Development of Higher-Level Vision: A Network Perspective.

Most studies on the development of the visual system have focused on the mechanisms shaping early visual stages up to the level of primary visual cortex (V1). Much less is known about the development of the stages after V1 that handle the higher visual functions fundamental to everyday life. The standard model for the maturation of these areas is that it occurs sequentially, according to the positions of areas in the adult hierarchy. Yet, the existing literature reviewed here paints a different picture, one in which the adult configuration emerges through a sequence of unique network configurations that are not mere partial versions of the adult hierarchy. In addition to studying higher visual development per se to fill major gaps in knowledge, it will be crucial to adopt a network-level perspective in future investigations to unravel normal developmental mechanisms, identify vulnerabilities to developmental disorders, and eventually devise treatments for these disorders.

Impairment in understanding grasping movements in egocentric and allocentric perspectives in children with cerebral palsy due to periventricular leukomalacia.

Recognizing and understanding the actions of others through motion information are vital functions for social adaptation. Conditions like neurological disorders and motor impairments can impact sensitivity to biological motion, highlighting the intricate relationship between perceiving and executing movements. Our study centred on assessing the ability of children, encompassing both those with typical development and those diagnosed with cerebral palsy due to periventricular leukomalacia (PVL), to discriminate between depicted grasping of a small cylinder and a large cube. This discrimination task involved observing a point-light animation depicting an actor grasping the object, presented from either an allocentric perspective (observing others) or an egocentric viewpoint (observing oneself). Notably, children with PVL exhibited a pronounced and specific impairment in this task, irrespective of the viewpoint, as evidenced by thresholds increasing by nearly a factor of two. When comparing this impairment to difficulties in form or motion perception, we identified a robust correlation between egocentric biological motion and form sensitivity. However, there was no similar correlation between motion and biological motion sensitivity, suggesting a deficit in the visual system rather than the visuo-motor control system. These findings contribute to our understanding of the intricate interplay between motor and visual processing in individuals with congenital brain lesions, shedding light on the significant involvement of the visual system in cases of PVL.

Investigating cross-orientation inhibition with continuous tracking.

We investigated cross-orientation inhibition with the recently developed continuous tracking technique. We designed an experiment where participants tracked the horizontal motion of a narrow vertical grating. The target was superimposed on one of three different backgrounds, in separate sessions: a uniform gray background or a sinusoidal grating oriented either parallel or orthogonal to the target. Both mask and target where phase reversed. We cross-correlated target and mouse movements and compared the peaks and lags of response with the different masks. Our results are in agreement with previous findings on cross-orientation inhibition: The orthogonal mask had a weak effect on the peaks and lags of correlation as a function of target contrast, consistently with a divisive effect of the mask, while the parallel mask acted subtractively on the response. Interestingly, lags of correlation decreased approximately linearly with contrast, with decrements of the order of 100 ms, even at 10 times the detection threshold, confirming that it is possible to investigate behavioral differences above threshold using the continuous tracking paradigm.

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.

The role of neural oscillations in visuo-motor communication at the time of saccades.

Saccadic eye-movements are fundamental for active vision, allowing observers to purposefully scan the environment with the high-resolution fovea. In this brief perspective we outline a series of experiments from our laboratories investigating the role of eye-movements and their consequences to active perception. We show that saccades lead to suppression of visual sensitivity at saccadic onset, and that this suppression is accompanied by endogenous neural oscillations in the delta range. Similar oscillations are initiated by purposeful hand movements, which lead to measurable changes in responsivity in area V1, and in the connectivity with motor area M1. Saccades also lead to clear distortions in apparent position, but only for verbal reports, not when participants respond with rapid pointing, consistent with the action of two separate visual systems in neurotypical adults. At the time of saccades, serial dependence, the positive influence on perception of previous stimulus attributes (such as orientation) is particularly strong. Again, these processes are accompanied by neural oscillations, in the alpha and low beta range. In general, oscillations seem to be tightly linked to serial dependence in perception, both in auditory judgments (around 10 Hz), and for visual judgements of face gender (14 Hz for female, 17 Hz for male). Taken together, the studies show that neural oscillations play a fundamental role in dynamic, active vision.

