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.

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.

Active vision gates ocular dominance plasticity in human adults.

Primary visual cortex (V1) retains a form of plasticity in adult humans: a brief period of monocular deprivation induces an enhanced response to the deprived eye, which can stabilize into a consolidated plastic change1,2 despite unaltered thalamic input3. This form of homeostatic plasticity in adults is thought to act through neuronal competition between the representations of the two eyes, which are still separate in primary visual cortex4,5. During monocular occlusion, neurons of the deprived eye are thought to increase response gain given the absence of visual input, leading to the post-deprivation enhancement. If the decrease of reliability of the monocular response is crucial to establish homeostatic plasticity, this could be induced in several different ways. There is increasing evidence that V1 processing is affected by voluntary action, allowing it to take into account the visual effects of self-motion6, important for efficient active vision7. Here we asked whether ocular dominance homeostatic plasticity could be elicited without degrading the quality of monocular visual images but simply by altering their role in visuomotor control by introducing a visual delay in one eye while participants actively performed a visuomotor task; this causes a discrepancy between what the subject sees and what he/she expects to see. Our results show that homeostatic plasticity is gated by the consistency between the monocular visual inputs and a person's actions, suggesting that action not only shapes visual processing but may also be essential for plasticity in adults.

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.

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.

Attention cueing in rivalry: insights from pupillometry.

We used pupillometry to evaluate the effects of attention cueing on perceptual bi-stability, as reported by adult human observers. Perceptual alternations and pupil diameter were measured during two forms of rivalry, generated by presenting a white and a black disk to the two eyes (binocular rivalry) or splitting the disks between eyes (interocular grouping rivalry). In line with previous studies, we found that subtle pupil size modulations (about 0.05 mm) tracked alternations between exclusive dominance phases of the black or white disk. These pupil responses were larger for perceptually stronger stimuli: presented to the dominant eye or with physically higher luminance contrast. However, cueing of endogenous attention to one of the rivaling percepts did not affect pupil modulations during exclusive dominance phases. This was observed despite the reliable effects of endogenous attention on perceptual dominance, which shifted in favor of the cued percept by about 10%. The results were comparable for binocular and interocular grouping rivalry. Cueing only had a marginal modulatory effect on pupil size during mixed percepts in binocular rivalry. This may suggest that, rather than acting by modulating perceptual strength, endogenous attention primarily acts during periods of unresolved competition, which is compatible with attention being automatically directed to the rivaling stimuli during periods of exclusive dominance and thereby sustaining perceptual alternations.Significance StatementBinocular rivalry depends on attention. When it is diverted away from the stimuli, perceptual alternations slow down; when it is preferentially directed to one stimulus, perception lingers more on it, consistent with attention enhancing the effective strength of the rivaling stimuli. Here we introduce pupillometry as a means to indirectly track changes in effective stimulus strength. We find that pupil size accurately tracks perceived luminance during two forms of rivalry: binocular rivalry and interocular grouping rivalry. Both show robust effects of attention cueing on perceptual dominance, but pupil modulations during exclusive dominance are unaffected by cueing. This suggests that endogenous attention does not affect perceptual strength during exclusive dominance, though it might do so during transition phases.

Vision: Optimizing each glimpse.

A new study uses a rigorous approach to isolate the consequences of eye movements on cortical visual processing, showing that our visual system does not shut down during saccades but specifically modulates sensitivity to selected stimuli.

Contextual Information Modulates Pupil Size in Autistic Children.

Recent Bayesian models suggest that perception is more "data-driven" and less dependent on contextual information in autistic individuals than others. However, experimental tests of this hypothesis have given mixed results, possibly due to the lack of objectivity of the self-report methods typically employed. Here we introduce an objective no-report paradigm based on pupillometry to assess the processing of contextual information in autistic children, together with a comparison clinical group. After validating in neurotypical adults a child-friendly pupillometric paradigm, in which we embedded test images within an animation movie that participants watched passively, we compared pupillary response to images of the sun and meaningless control images in children with autism vs. age- and IQ-matched children presenting developmental disorders unrelated to the autistic spectrum. Both clinical groups showed stronger pupillary constriction for the sun images compared with control images, like the neurotypical adults. However, there was no detectable difference between autistic children and the comparison group, despite a significant difference in pupillary light responses, which were enhanced in the autistic group. Our report introduces an objective technique for studying perception in clinical samples and children. The lack of statistically significant group differences in our tests suggests that autistic children and the comparison group do not show large differences in perception of these stimuli. This opens the way to further studies testing contextual processing at other levels of perception.

