Visual perceptual learning modulates microsaccade rate and directionality.

Microsaccades, incessant "fixational eye movements" (< 1°), are an important window into cognitive functions. Yet, its role in visual perceptual learning (VPL)-improvements in visual discrimination due to practice-remains practically unexplored. Here we investigated whether and how microsaccades change in VPL. Human observers performed a Landolt acuity task for 5 consecutive days and were assigned to the Neutral or Attention group. On each trial, two peripheral Landolt squares were presented briefly along a diagonal. Observers reported the gap side of the target stimulus. Training improved acuity and modified the microsaccade rate; with training, the rate decreased during the fixation period but increased during the response cue. Furthermore, microsaccade direction during the response cue was biased toward the target location, and training enhanced and sped up this bias. Finally, the microsaccade rate during a task-free fixation period correlated with observers' initial acuity threshold, indicating that the fewer the microsaccades during fixation the better the individual visual acuity. All these results, which were similar for both the Neutral and Attention groups and at both trained and untrained locations, suggest that microsaccades could serve as a physiological marker reflecting functional dynamics in human perceptual learning.

Microsaccades as a long-term oculomotor correlate in visual perceptual learning.

Human perceptual learning, experience-induced gains in sensory discrimination, typically yields long-term performance improvements. Recent research revealed long-lasting transfer at the untrained location enabled by feature-based attention (FBA), reminiscent of its global effect (Hung & Carrasco, Scientific Reports, 11(1), 13914, (2021)). Visual Perceptual Learning (VPL) is typically studied while observers maintain fixation, but the role of fixational eye movements is unknown. Microsaccades - the largest of fixational eye movements - provide a continuous, online, physiological measure from the oculomotor system that reveals dynamic processing, which is unavailable from behavioral measures alone. We investigated whether and how microsaccades change after training in an orientation discrimination task. For human observers trained with or without FBA, microsaccade rates were significantly reduced during the response window in both trained and untrained locations and orientations. Critically, consistent with long-term training benefits, this microsaccade-rate reduction persisted over a year. Furthermore, microsaccades were biased toward the target location prior to stimulus onset and were more suppressed for incorrect than correct trials after observers' responses. These findings reveal that fixational eye movements and VPL are tightly coupled and that learning-induced microsaccade changes are long lasting. Thus, microsaccades reflect functional dynamics of the oculomotor system during information encoding, maintenance and readout, and may serve as a reliable long-term physiological correlate in VPL.

Feature-based attention enables robust, long-lasting location transfer in human perceptual learning.

Visual perceptual learning (VPL) is typically specific to the trained location and feature. However, the degree of specificity depends upon particular training protocols. Manipulating covert spatial attention during training facilitates learning transfer to other locations. Here we investigated whether feature-based attention (FBA), which enhances the representation of particular features throughout the visual field, facilitates VPL transfer, and how long such an effect would last. To do so, we implemented a novel task in which observers discriminated a stimulus orientation relative to two reference angles presented simultaneously before each block. We found that training with FBA enabled remarkable location transfer, reminiscent of its global effect across the visual field, but preserved orientation specificity in VPL. Critically, both the perceptual improvement and location transfer persisted after 1 year. Our results reveal robust, long-lasting benefits induced by FBA in VPL, and have translational implications for improving generalization of training protocols in visual rehabilitation.

Roles of Category, Shape, and Spatial Frequency in Shaping Animal and Tool Selectivity in the Occipitotemporal Cortex.

