Marnix Naber

Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes.

Declarative memories of personal experiences are a key factor in defining oneself as an individual, which becomes particularly evident when this capability is impaired. Assessing the physiological mechanisms of human declarative memory is typically restricted to patients with specific lesions and requires invasive brain access or functional imaging. We investigated whether the pupil, an accessible physiological measure, can be utilized to probe memories for complex natural visual scenes. During memory encoding, scenes that were later remembered elicited a stronger pupil constriction compared to scenes that were later forgotten. Thus, pupil size predicts success or failure of memory formation. In contrast, novel scenes elicited stronger pupil constriction than familiar scenes during retrieval. When viewing previously memorized scenes, those that were forgotten (misjudged as novel) still elicited stronger pupil constrictions than those correctly judged as familiar. Furthermore, pupil constriction was influenced more strongly if images were judged with high confidence. Thus, we propose that pupil constriction can serve as a marker of novelty. Since stimulus novelty modulates the efficacy of memory formation, our pupil measurements during learning indicate that the later forgotten images were perceived as less novel than the later remembered pictures. Taken together, our data provide evidence that pupil constriction is a physiological correlate of a neural novelty signal during formation and retrieval of declarative memories for complex, natural scenes.

Animal detection and identification in natural scenes: Image statistics and emotional valence

Humans process natural scenes rapidly and accurately. Low-level image features and emotional valence affect such processing but have mostly been studied in isolation. At which processing stage these factors operate and how they interact has remained largely unaddressed. Here, we briefly presented natural images and asked observers to report the presence or absence of an animal (detection), species of the detected animal (identification), and their confidence. In a second experiment, the same observers rated images with respect to their emotional affect and estimated their anxiety when imagining a real-life encounter with the depicted animal. We found that detection and identification improved with increasing image luminance, background contrast, animal saturation, and luminance plus color contrast between target and background. Surprisingly, animals associated with lower anxiety were detected faster and identified with higher confidence, and emotional affect was a better predictor of performance than anxiety. Pupil size correlated with detection, identification, and emotional valence judgments at different time points after image presentation. Remarkably, images of threatening animals induced smaller pupil sizes, and observers with higher mean anxiety ratings had smaller pupils on average. In sum, rapid visual processing depends on contrasts between target and background features rather than overall visual context, is negatively affected by anxiety, and finds its processing stages differentially reflected in the pupillary response.

Speed and Lateral Inhibition of Stimulus Processing Contribute to Individual Differences in Stroop-Task Performance

The Stroop task is a popular neuropsychological test that measures executive control. Strong Stroop interference is commonly interpreted in neuropsychology as a diagnostic marker of impairment in executive control, possibly reflecting executive dysfunction. However, popular models of the Stroop task indicate that several other aspects of color and word processing may also account for individual differences in the Stroop task, independent of executive control. Here we use new approaches to investigate the degree to which individual differences in Stroop interference correlate with the relative processing speed of word and color stimuli, and the lateral inhibition between visual stimuli. We conducted an electrophysiological and behavioral experiment to measure (1) how quickly an individual’s brain processes words and colors presented in isolation (P3 latency), and (2) the strength of an individual’s lateral inhibition between visual representations with a visual illusion. Both measures explained at least 40% of the variance in Stroop interference across individuals. As these measures were obtained in contexts not requiring any executive control, we conclude that the Stroop effect also measures an individual’s pre-set way of processing visual features such as words and colors. This study highlights the important contributions of stimulus processing speed and lateral inhibition to individual differences in Stroop interference, and challenges the general view that the Stroop task primarily assesses executive control.

The Spatial Origin of a Perceptual Transition in Binocular Rivalry

When the left and the right eye are simultaneously presented with incompatible images at overlapping retinal locations, an observer typically reports perceiving only one of the two images at a time. This phenomenon is called binocular rivalry. Perception during binocular rivalry is not stable; one of the images is perceptually dominant for a certain duration (typically in the order of a few seconds) after which perception switches towards the other image. This alternation between perceptual dominance and suppression will continue for as long the images are presented. A characteristic of binocular rivalry is that a perceptual transition from one image to the other generally occurs in a gradual manner: the image that was temporarily suppressed will regain perceptual dominance at isolated locations within the perceived image, after which its visibility spreads throughout the whole image. These gradual transitions from perceptual suppression to perceptual dominance have been labeled as traveling waves of perceptual dominance. In this study we investigate whether stimulus parameters affect the location at which a traveling wave starts. We varied the contrast, spatial frequency or motion speed in one of the rivaling images, while keeping the same parameter constant in the other image. We used a flash-suppression paradigm to force one of the rival images into perceptual suppression. Observers waited until the suppressed image became perceptually dominant again, and indicated the position at which this breakthrough from suppression occurred. Our results show that the starting point of a traveling wave during binocular rivalry is highly dependent on local stimulus parameters. More specifically, a traveling wave most likely started at the location where the contrast of the suppressed image was higher than that of the dominant one, the spatial frequency of the suppressed image was lower than that of the dominant one, and the motion speed of the suppressed image was higher than that of the dominant one. We suggest that a breakthrough from suppression to dominance occurs at the location where salience (the degree to which a stimulus element stands out relative to neighboring elements) of the suppressed image is higher than that of the dominant one. Our results further show that stimulus parameters affecting the temporal dynamics during continuous viewing of rival images described in other studies, also affect the spatial origin of traveling waves during binocular rivalry.

