Correlated P300b and phasic pupil-dilation responses to motivationally significant stimuli.

Motivationally significant events like oddball stimuli elicit both a characteristic event-related potential (ERPs) known as P300 and a set of autonomic responses including a phasic pupil dilation. Although co-occurring, P300 and pupil-dilation responses to oddball events have been repeatedly found to be uncorrelated, suggesting separate origins. We re-examined their relationship in the context of a three-stimulus version of the auditory oddball task, independently manipulating the frequency (rare vs. repeated) and motivational significance (relevance for the participant's task) of the stimuli. We used independent component analysis to derive a P300b component from EEG traces and linear modeling to separate a stimulus-related pupil-dilation response from a potentially confounding action-related response. These steps revealed that, once the complexity of ERP and pupil-dilation responses to oddball targets is accounted for, the amplitude of phasic pupil dilations and P300b are tightly and positively correlated (across participants: r = .69 p = .002), supporting their coordinated generation.

Effect of fasting on short-term visual plasticity in adult humans.

Brain plasticity and function is impaired in conditions of metabolic dysregulation, such as obesity. Less is known on whether brain function is also affected by transient and physiological metabolic changes, such as the alternation between fasting and fed state. Here we asked whether these changes affect the transient shift of ocular dominance that follows short-term monocular deprivation, a form of homeostatic plasticity. We further asked whether variations in three of the main metabolic and hormonal pathways affected in obesity (glucose metabolism, leptin signalling and fatty acid metabolism) correlate with plasticity changes. We measured the effects of 2 h monocular deprivation in three conditions: post-absorptive state (fasting), after ingestion of a standardised meal and during infusion of glucagon-like peptide-1 (GLP-1), an incretin physiologically released upon meal ingestion that plays a key role in glucose metabolism. We found that short-term plasticity was less manifest in fasting than in fed state, whereas GLP-1 infusion did not elicit reliable changes compared to fasting. Although we confirmed a positive association between plasticity and supraphysiological GLP-1 levels, achieved by GLP-1 infusion, we found that none of the parameters linked to glucose metabolism could predict the plasticity reduction in the fasting versus fed state. Instead, this was selectively associated with the increase in plasma beta-hydroxybutyrate (B-OH) levels during fasting, which suggests a link between neural function and energy substrates alternative to glucose. These results reveal a previously unexplored link between homeostatic brain plasticity and the physiological changes associated with the daily fast-fed cycle.

Measuring the reliability of binocular rivalry.

Binocular rivalry is a widely used tool in sensory and cognitive neuroscience to investigate different aspects of vision and cognition. The dynamics of binocular rivalry (e.g., duration of perceptual dominance phases and mixed percept proportions) differ across individuals; based on rivalry dynamics, it is also possible to calculate an index of ocular dominance (by comparing the perceptual dominance of the images in the two eyes). In this study, we investigated the reliability of binocular rivalry dynamics using different methods for dichoptic stimulation and different rivalry stimuli. For the three main indices we defined (ocular dominance, phase durations and mixed percept proportions), we found a high test-retest reliability across sessions. Moreover, the test-retest reliability of the ocular dominance index was predictable from its internal consistency, supporting its stability over time. Phase durations and mixed percept proportions, in contrast, had worse test-retest reliability than expected based on internal consistency, indicating that these parameters are susceptible to state-dependent changes. Our results support the use of the ocular dominance index and binocular rivalry in the measurement of sensory eye dominance and its plasticity, but advise caution when investigating the association between phase durations or mixed percepts and stable characteristics like psychological traits or disorders.

Development of local-global preference in vision and haptics.

We aimed to advance our understanding of local-global preference by exploring its developmental path within and across sensory modalities: vision and haptics. Neurotypical individuals from six years of age through adulthood completed a similarity judgement task with hierarchical haptic or visual stimuli made of local elements (squares or triangles) forming a global shape (a square or a triangle). Participants chose which of two probes was more similar to a target: the one sharing the global shape (but different local shapes) or the one with the same local shapes (but different global shape). Across trials, we independently varied the size of the local elements and that of the global configuration-the latter was varied by manipulating local element density while keeping their numerosity constant. We found that the size of local elements (but not global size) modulates the effects of age and modality. For stimuli with smaller local elements, the proportion of global responses increased with age and was similar for visual and haptic stimuli. However, for stimuli made of our largest local elements, the global preference was reduced or absent, particularly in haptics, regardless of age. These results suggest that vision and haptics progressively converge toward similar global preference with age, but residual differences across modalities and across individuals may be observed, depending on the characteristics of the stimuli.