Serial dependence in orientation judgments at the time of saccades.

We actively seek information from the environment through saccadic eye movements, necessitating continual integration of presaccadic and postsaccadic signals, which are displaced on the retina by each saccade. We tested whether trans-saccadic integration may be related to serial dependence (a measure of how perceptual history influences current perception) by measuring how viewing a presaccadic stimulus affects the perceived orientation of a subsequent test stimulus presented around the time of a saccade. Participants reproduced the position, and orientation of a test stimulus presented around a 16° saccade. The reproduced position was mislocalized toward the saccadic target, agreeing with previous work. The reproduced orientation was attracted toward the prior stimulus and regressed to the mean orientation. These results suggest that both short- and long-term past information affects trans-saccadic perception, most strongly when the test stimulus is presented perisaccadically. This study unites the fields of serial dependence and trans-saccadic perception, leading to potential new insights of how information is transferred and accumulated across saccades.

The duration effect of short-term monocular deprivation measured by binocular rivalry and binocular combination.

The ocular dominance shift observed after short-term monocular deprivation is a widely used measure of visual homeostatic plasticity in adult humans. Binocular rivalry and binocular combination techniques are used interchangeably to characterize homeostatic plasticity, sometimes leading to contradictory results. Here we directly compare the effect of short-term monocular deprivation on ocular dominance measured by either binocular rivalry or binocular combination and its dependence on the duration of deprivation (15 or 120 min) in the same group of participants. Our results show that both binocular rivalry and binocular combination provide reliable estimates of ocular dominance, which are strongly correlated across techniques both before and after deprivation. Moreover, while 15 min of monocular deprivation induce a larger shift of ocular dominance when measured using binocular combination compared to binocular rivalry, for both techniques, the shift in ocular dominance exhibits a strong dependence on the duration of monocular deprivation, with longer deprivation inducing a larger and longer-lasting shift in ocular dominance. Taken together, our results indicate that both binocular rivalry and binocular combination offer very consistent and reliable measurements of both ocular dominance and the effect short-term monocular deprivation.

Quantum spin models for numerosity perception.

Humans share with animals, both vertebrates and invertebrates, the capacity to sense the number of items in their environment already at birth. The pervasiveness of this skill across the animal kingdom suggests that it should emerge in very simple populations of neurons. Current modelling literature, however, has struggled to provide a simple architecture carrying out this task, with most proposals suggesting the emergence of number sense in multi-layered complex neural networks, and typically requiring supervised learning; while simple accumulator models fail to predict Weber's Law, a common trait of human and animal numerosity processing. We present a simple quantum spin model with all-to-all connectivity, where numerosity is encoded in the spectrum after stimulation with a number of transient signals occurring in a random or orderly temporal sequence. We use a paradigmatic simulational approach borrowed from the theory and methods of open quantum systems out of equilibrium, as a possible way to describe information processing in neural systems. Our method is able to capture many of the perceptual characteristics of numerosity in such systems. The frequency components of the magnetization spectra at harmonics of the system's tunneling frequency increase with the number of stimuli presented. The amplitude decoding of each spectrum, performed with an ideal-observer model, reveals that the system follows Weber's law. This contrasts with the well-known failure to reproduce Weber's law with linear system or accumulators models.

Development of BOLD Response to Motion in Human Infants.