Does the nature of representation in the category-selective regions in the occipitotemporal cortex reflect visual or conceptual properties? Previous research showed that natural variability in visual features across categories, quantified by image gist statistics, is highly correlated with the different neural responses observed in the occipitotemporal cortex. Using fMRI, we examined whether category selectivity for animals and tools would remain, when image gist statistics were comparable across categories. Critically, we investigated how category, shape, and spatial frequency may contribute to the category selectivity in the animal- and tool-selective regions. Female and male human observers viewed low- or high-passed images of round or elongated animals and tools that shared comparable gist statistics in the main experiment, and animal and tool images of naturally varied gist statistics in a separate localizer. Univariate analysis revealed robust category-selective responses for images with comparable gist statistics across categories. Successful classification for category (animals/tools), shape (round/elongated), and spatial frequency (low/high) was also observed, with highest classification accuracy for category. Representational similarity analyses further revealed that the activation patterns in the animal-selective regions were most correlated with a model that represents only animal information, whereas the activation patterns in the tool-selective regions were most correlated with a model that represents only tool information, suggesting that these regions selectively represent information of only animals or tools. Together, in addition to visual features, the distinction between animal and tool representations in the occipitotemporal cortex is likely shaped by higher-level conceptual influences such as categorization or interpretation of visual inputs.SIGNIFICANCE STATEMENT Since different categories often vary systematically in both visual and conceptual features, it remains unclear what kinds of information determine category-selective responses in the occipitotemporal cortex. To minimize the influences of low- and mid-level visual features, here we used a diverse image set of animals and tools that shared comparable gist statistics. We manipulated category (animals/tools), shape (round/elongated), and spatial frequency (low/high), and found that the representational content of the animal- and tool-selective regions is primarily determined by their preferred categories only, regardless of shape or spatial frequency. Our results show that category-selective responses in the occipitotemporal cortex are influenced by higher-level processing such as categorization or interpretation of visual inputs, and highlight the specificity in these category-selective regions.

Influences of High-Level Features, Gaze, and Scene Transitions on the Reliability of BOLD Responses to Natural Movie Stimuli.

Complex, sustained, dynamic, and naturalistic visual stimulation can evoke distributed brain activities that are highly reproducible within and across individuals. However, the precise origins of such reproducible responses remain incompletely understood. Here, we employed concurrent functional magnetic resonance imaging (fMRI) and eye tracking to investigate the experimental and behavioral factors that influence fMRI activity and its intra- and inter-subject reproducibility during repeated movie stimuli. We found that widely distributed and highly reproducible fMRI responses were attributed primarily to the high-level natural content in the movie. In the absence of such natural content, low-level visual features alone in a spatiotemporally scrambled control stimulus evoked significantly reduced degree and extent of reproducible responses, which were mostly confined to the primary visual cortex (V1). We also found that the varying gaze behavior affected the cortical response at the peripheral part of V1 and in the oculomotor network, with minor effects on the response reproducibility over the extrastriate visual areas. Lastly, scene transitions in the movie stimulus due to film editing partly caused the reproducible fMRI responses at widespread cortical areas, especially along the ventral visual pathway. Therefore, the naturalistic nature of a movie stimulus is necessary for driving highly reliable visual activations. In a movie-stimulation paradigm, scene transitions and individuals' gaze behavior should be taken as potential confounding factors in order to properly interpret cortical activity that supports natural vision.

Confidence-based integrated reweighting model of task-difficulty explains location-based specificity in perceptual learning.

Perceptual learning is classically thought to be highly specific to the trained stimuli's retinal locations. However, recent research using a novel double-training paradigm has found dramatic transfer of perceptual learning to untrained locations. These results challenged existing models of perceptual learning and provoked intense debate in the field. Recently, Hung and Seitz (2014) showed that previously reported results could be reconciled by considering the details of the training procedure, in particular, whether it involves prolonged training at threshold using a single staircase procedure or multiple staircases. Here, we examine a hierarchical neural network model of the visual pathway, built upon previously proposed integrated reweighting models of perceptual learning, to understand how retinotopic transfer depends on the training procedure adopted. We propose that the transfer and specificity of learning between retinal locations can be explained by considering the task-difficulty and confidence during training. In our model, difficult tasks lead to higher learning of weights from early visual cortex to the decision unit, and thus to specificity, while easy tasks lead to higher learning of weights from later stages of the visual hierarchy and thus to more transfer. To model interindividual difference in task-difficulty, we relate task-difficulty to the confidence of subjects. We show that our confidence-based reweighting model can account for the results of Hung and Seitz (2014) and makes testable predictions.