Short-term plasticity in the human visual thalamus.

While there is evidence that the visual cortex retains a potential for plasticity in adulthood, less is known about the subcortical stages of visual processing. Here, we asked whether short-term ocular dominance plasticity affects the human visual thalamus. We addressed this question in normally sighted adult humans, using ultra-high field (7T) magnetic resonance imaging combined with the paradigm of short-term monocular deprivation. With this approach, we previously demonstrated transient shifts of perceptual eye dominance and ocular dominance in visual cortex (Binda et al., 2018). Here, we report evidence for short-term plasticity in the ventral division of the pulvinar (vPulv), where the deprived eye representation was enhanced over the nondeprived eye. This vPulv plasticity was similar as previously seen in visual cortex and it was correlated with the ocular dominance shift measured behaviorally. In contrast, there was no effect of monocular deprivation in two adjacent thalamic regions: dorsal pulvinar and Lateral Geniculate Nucleus. We conclude that the visual thalamus retains potential for short-term plasticity in adulthood; the plasticity effect differs across thalamic subregions, possibly reflecting differences in their corticofugal connectivity.

The pupil responds spontaneously to perceived numerosity.

Although luminance is the main determinant of pupil size, the amplitude of the pupillary light response is also modulated by stimulus appearance and attention. Here we ask whether perceived numerosity modulates the pupillary light response. Participants passively observed arrays of black or white dots of matched physical luminance but different physical or illusory numerosity. In half the patterns, pairs of dots were connected by lines to create dumbbell-like shapes, inducing an illusory underestimation of perceived numerosity; in the other half, connectors were either displaced or removed. Constriction to white arrays and dilation to black were stronger for patterns with higher perceived numerosity, either physical or illusory, with the strength of the pupillary light response scaling with the perceived numerosity of the arrays. Our results show that even without an explicit task, numerosity modulates a simple automatic reflex, suggesting that numerosity is a spontaneously encoded visual feature.

Predictive visuo-motor communication through neural oscillations.

The mechanisms coordinating action and perception over time are poorly understood. The sensory cortex needs to prepare for upcoming changes contingent on action, and this requires temporally precise communication that takes into account the variable delays between sensory and motor processing. Several theorists1,2 have proposed synchronization of the endogenous oscillatory activity observed in most regions of the brain3 as the basis for an efficient and flexible communication protocol between distal brain areas,2,4 a concept known as "communication through coherence." Synchronization of endogenous oscillations5,6 occurs after a salient sensory stimulus, such as a flash or a sound,7-11 and after a voluntary action,12-18 and this directly impacts perception, causing performance to oscillate rhythmically over time. Here we introduce a novel fMRI paradigm to probe the neural sources of oscillations, based on the concept of perturbative signals, which overcomes the low temporal resolution of BOLD signals. The assumption is that a synchronized endogenous rhythm will modulate cortical excitability rhythmically, which should be reflected in the BOLD responses to brief stimuli presented at different phases of the oscillation cycle. We record rhythmic oscillations of V1 BOLD synchronized by a simple voluntary action, in phase with behaviorally measured oscillations in visual sensitivity in the theta range. The functional connectivity between V1 and M1 also oscillates at the same rhythm. By demonstrating oscillatory temporal coupling between primary motor and sensory cortices, our results strongly implicate communication through coherence to achieve precise coordination and to encode sensory-motor timing.

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.

Objective pupillometry shows that perceptual styles covary with autistic-like personality traits.