Improved human visuomotor performance and pupil constriction after choline supplementation in a placebo-controlled double-blind study

Only few nutrients are known to enhance cognition. Here we explore whether visuomotor performance can be improved through the intake of the nutrient choline, an essential chemical compound in a vertebrate’s diet. Choline is abundant in for example eggs and shrimps and many animal studies suggest that it serves as a cognitive enhancer. As choline is important for the communication between motor neurons and the control of skeletal muscles, we assumed that choline supplementation may have positive effects on action coordination in humans. A group of twenty-eight individuals ingested two grams of choline bitartrate or a placebo in two separate sessions. Seventy minutes post ingestion, participants performed a visuomotor aiming task in which they had to rapidly hit the centers of targets. Results showed that participants hit targets more centrally after choline supplementation. Pupil size (a cognition-sensitive biomarker) also significantly decreased after choline intake and correlated positively with the hit distance to the targets and the number of target misses, and negatively with reaction times. These findings point to a choline-induced bias towards action precision in the trade-off between speed and accuracy. The changes in pupil size suggest that choline uptake alters cholinergic functions in the nervous system.

No Acute Effects of Choline Bitartrate Food Supplements on Memory in Healthy, Young, Human Adults.

Choline is a dietary component and precursor of acetylcholine, a crucial neurotransmitter for memory-related brain functions. In two double-blind, placebo-controlled cross-over experiments, we investigated whether the food supplement choline bitartrate improved declarative memory and working memory in healthy, young students one to two hours after supplementation. In experiment 1, 28 participants performed a visuospatial working memory task. In experiment 2, 26 participants performed a declarative picture memorization task. In experiment 3, 40 participants performed a verbal working memory task in addition to the visuospatial working memory and declarative picture task. All tasks were conducted approximately 60 minutes after the ingestion of 2.0–2.5g of either choline bitartrate or placebo. We found that choline did not significantly enhance memory performance during any of the tasks. The null hypothesis that choline does not improve memory performance as compared to placebo was strongly supported by Bayesian statistics. These results are in contrast with animal studies suggesting that choline supplementation boosts memory performance and learning. We conclude that choline likely has no acute effects on cholinergic memory functions in healthy human participants.

Eye tracking under dichoptic viewing conditions: a practical solution

In several research contexts it is important to obtain eye-tracking measures while presenting visual stimuli independently to each of the two eyes (dichoptic stimulation). However, the hardware that allows dichoptic viewing, such as mirrors, often interferes with high-quality eye tracking, especially when using a video-based eye tracker. Here we detail an approach to combining mirror-based dichoptic stimulation with video-based eye tracking, centered on the fact that some mirrors, although they reflect visible light, are selectively transparent to the infrared wavelength range in which eye trackers record their signal. Although the method we propose is straightforward, affordable (on the order of US

Commentary: Is the Frontal Lobe Involved in Conscious Perception?

1,000) and easy to implement, for many purposes it makes for an improvement over existing methods, which tend to require specialized equipment and often compromise on the quality of the visual stimulus and/or the eye tracking signal. The proposed method is compatible with standard display screens and eye trackers, and poses no additional limitations on the quality or nature of the stimulus presented or the data obtained. We include an evaluation of the quality of eye tracking data obtained using our method, and a practical guide to building a specific version of the setup used in our laboratories.

Pupillary Responses to Robotic and Human Emotions: The Uncanny Valley and Media Equation Confirmed

Like any other field, the field of consciousness research benefits from a careful distinction between the concepts involved. An example is the distinction between the state of being conscious (e.g., whether someone is awake) and the contents of consciousness (e.g., whether someone perceives a dress as white or blue). A similar type of distinction can contribute to the resolution of a debate regarding the role of the frontal cortex in conscious perception. In a recent publication Safavi et al. (2014) responded to conclusions drawn in a study regarding the role of frontal cortex in conscious perception. This study, by Frassle et al. (2014), employed binocular rivalry to show that well-established frontal BOLD correlates of perceptual switches (Lumer et al., 1998; Sterzer and Kleinschmidt, 2007) were strongly diminished when participants passively viewed these switches rather than reporting them. Frassle and co-workers (among whom the present papers first author) concluded: “frontal areas are associated with active report and introspection rather than with rivalry per se.” This statement is a bit audacious, as it rules out any role of frontal areas in rivalry other than their role in reporting perception. As such, Safavi and co-workers draw into question this conclusion, based on evidence indicating that neural activity in frontal areas, in particular in the lateral prefrontal cortex, reflects the contents of consciousness in paradigms that do not involve active report.

Similarity of Actions Depends on the Functionality of Previously Observed Actions

Physiological responses during human–robots interaction are useful alternatives to subjective measures of uncanny feelings for nearly humanlike robots (uncanny valley) and comparable emotional responses between humans and robots (media equation). However, no studies have employed the easily accessible measure of pupillometry to confirm the uncanny valley and media equation hypotheses, evidence in favor of the existence of these hypotheses in interaction with emotional robots is scarce, and previous studies have not controlled for low level image statistics across robot appearances. We therefore recorded pupil size of 40 participants that viewed and rated pictures of robotic and human faces that expressed a variety of basic emotions. The robotic faces varied along the dimension of human likeness from cartoonish to humanlike. We strictly controlled for confounding factors by removing backgrounds, hair, and color, and by equalizing low level image statistics. After the presentation phase, participants indicated to what extent the robots appeared uncanny and humanlike, and whether they could imagine social interaction with the robots in real life situations. The results show that robots rated as nearly humanlike scored higher on uncanniness, scored lower on imagined social interaction, evoked weaker pupil dilations, and their emotional expressions were more difficult to recognize. Pupils dilated most strongly to negative expressions and the pattern of pupil responses across emotions was highly similar between robot and human stimuli. These results highlight the usefulness of pupillometry in emotion studies and robot design by confirming the uncanny valley and media equation hypotheses.