Prolonged training at threshold promotes robust retinotopic specificity in perceptual learning.

Human perceptual learning is classically thought to be highly specific to trained stimuli's retinal location. Together with evidence that specific learning effects can result in corresponding changes in early visual cortex, researchers have theorized that specificity implies regionalization of learning in the brain. However, other research suggests that specificity can arise from learning readout in decision areas or through top-down processes. Notably, recent research using a novel double-training paradigm reveals dramatic generalization of perceptual learning to untrained locations when multiple stimuli are trained. These data provoked significant controversy in the field and challenged extant models of perceptual learning. To resolve this controversy, we investigated mechanisms that account for retinotopic specificity in perceptual learning. We replicated findings of transfer after double training; however, we show that prolonged training at threshold, which leads to a greater number of difficult trials during training, preserves location specificity when double training occurred at the same location or sequentially at different locations. Likewise, we find that prolonged training at threshold determines the degree of transfer in single training of a peripheral orientation discrimination task. Together, these data show that retinotopic specificity depends highly upon particularities of the training procedure. We suggest that perceptual learning can arise from decision rules, attention learning, or representational changes, and small differences in the training approach can emphasize some of these over the others.

Retrograde interference in perceptual learning of a peripheral hyperacuity task.

Consolidation, a process that stabilizes memory trace after initial acquisition, has been studied for over a century. A number of studies have shown that a skill or memory must be consolidated after acquisition so that it becomes resistant to interference from new information. Previous research found that training on a peripheral 3-dot hyperacuity task could retrogradely interfere with earlier training on the same task but with a mirrored stimulus configuration. However, a recent study failed to replicate this finding. Here we address the controversy by replicating both patterns of results, however, under different experimental settings. We find that retrograde interference occurs when eye-movements are tightly controlled, using a gaze-contingent display, where the peripheral stimuli were only presented when subjects maintained fixation. On the other hand, no retrograde interference was found in a group of subjects who performed the task without this fixation control. Our results provide a plausible explanation of why divergent results were found for retrograde interference in perceptual learning on the 3-dot hyperacuity task and confirm that retrograde interference can occur in this type of low-level perceptual learning. Furthermore, our results demonstrate the importance of eye-movement controls in studies of perceptual learning in the peripheral visual field.

Developmental gene regulatory networks in the zebrafish embryo.

The genomic developmental program operates mainly through the regulated expression of genes encoding transcription factors and signaling pathways. Complex networks of regulatory genetic interactions control developmental cell specification and fates. Development in the zebrafish, Danio rerio, has been studied extensively and large amounts of experimental data, including information on spatial and temporal gene expression patterns, are available. A wide variety of maternal and zygotic regulatory factors and signaling pathways have been discovered in zebrafish, and these provide a useful starting point for reconstructing the gene regulatory networks (GRNs) underlying development. In this review, we describe in detail the genetic regulatory subcircuits responsible for dorsoanterior-ventroposterior patterning and endoderm formation. We describe a number of regulatory motifs, which appear to act as the functional building blocks of the GRNs. Different positive feedback loops drive the ventral and dorsal specification processes. Mutual exclusivity in dorsal-ventral polarity in zebrafish is governed by intra-cellular cross-inhibiting GRN motifs, including vent/dharma and tll1/chordin. The dorsal-ventral axis seems to be determined by competition between two maternally driven positive-feedback loops (one operating on Dharma, the other on Bmp). This is the first systematic approach aimed at developing an integrated model of the GRNs underlying zebrafish development. Comparison of GRNs' organizational motifs between different species will provide insights into developmental specification and its evolution. The online version of the zebrafish GRNs can be found at http://www.zebrafishGRNs.org.