Bariatric surgery restores visual cortical plasticity in nondiabetic subjects with obesity.

BACKGROUND/OBJECTIVES: Obesity leads to changes in synaptic plasticity. We aimed at investigating the impact of bariatric surgery (RYGB) on visual neural plasticity (NP) and its relationship with the main gut peptides, leptin, and brain-derived neurotrophic factor (BDNF). SUBJECTS/METHODS: NP was assessed testing binocular rivalry before and after 2 h of monocular deprivation (index of visual brain plasticity) in 15 subjects with obesity (age 42.3 ± 9.8 years; BMI 46.1 ± 4.9 kg/m2) before and after RYGB. Gut peptides, leptin, and BDNF were obtained at baseline and 6 months after surgery in 13 subjects. RESULTS: A significant reduction in BMI (p < 0.001 vs. baseline) and a significant increase of disposition index (DI, p = 0.02 vs baseline) were observed after RYGB. Total and active GLP-1 release in response to glucose ingestion significantly increased after RYGB, while no changes occurred in VIP, GIP, and BDNF levels. Fasting leptin concentration was lower after RYGB (p = 0.001 vs. baseline). Following RYGB, NP was progressively restored (p < 0.002). NP was correlated with DI and fasting glucose at baseline (r = 0.75, p = 0.01; r = -0.7, p = 0.02; respectively), but not with BMI. A positive correlation between post-pre-RYGB changes in AUCactive GLP-1 and NP was observed (r = 0.70, p < 0.01). Leptin was inversely correlated with NP 6 months after surgery (r = -0.63, p = 0.02). No correlation was observed between GIP, VIP, BDNF, and NP. CONCLUSIONS: Visual plasticity is altered in subjects with obesity, and it can be restored after RYGB. The improvement may be mediated by amelioration of insulin sensitivity, increased GLP-1 levels, and reduced leptin levels.

Fast saccadic eye-movements in humans suggest that numerosity perception is automatic and direct.

Fast saccades are rapid automatic oculomotor responses to salient and ecologically important visual stimuli such as animals and faces. Discriminating the number of friends, foe, or prey may also have an evolutionary advantage. In this study, participants were asked to saccade rapidly towards the more numerous of two arrays. Participants could discriminate numerosities with high accuracy and great speed, as fast as 190 ms. Intermediate numerosities were more likely to elicit fast saccades than very low or very high numerosities. Reaction-times for vocal responses (collected in a separate experiment) were slower, did not depend on numerical range, and correlated only with the slow not the fast saccades, pointing to different systems. The short saccadic reaction-times we observe are surprising given that discrimination using numerosity estimation is thought to require a relatively complex neural circuit, with several relays of information through the parietal and prefrontal cortex. Our results suggest that fast numerosity-driven saccades may be generated on a single feed-forward pass of information recruiting a primitive system that cuts through the cortical hierarchy and rapidly transforms the numerosity information into a saccade command.

Pupillometry correlates of visual priming, and their dependency on autistic traits.

In paradigms of visual search where the search feature (say color) can change from trial to trials, responses are faster for trials where the search color is repeated than when it changes. This is a clear example of "priming" of attention. Here we test whether the priming effects can be revealed by pupillometry, and also whether they are related to autistic-like personality traits, as measured by the Autism-Spectrum Quotient (AQ). We repeated Maljkovic and Nakayama's (1994) classic priming experiment, asking subjects to identify rapidly the shape of a singleton target defined by color. As expected, reaction times were faster when target color repeated, and the effect accumulated over several trials; but the magnitude of the effect did not correlate with AQ. Reaction times were also faster when target position was repeated, again independent of AQ. Presentation of stimuli caused the pupil to dilate, and the magnitude of dilation was greater for switched than repeated trials. This effect did not accumulate over trials, and did not correlate with the reaction times difference, suggesting that the two indexes measure independent aspects of the priming phenomenon. Importantly, the amplitude of pupil modulation correlated negatively with AQ, and was significant only for those participants with low AQ. The results confirm that pupillometry can track perceptual and attentional processes, and furnish useful information unobtainable from standard psychophysics, including interesting dependencies on personality traits.