We measured the modulation of pupil size (in constant lighting) elicited by observing transparent surfaces of black and white moving dots, perceived as a cylinder rotating about its vertical axis. The direction of rotation was swapped periodically by flipping stereo-depth of the two surfaces. Pupil size modulated in synchrony with the changes in front-surface color (dilating when black). The magnitude of pupillary modulation was larger for human participants with higher Autism-Spectrum Quotient (AQ), consistent with a local perceptual style, with attention focused on the front surface. The modulation with surface color, and its correlation with AQ, was equally strong when participants passively viewed the stimulus. No other indicator, including involuntary pursuit eye movements, covaried with AQ. These results reinforce our previous report with a similar bistable stimulus (Turi, Burr, & Binda, 2018), and go on to show that bistable illusory motion is not necessary for the effect, or its dependence on AQ.

Pupillary Responses Obey Emmert's Law and Co-vary with Autistic Traits.

We measured the pupil response to a light stimulus subject to a size illusion and found that stimuli perceived as larger evoke a stronger pupillary response. The size illusion depends on combining retinal signals with contextual 3D information; contextual processing is thought to vary across individuals, being weaker in individuals with stronger autistic traits. Consistent with this theory, autistic traits correlated negatively with the magnitude of pupil modulations in our sample of neurotypical adults; however, psychophysical measurements of the illusion did not correlate with autistic traits, or with the pupil modulations. This shows that pupillometry provides an accurate objective index of complex perceptual processes, particularly useful for quantifying interindividual differences, and potentially more informative than standard psychophysical measures.

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.

Spontaneous pupillary oscillations increase during mindfulness meditation.

A significant body of literature has shown that pupil size varies with cognitive and perceptual states [1,2]. Furthermore, the pupil diameter oscillates spontaneously at low frequencies, sometimes referred to as pupillary hippus [3,4]. Oscillation amplitude varies with many neural factors, including arousal and cortical excitability. Here we show that pupillary oscillations are modulated by mindfulness meditation, increasing by 53% compared to pre- and post-meditation baselines. The effect occurs only in trained meditators and is specific for low frequencies (below 1 Hz), with delta frequencies (1-5 Hz) unchanged. The study suggests that pupil size may be a useful marker of the altered cortical state during meditation.

Non-spatial skills differ in the front and rear peri-personal space.

In measuring behavioural and pupillary responses to auditory oddball stimuli delivered in the front and rear peri-personal space, we find that pupils dilate in response to rare stimuli, both target and distracters. Dilation in response to targets is stronger than the response to distracters, implying a task relevance effect on pupil responses. Crucially, pupil dilation in response to targets is also selectively modulated by the location of sound sources: stronger in the front than in the rear peri-personal space, in spite of matching behavioural performance. This supports the concept that even non-spatial skills, such as the ability to alert in response to behaviourally relevant events, are differentially engaged across subregions of the peri-personal space.

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).

A closer look at the timecourse of mind wandering: Pupillary responses and behaviour.

Mind wandering (MW) refers to the shift of attention away from a primary task and/or external environment towards thoughts unrelated to the task. Recent evidence has shown that pupillometry can be used as an objective marker of the onset and maintenance of externally-driven MW episodes. In the present study we aimed to further investigate pupillary changes associated with the onset and duration of self-reported MW episodes. We used a modified version of the joint behavioural-pupillometry paradigm we recently introduced. Participants were asked to perform a monotonous vigilance task which was intermixed with task-irrelevant cue-phrases (visually presented verbal cues); they were instructed to interrupt the task whenever a thought came to mind (self-caught method) and to indicate the trigger of their thought, if any. We found systematic pupil dilation after the presentation of verbal cues reported to have triggered MW, compared with other verbal cues presented during a supposedly on-task period (i.e., the period immediately following the resuming of the task after a self-caught interruption and MW report). These results confirm that pupil diameter is sensitive to the changes associated with the onset of MW and its unfolding over time. Moreover, by computing the latency between the trigger presentation and the task interruption (self-catch), we could also estimate the duration of MW episodes triggered by verbal cues. However, a high variability was found, implying very large inter-event variability, which could not be explained by any of the MW properties we acquired (including: temporal focus, specificity, emotional valence). Our behavioural and pupillometry findings stress the need for objective measures about the temporal unfolding of MW (while most studies focus on arbitrary time-window preceding self-reports of MW).