Behavioral studies suggest that motion perception is rudimentary at birth and matures steadily over the first few years. We demonstrated previously that the major cortical associative areas serving motion processing, like middle temporal complex (MT+), visual cortex area 6 (V6), and PIVC in adults, show selective responses to coherent flow in 8-week-old infants. Here, we study the BOLD response to the same motion stimuli in 5-week-old infants (four females and four males) and compare the maturation between these two ages. The results show that MT+ and PIVC areas show a similar motion response at 5 and 8 weeks, whereas response in the V6 shows a reduced BOLD response to motion at 5 weeks, and cuneus associative areas are not identifiable at this young age. In infants and in adults, primary visual cortex (V1) does not show a selectivity for coherent motion but shows very fast development between 5 and 8 weeks of age in response to the appearance of motion stimuli. Resting-state correlations demonstrate adult-like functional connectivity between the motion-selective associative areas but not between primary cortex and temporo-occipital and posterior-insular cortices. The results are consistent with a differential developmental trajectory of motion area respect to other occipital regions, probably reflecting also a different development trajectory of the central and peripheral visual field.SIGNIFICANCE STATEMENT How the cortical visual areas attain the specialization that we observed in human adults in the first few months of life is unknown. However, this knowledge is crucial to understanding the consequence of perinatal brain damage and its outcome. Here, we show that motion selective areas are already functioning well in 5-week-old infants with greater responses for detecting coherent motion over random motion, suggesting that very little experience is needed to attain motion selectivity.

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.

Vision: Neuronal mechanisms enabling stable perception.

Eye movements cause rapid motion of the retinal image, potentially confusable with external motion. A recent study shows that neurons in mouse primary visual cortex distinguish self-generated from external motion by combining sensory input with saccade-related signals from the thalamic pulvinar nucleus.

The Readiness Potential Correlates with Action-Linked Modulation of Visual Accuracy.

Visual accuracy is consistently shown to be modulated around the time of the action execution. The neural underpinning of this motor-induced modulation of visual perception is still unclear. Here, we investigate with EEG whether it is related to the readiness potential, an event-related potential (ERP) linked to motor preparation. Across 18 human participants, the magnitude of visual modulation following a voluntary button press was found to correlate with the readiness potential amplitude measured during visual discrimination. Participants' amplitude of the readiness potential in a purely motor-task was also found to correlate with the extent of the motor-induced modulation of visual perception in the visuomotor task. These results provide strong evidence that perceptual changes close to action execution are associated with motor preparation processes and that this mechanism is independent of task contingencies. Further, our findings suggest that the readiness potential provides a fingerprint of individual visuomotor interaction.

Evidence of Serial Dependence from Decoding of Visual Evoked Potentials.

It is well known that recent sensory experience influences perception, recently demonstrated by a phenomenon termed "serial dependence." However, its underlying neural mechanisms are poorly understood. We measured ERP responses to pairs of stimuli presented randomly to the left or right hemifield. Seventeen male and female adults judged whether the upper or lower half of the grating had higher spatial frequency, independent of the horizontal position of the grating. This design allowed us to trace the memory signal modulating task performance and also the implicit memory signal associated with hemispheric position. Using classification techniques, we decoded the position of the current and previous stimuli and the response from voltage scalp distributions of the current trial. Classification of previous responses reached full significance only 700 ms after presentation of the current stimulus, consistent with retrieval of an activity-silent memory trace. Cross-condition classification accuracy of past responses (trained on current responses) correlated with the strength of serial dependence effects of individual participants. Overall, our data provide evidence for a silent memory signal that can be decoded from the EEG potential, which interacts with the neural processing of the current stimulus. This silent memory signal could be the physiological substrate subserving at least one type of serial dependence.SIGNIFICANCE STATEMENT The neurophysiological underpinnings of how past perceptual experience affects current perception are poorly understood. Here, we show that recent experience is reactivated when a new stimulus is presented and that the strength of this reactivation correlates with serial biases in individual participants, suggesting that serial dependence is established on the basis of a silent memory signal.

Long Covid: where we stand and challenges ahead.