Using psychophysical performance to predict short-term ocular dominance plasticity in human adults.

Binocular rivalry has become an important index of visual performance, both to measure ocular dominance or its plasticity, and to index bistable perception. We investigated its interindividual variability across 50 normal adults and found that the duration of dominance phases in rivalry is linked with the duration of dominance phases in another bistable phenomenon (structure from motion). Surprisingly, it also correlates with the strength of center-surround interactions (indexed by the tilt illusion), suggesting a common mechanism supporting both competitive interactions: center-surround and rivalry. In a subset of 34 participants, we further investigated the variability of short-term ocular dominance plasticity, measured with binocular rivalry before and after 2 hours of monocular deprivation. We found that ocular dominance shifts in favor of the deprived eye and that a large portion of ocular dominance variability after deprivation can be predicted from the dynamics of binocular rivalry before deprivation. The single best predictor is the proportion of mixed percepts (phases without dominance of either eye) before deprivation, which is positively related to ocular dominance unbalance after deprivation. Another predictor is the duration of dominance phases, which interacts with mixed percepts to explain nearly 50% of variance in ocular dominance unbalance after deprivation. A similar predictive power is achieved by substituting binocular rivalry dominance phase durations with tilt illusion magnitude, or structure from motion phase durations. Thus, we speculate that ocular dominance plasticity is modulated by two types of signals, estimated from psychophysical performance before deprivation, namely, interocular inhibition (promoting binocular fusion, hence mixed percepts) and inhibition for perceptual competition (promoting longer dominance phases and stronger center-surround interactions).

Exenatide modulates visual cortex responses.

BACKGROUND: Increasing evidence suggests that metabolism affects brain physiology. Here, we examine the effect of GLP-1 on simple visual-evoked functional Magnetic Resonance Imaging (fMRI) responses in cortical areas. METHODS: Lean (n = 10) and nondiabetic obese (n = 10) subjects received exenatide (a GLP-1 agonist) or saline infusion, and fMRI responses to visual stimuli (food and nonfood images) were recorded. We analysed the effect of exenatide on fMRI signals across the cortical surface with special reference to the visual areas. We evaluated the effects of exenatide on the raw fMRI signal and on the fMRI signal change during visual stimulation (vs rest). RESULTS: In line with previous studies, we find that exenatide eliminates the preference for food (over nonfood) images present under saline infusion in high-level visual cortex (temporal pole). In addition, we find that exenatide (vs saline) also modulates the response of early visual areas, enhancing responses to both food and nonfood images in several extrastriate occipital areas, similarly in obese and lean participants. Unexpectedly, exenatide increased fMRI raw signals (signal intensity during rest periods without stimulation) in a large occipital region, which were negatively correlated to BMI. CONCLUSIONS: In both lean and obese individuals, exenatide affects neural processing in visual cortex, both in early visual areas and in higher order areas. This effect may contribute to the known effect of GLP1 analogues on food-related behaviour.

Trans-saccadic integration of orientation information.

Does visual processing start anew after each eye movement, or is information integrated across saccades? Here we test a strong prediction of the integration hypothesis: that information acquired after a saccade interferes with the perception of images acquired before the saccade. We investigate perception of a basic visual feature, grating orientation, and we take advantage of a delayed interference phenomenon-in human participants, the reported orientation of a target grating, briefly presented at an eccentric location, is strongly biased toward the orientation of flanker gratings that are flashed shortly after the target. Crucially, we find that the effect is the same whether or not a saccade is made during the delay interval even though the eye movement produces a large retinotopic separation between target and flankers. However, the trans-saccadic effect nearly vanishes when flankers are displaced to a different screen location even when this location matches the retinotopic coordinates of the target. We conclude that information about grating orientation is integrated across saccades within a spatial region that is defined in external coordinates and thereby is stable in spite of the movement of the eyes.

Short-Term Monocular Deprivation Enhances Physiological Pupillary Oscillations.

