Tomas Knapen

The Role of Frontal and Parietal Brain Areas in Bistable Perception

When sensory input allows for multiple, competing perceptual interpretations, observers perception can fluctuate over time, which is called bistable perception. Imaging studies in humans have revealed transient responses in a right-lateralized network in the frontal-parietal cortex (rFPC) around the time of perceptual transitions between interpretations, potentially reflecting the neural initiation of transitions. We investigated the role of this activity in male human observers, with specific interest in its relation to the temporal structure of transitions, which can be either instantaneous or prolonged by periods during which observers experience a mix of both perceptual interpretations. Using both bistable apparent motion and binocular rivalry, we show that transition-related rFPC activity is larger for transitions that last longer, suggesting that rFPC remains active as long as a transition lasts. We also replicate earlier findings that rFPC activity during binocular rivalry transitions exceeds activity during yoked transitions that are simulated using video replay. However, we show that this established finding holds only when perceptual transitions are replayed as instantaneous events. When replay, instead, depicts transitions with the actual durations reported during rivalry, yoked transitions and genuine rivalry transitions elicit equal activity. Together, our results are consistent with the view that at least a component of rFPC activation during bistable perception reflects a response to perceptual transitions, both real and yoked, rather than their cause. This component of activity could reflect the change in sensory experience and task demand that occurs during transitions, which fits well with the known role of these areas in attention and decision making.

Multi-timescale perceptual history resolves visual ambiguity

When visual input is inconclusive, does previous experience aid the visual system in attaining an accurate perceptual interpretation? Prolonged viewing of a visually ambiguous stimulus causes perception to alternate between conflicting interpretations. When viewed intermittently, however, ambiguous stimuli tend to evoke the same percept on many consecutive presentations. This perceptual stabilization has been suggested to reflect persistence of the most recent percept throughout the blank that separates two presentations. Here we show that the memory trace that causes stabilization reflects not just the latest percept, but perception during a much longer period. That is, the choice between competing percepts at stimulus reappearance is determined by an elaborate history of prior perception. Specifically, we demonstrate a seconds-long influence of the latest percept, as well as a more persistent influence based on the relative proportion of dominance during a preceding period of at least one minute. In case short-term perceptual history and long-term perceptual history are opposed (because perception has recently switched after prolonged stabilization), the long-term influence recovers after the effect of the latest percept has worn off, indicating independence between time scales. We accommodate these results by adding two positive adaptation terms, one with a short time constant and one with a long time constant, to a standard model of perceptual switching.

Decision-related pupil dilation reflects upcoming choice and individual bias

Significance A number of studies reported that the pupil dilates (under constant illumination) during decision-making. Pupil dilation is also associated with the brain-wide release of modulatory neurotransmitters. It has remained unknown which specific elements of decision processes drive pupil dilation. Using a visual detection task, we here show that pupil dilation is primarily driven during, and not at the end of, a protracted decision. Further, pupil dilation differentiates between “yes” and “no” choices for conservative subjects deciding yes against their bias. Thus, pupil dilation reveals the content of the evolving decision and the decision maker’s attitude. These findings have important implications for interpreting decision-related brain activity. They also point to a possible role of neuromodulation in interacting with decision biases. A number of studies have shown that pupil size increases transiently during effortful decisions. These decision-related changes in pupil size are mediated by central neuromodulatory systems, which also influence the internal state of brain regions engaged in decision making. It has been proposed that pupil-linked neuromodulatory systems are activated by the termination of decision processes, and, consequently, that these systems primarily affect the postdecisional brain state. Here, we present pupil results that run contrary to this proposal, suggesting an important intradecisional role. We measured pupil size while subjects formed protracted decisions about the presence or absence (“yes” vs. “no”) of a visual contrast signal embedded in dynamic noise. Linear systems analysis revealed that the pupil was significantly driven by a sustained input throughout the course of the decision formation. This sustained component was larger than the transient component during the final choice (indicated by button press). The overall amplitude of pupil dilation during decision formation was bigger before yes than no choices, irrespective of the physical presence of the target signal. Remarkably, the magnitude of this pupil choice effect (yes > no) reflected the individual criterion: it was strongest in conservative subjects choosing yes against their bias. We conclude that the central neuromodulatory systems controlling pupil size are continuously engaged during decision formation in a way that reveals how the upcoming choice relates to the decision maker’s attitude. Changes in brain state seem to interact with biased decision making in the face of uncertainty.

