive to the relative amplitudes and orientations of the patterns. Here we show that these shape aftereffects can be accounted for by the application of local tilt aftereffects around the shape contour. We suggest that fields of tilt aftereffects might provide a general mechanism for exaggerating the perceptual difference between successively experienced stimuli, making them more discriminable. If the human visual system does indeed exploit this possibility, then the conclusions often made by studies assuming adaptation within mechanisms sensitive to the shape of stimuli will need to be reconsidered. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Border ownership-dependent tilt aftereffect for shape defined by binocular disparity and motion parallax.

Discerning objects from their surrounds (i.e., figure-ground segmentation) in a way that guides adaptive behaviors is a fundamental task of the brain. Neurophysiological work has revealed a class of cells in the macaque visual cortex that may be ideally suited to support this neural computation: border ownership cells (Zhou H, Friedman HS, von der Heydt R. J Neurosci 20: 6594–6611, 2000). These orientation-tuned cells appear to respond conditionally to the borders of objects. A behavioral correlate supporting the existence of these cells in humans was demonstrated with two-dimensional luminance-defined objects (von der Heydt R, Macuda T, Qiu FT. J Opt Soc Am A Opt Image Sci Vis 22: 2222–2229, 2005). However, objects in our natural visual environments are often signaled by complex cues, such as motion and binocular disparity. Thus for border ownership systems to effectively support figure-ground segmentation and object depth ordering, they must have access to information from multiple depth cues with strict depth order selectivity. Here we measured in humans (of both sexes) border ownership-dependent tilt aftereffects after adaptation to figures defined by either motion parallax or binocular disparity. We find that both depth cues produce a tilt aftereffect that is selective for figure-ground depth order. Furthermore, we find that the effects of adaptation are transferable between cues, suggesting that these systems may combine depth cues to reduce uncertainty (Bülthoff HH, Mallot HA. J Opt Soc Am A 5: 1749–1758, 1988). These results suggest that border ownership mechanisms have strict depth order selectivity and access to multiple depth cues that are jointly encoded, providing compelling psychophysical support for their role in figure-ground segmentation in natural visual environments.NEW & NOTEWORTHY Figure-ground segmentation is a critical function that may be supported by “border ownership” neural systems that conditionally respond to object borders. We measured border ownership-dependent tilt aftereffects to figures defined by motion parallax or binocular disparity and found aftereffects for both cues. These effects were transferable between cues but selective for figure-ground depth order, suggesting that the neural systems supporting figure-ground segmentation have strict depth order selectivity and access to multiple depth cues that are jointly encoded.