Short-term monocular deprivation alters visual perception in adult humans, increasing the dominance of the deprived eye, for example, as measured with binocular rivalry. This form of plasticity may depend upon the inhibition/excitation balance in the visual cortex. Recent work suggests that cortical excitability is reliably tracked by dilations and constrictions of the pupils of the eyes. Here, we ask whether monocular deprivation produces a systematic change of pupil behavior, as measured at rest, that is independent of the change of visual perception. During periods of minimal sensory stimulation (in the dark) and task requirements (minimizing body and gaze movements), slow pupil oscillations, "hippus," spontaneously appear. We find that hippus amplitude increases after monocular deprivation, with larger hippus changes in participants showing larger ocular dominance changes (measured by binocular rivalry). This tight correlation suggests that a single latent variable explains both the change of ocular dominance and hippus. We speculate that the neurotransmitter norepinephrine may be implicated in this phenomenon, given its important role in both plasticity and pupil control. On the practical side, our results indicate that measuring the pupil hippus (a simple and short procedure) provides a sensitive index of the change of ocular dominance induced by short-term monocular deprivation, hence a proxy for plasticity.

Corrigendum to "Short-Term Monocular Deprivation Enhances Physiological Pupillary Oscillations".

[This corrects the article DOI: 10.1155/2017/6724631.].

Resting-State Retinotopic Organization in the Absence of Retinal Input and Visual Experience.

Early visual areas have neuronal receptive fields that form a sampling mosaic of visual space, resulting in a series of retinotopic maps in which the same region of space is represented in multiple visual areas. It is not clear to what extent the development and maintenance of this retinotopic organization in humans depend on retinal waves and/or visual experience. We examined the corticocortical receptive field organization of resting-state BOLD data in normally sighted, early blind, and anophthalmic (in which both eyes fail to develop) individuals and found that resting-state correlations between V1 and V2/V3 were retinotopically organized for all subject groups. These results show that the gross retinotopic pattern of resting-state connectivity across V1-V3 requires neither retinal waves nor visual experience to develop and persist into adulthood. Significance statement: Evidence from resting-state BOLD data suggests that the connections between early visual areas develop and are maintained even in the absence of retinal waves and visual experience.

Dissociable saccadic suppression of pupillary and perceptual responses to light.

We measured pupillary constrictions in response to full-screen flashes of variable luminance, occurring either at the onset of a saccadic eye movement or well before/after it. A large fraction of perisaccadic flashes were undetectable to the subjects, consistent with saccadic suppression of visual sensitivity. Likewise, pupillary responses to perisaccadic flashes were strongly suppressed. However, the two phenomena appear to be dissociable. Across subjects and luminance levels of the flash stimulus, there were cases in which conscious perception of the flash was completely depleted yet the pupillary response was clearly present, as well as cases in which the opposite occurred. On one hand, the fact that pupillary light responses are subject to saccadic suppression reinforces evidence that this is not a simple reflex but depends on the integration of retinal illumination with complex "extraretinal" cues. On the other hand, the relative independence of pupillary and perceptual responses suggests that suppression acts separately on these systems-consistent with the idea of multiple visual pathways that are differentially affected by saccades.

Spatial attention increases the pupillary response to light changes.

We measured pupil size in adult human subjects while we manipulated both the luminance of the visual scene and the location of attention. We found that, with central fixation maintained, pupillary constrictions and dilations evoked by peripheral luminance increments and decrements are larger when spatial attention is covertly (i.e., with no eye movements) directed to the stimulus region versus when it is directed to the opposite hemifield. Irrespective of the size of the attended region (focused at the center of the stimulus or spread within and outside the stimulus), the attentional enhancement is large: more than 20% of the response to stimuli in the unattended hemifield. This indicates that a sizable portion of this simple ocular behavior­often considered a subcortical "reflex"­in fact depends on cortical processing. Together, these features indicate that pupillometry is not only an index of retinal and brainstem function, but also an objective measure of complex constructs such as attention and its effects on sensory processing.

Attention to bright surfaces enhances the pupillary light reflex.

One longstanding question is how early in the visual system attention exerts its influence. Here we show that an effect of attention can be measured at the earliest possible stage of visual information processing, as a change in the optics of the eye. We tested human subjects and found that covertly attending to bright surfaces results in an enhanced pupillary light reflex (PLR)-the pupillary constriction that occurs in response to light increments. The PLR optimizes the optical quality of the retinal image across illumination conditions, increasing sensitivity by modulating retinal illumination, and improving acuity by reducing spherical aberrations. The attentional modulation of the PLR that we describe constitutes a new mechanism through which vision is affected by attention; we discuss three alternatives for the neural substrates of this effect, including the possibility that attention might act indirectly, via its well established effects in early visual cortex.