GABA Shapes the Dynamics of Bistable Perception

Sometimes, perception fluctuates spontaneously between two distinct interpretations of a constant sensory input. These bistable perceptual phenomena provide a unique window into the neural mechanisms that create the contents of conscious perception. Models of bistable perception posit that mutual inhibition between stimulus-selective neural populations in visual cortex plays a key role in these spontaneous perceptual fluctuations. However, a direct link between neural inhibition and bistable perception has not yet been established experimentally. Here, we link perceptual dynamics in three distinct bistable visual illusions (binocular rivalry, motion-induced blindness, and structure from motion) to measurements of gamma-aminobutyric acid (GABA) concentrations in human visual cortex (as measured with magnetic resonance spectroscopy) and to pharmacological stimulation of the GABAA receptor by means of lorazepam. As predicted by a model of neural interactions underlying bistability, both higher GABA concentrations in visual cortex and lorazepam administration induced slower perceptual dynamics, as reflected in a reduced number of perceptual switches and a lengthening of percept durations. Thus, we show that GABA, the main inhibitory neurotransmitter, shapes the dynamics of bistable perception. These results pave the way for future studies into the competitive neural interactions across the visual cortical hierarchy that elicit conscious perception.

The reference frame of the motion aftereffect is retinotopic

Although eye-, head- and body-movements can produce large-scale translations of the visual input on the retina, perception is notable for its spatiotemporal continuity. The visual system might achieve this by the creation of a detailed map in world coordinates--a spatiotopic representation. We tested the coordinate system of the motion aftereffect by adapting observers to translational motion and then tested (1) at the same retinal and spatial location (full aftereffect condition), (2) at the same retinal location, but at a different spatial location (retinotopic condition), (3) at the same spatial, but at a different retinal location (spatiotopic condition), or (4) at a different spatial and retinal location (general transfer condition). We used large stimuli moving at high speed to maximize the likelihood of motion integration across space. In a second experiment, we added a contrast-decrement detection task to the motion stimulus to ensure attention was directed at the adapting location. Strong motion aftereffects were found when observers were tested in the full and retinotopic aftereffect conditions. We also found a smaller aftereffect at the spatiotopic location but it did not differ from that at the location that was neither spatiotopic nor retinotopic. This pattern of results did not change when attention was explicitly directed at the adapting stimulus. We conclude that motion adaptation took place at retinotopic levels of visual cortex and that no spatiotopic interaction of motion adaptation and test occurred across saccades.

The reference frame of the tilt aftereffect.

Perceptual aftereffects provide a sensitive tool to investigate the influence of eye and head position on visual processing. There have been recent indications that the TAE is remapped around the time of a saccade to remain aligned to the adapting location in the world. Here, we investigate the spatial frame of reference of the TAE by independently manipulating retinal position, gaze orientation, and head orientation between adaptation and test. The results show that the critical factor in the TAE is the correspondence between the adaptation and test locations in a retinotopic frame of reference, whereas world- and head-centric frames of reference do not play a significant role. Our results confirm that adaptation to orientation takes place at retinotopic levels of visual processing. We suggest that the remapping process that plays a role in visual stability does not transfer feature gain information around the time of eye (or head) movements.