Post-acute sequelae of SARS-CoV-2 (PASC), also known as Post-Covid Syndrome, and colloquially as Long Covid, has been defined as a constellation of signs and symptoms which persist for weeks or months after the initial SARS-CoV-2 infection. PASC affects a wide range of diverse organs and systems, with manifestations involving lungs, brain, the cardiovascular system and other organs such as kidney and the neuromuscular system. The pathogenesis of PASC is complex and multifactorial. Evidence suggests that seeding and persistence of SARS-CoV-2 in different organs, reactivation, and response to unrelated viruses such as EBV, autoimmunity, and uncontrolled inflammation are major drivers of PASC. The relative importance of pathogenetic pathways may differ in different tissue and organ contexts. Evidence suggests that vaccination, in addition to protecting against disease, reduces PASC after breakthrough infection although its actual impact remains to be defined. PASC represents a formidable challenge for health care systems and dissecting pathogenetic mechanisms may pave the way to targeted preventive and therapeutic approaches.

Mutual interaction between visual homeostatic plasticity and sleep in adult humans.

Sleep and plasticity are highly interrelated, as sleep slow oscillations and sleep spindles are associated with consolidation of Hebbian-based processes. However, in adult humans, visual cortical plasticity is mainly sustained by homeostatic mechanisms, for which the role of sleep is still largely unknown. Here, we demonstrate that non-REM sleep stabilizes homeostatic plasticity of ocular dominance induced in adult humans by short-term monocular deprivation: the counterintuitive and otherwise transient boost of the deprived eye was preserved at the morning awakening (>6 hr after deprivation). Subjects exhibiting a stronger boost of the deprived eye after sleep had increased sleep spindle density in frontopolar electrodes, suggesting the involvement of distributed processes. Crucially, the individual susceptibility to visual homeostatic plasticity soon after deprivation correlated with the changes in sleep slow oscillations and spindle power in occipital sites, consistent with a modulation in early occipital visual cortex.

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.

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.

Normal Retinotopy in Primary Visual Cortex in a Congenital Complete Unilateral Lesion of Lateral Geniculate Nucleus in Human: A Case Study.

Impairment of the geniculostriate pathway results in scotomas in the corresponding part of the visual field. Here, we present a case of patient IB with left eye microphthalmia and with lesions in most of the left geniculostriate pathway, including the Lateral Geniculate Nucleus (LGN). Despite the severe lesions, the patient has a very narrow scotoma in the peripheral part of the lower-right-hemifield only (beyond 15° of eccentricity) and complete visual field representation in the primary visual cortex. Population receptive field mapping (pRF) of the patient's visual field reveals orderly eccentricity maps together with contralateral activation in both hemispheres. With diffusion tractography, we revealed connections between superior colliculus (SC) and cortical structures in the hemisphere affected by the lesions, which could mediate the retinotopic reorganization at the cortical level. Our results indicate an astonishing case for the flexibility of the developing retinotopic maps where the contralateral thalamus receives fibers from both the nasal and temporal retinae.

Propagation and update of auditory perceptual priors through alpha and theta rhythms.

To maintain a continuous and coherent percept over time, the brain makes use of past sensory information to anticipate forthcoming stimuli. We recently showed that auditory experience of the immediate past is propagated through ear-specific reverberations, manifested as rhythmic fluctuations of decision bias at alpha frequencies. Here, we apply the same time-resolved behavioural method to investigate how perceptual performance changes over time under conditions of stimulus expectation and to examine the effect of unexpected events on behaviour. As in our previous study, participants were required to discriminate the ear-of-origin of a brief monaural pure tone embedded in uncorrelated dichotic white noise. We manipulated stimulus expectation by increasing the target probability in one ear to 80%. Consistent with our earlier findings, performance did not remain constant across trials, but varied rhythmically with delay from noise onset. Specifically, decision bias showed a similar oscillation at ~9 Hz, which depended on ear congruency between successive targets. This suggests rhythmic communication of auditory perceptual history occurs early and is not readily influenced by top-down expectations. In addition, we report a novel observation specific to infrequent, unexpected stimuli that gave rise to oscillations in accuracy at ~7.6 Hz one trial after the target occurred in the non-anticipated ear. This new behavioural oscillation may reflect a mechanism for updating the sensory representation once a prediction error has been detected.