Pupil size reflects the focus of feature-based attention.

We measured pupil size in adult human subjects while they selectively attended to one of two surfaces, bright and dark, defined by coherently moving dots. The two surfaces were presented at the same location; therefore, subjects could select the cued surface only on the basis of its features. With no luminance change in the stimulus, we find that pupil size was smaller when the bright surface was attended and larger when the dark surface was attended: an effect of feature-based (or surface-based) attention. With the same surfaces at nonoverlapping locations, we find a similar effect of spatial attention. The pupil size modulation cannot be accounted for by differences in eye position and by other variables known to affect pupil size such as task difficulty, accommodation, or the mere anticipation (imagery) of bright/dark stimuli. We conclude that pupil size reflects not just luminance or cognitive state, but the interaction between the two: it reflects which luminance level in the visual scene is relevant for the task at hand.

Pupillometry indexes ocular dominance plasticity.

Short-term monocular deprivation in normally sighted adult humans produces a transient shift of ocular dominance, boosting the deprived eye. This effect has been documented with both perceptual tests and through physiological recordings, but no previous study simultaneously measured physiological responses and the perceptual effects of deprivation. Here we propose an integrated experimental paradigm that combines binocular rivalry with pupillometry, to introduce an objective physiological index of ocular dominance plasticity, acquired concurrently with perceptual testing. Ten participants reported the perceptual dynamics of binocular rivalry, while we measured pupil diameter. Stimuli were a white and a black disk, each presented monocularly. Rivalry dynamics and pupil-size traces were compared before and after 2 h of monocular deprivation, achieved by applying a translucent patch over the dominant eye. Consistent with prior research, we observed that monocular deprivation boosts the deprived-eye signal and consequently increases ocular dominance. In line with previous studies, we also observed subtle but systematic modulations of pupil size that tracked alternations between exclusive dominance phases of the black or white disk. Following monocular deprivation, the amplitude of these pupil-size modulations increased, which is consistent with the post-deprivation boost of the deprived eye and the increase of ocular dominance. This provides evidence that deprivation impacts the effective strength of monocular visual stimuli, coherently affecting perceptual reports and the automatic and unconscious regulation of pupil diameter. Our results show that a combined paradigm of binocular rivalry and pupillometry gives new insights into the physiological mechanisms underlying deprivation effects.

Adaptation to numerosity affects the pupillary light response.

We recently showed that the gain of the pupillary light response depends on numerosity, with weaker responses to fewer items. Here we show that this effect holds when the stimuli are physically identical but are perceived as less numerous due to numerosity adaptation. Twenty-eight participants adapted to low (10 dots) or high (160 dots) numerosities and subsequently watched arrays of 10-40 dots, with variable or homogeneous dot size. Luminance was constant across all stimuli. Pupil size was measured with passive viewing, and the effects of adaptation were checked in a separate psychophysical session. We found that perceived numerosity was systematically lower, and pupillary light responses correspondingly smaller, following adaptation to high rather than low numerosities. This is consistent with numerosity being a primary visual feature, spontaneously encoded even when task irrelevant, and affecting automatic and unconscious behaviours like the pupillary light response.

Transient spatiotopic integration across saccadic eye movements mediates visual stability.

Eye movements pose major problems to the visual system, because each new saccade changes the mapping of external objects on the retina. It is known that stimuli briefly presented around the time of saccades are systematically mislocalized, whereas continuously visible objects are perceived as spatially stable even when they undergo large transsaccadic displacements. In this study we investigated the relationship between these two phenomena and measured how human subjects perceive the position of pairs of bars briefly displayed around the time of large horizontal saccades. We show that they interact strongly, with the perisaccadic bar being drawn toward the other, dramatically altering the pattern of perisaccadic mislocalization. The interaction field extends over a wide range (200 ms and 20°) and is oriented along the retinotopic trajectory of the saccade-induced motion, suggesting a mechanism that integrates pre- and postsaccadic stimuli at different retinal locations but similar external positions. We show how transient changes in spatial integration mechanisms, which are consistent with the present psychophysical results and with the properties of "remapping cells" reported in the literature, can create transient craniotopy by merging the distinct retinal images of the pre- and postsaccadic fixations to signal a single stable object.