Flash suppression and flash facilitation in binocular rivalry

We show that previewing one half image of a binocular rivalry pair can cause it to gain initial dominance when the other half is added, a novel phenomenon we term flash facilitation. This is the converse of a known effect called flash suppression, where the previewed image becomes suppressed upon rivalrous presentation. The exact effect of previewing an image depends on both the duration and the contrast of the prior stimulus. Brief, low-contrast prior stimuli facilitate, whereas long, high-contrast ones suppress. These effects have both an eye-based component and a pattern-based component. Our results suggest that, instead of reflecting two unrelated mechanisms, both facilitation and suppression are manifestations of a single process that occurs progressively during presentation of the prior stimulus. The distinction between the two phenomena would then lie in the extent to which the process has developed during prior stimulation. This view is consistent with a neural model previously proposed to account for perceptual stabilization of ambiguous stimuli, suggesting a relation between perceptual stabilization and the present phenomena.

Opposite influence of perceptual memory on initial and prolonged perception of sensory ambiguity.

Observers continually make unconscious inferences about the state of the world based on ambiguous sensory information. This process of perceptual decision-making may be optimized by learning from experience. We investigated the influence of previous perceptual experience on the interpretation of ambiguous visual information. Observers were pre-exposed to a perceptually stabilized sequence of an ambiguous structure-from-motion stimulus by means of intermittent presentation. At the subsequent re-appearance of the same ambiguous stimulus perception was initially biased toward the previously stabilized perceptual interpretation. However, prolonged viewing revealed a bias toward the alternative perceptual interpretation. The prevalence of the alternative percept during ongoing viewing was largely due to increased durations of this percept, as there was no reliable decrease in the durations of the pre-exposed percept. Moreover, the duration of the alternative percept was modulated by the specific characteristics of the pre-exposure, whereas the durations of the pre-exposed percept were not. The increase in duration of the alternative percept was larger when the pre-exposure had lasted longer and was larger after ambiguous pre-exposure than after unambiguous pre-exposure. Using a binocular rivalry stimulus we found analogous perceptual biases, while pre-exposure did not affect eye-bias. We conclude that previously perceived interpretations dominate at the onset of ambiguous sensory information, whereas alternative interpretations dominate prolonged viewing. Thus, at first instance ambiguous information seems to be judged using familiar percepts, while re-evaluation later on allows for alternative interpretations.

The spatial scale of perceptual memory in ambiguous figure perception.

Ambiguous visual stimuli highlight the constructive nature of vision: perception alternates between two plausible interpretations of unchanging input. However, when a previously viewed ambiguous stimulus reappears, its earlier perception almost entirely determines the new interpretation; memory disambiguates the input. Here, we investigate the spatial properties of this perceptual memory, taking into account strong anisotropies in percept preference across the visual field. Countering previous findings, we show that perceptual memory is not confined to the location in which it was instilled. Rather, it spreads to noncontiguous regions of the visual field, falling off at larger distances. Furthermore, this spread of perceptual memory takes place in a frame of reference that is tied to the surface of the retina. These results place the neural locus of perceptual memory in retinotopically organized sensory cortical areas, with implications for the wider function of perceptual memory in facilitating stable vision in natural, dynamic environments.

A dissociation of attention and awareness in phase-sensitive but not phase-insensitive visual channels

The elements most vivid in our conscious awareness are the ones to which we direct our attention. Scientific study confirms the impression of a close bond between selective attention and visual awareness, yet the nature of this association remains elusive. Using visual afterimages as an index, we investigate neural processing of stimuli as they enter awareness and as they become the object of attention. We find evidence of response enhancement accompanying both attention and awareness, both in the phase-sensitive neural channels characteristic of early processing stages and in the phase-insensitive channels typical of higher cortical areas. The effects of attention and awareness on phase-insensitive responses are positively correlated, but in the same experiments, we observe no correlation between the effects on phase-sensitive responses. This indicates independent signatures of attention and awareness in early visual areas yet a convergence of their effects at more advanced processing stages.