a-gaze-contingent-display-framework-for-perceptual-learning-research

A Gaze-Contingent Display Framework for Perceptual Learning Research with Simulated Central Vision Loss

Macular degeneration (MD) is one of the leading causes of vision impairment in the Western world. Patients with MD tend to develop spontaneous eye ...

University of California, Riverside

A hallmark of modern Perceptual Learning (PL) is the extent to which learning is specific to the trained stimuli. Such specificity to orientation, spatial location and even eye of training has been used as psychophysical evidence of the neural basis of learning. This argument that specificity of PL implies regionalization of brain plasticity implicitly assumes that examination of a singular locus of PL is an appropriate approach to understand learning. However, recent research shows that learning effects once thought to be specific depend on subtleties of the training paradigm and that within even a simple training procedure there are multiple aspects of the task and stimuli that are learned simultaneously. Here, we suggest that learning on any task involves a broad network of brain regions undergoing changes in representations, read-out weights, decision rules, attention and feedback processes as well as oculomotor changes. However, importantly, the distribution of learning across the neural system depends upon the details of the training procedure and the characterstics of the individual being trained. We propose that to advance our understanding of PL, the field must move towards understanding how distributed brain processes jointly contribute to behavioral learning effects.

Towards a whole brain model of Perceptual Learning.

Visual crowding, the difficulty of recognizing elements when surrounded by similar items, is a widely studied perceptual phenomenon and a trademark characteristic of peripheral vision. Perceptual Learning (PL) has been shown to reduce crowding, although a large number of sessions is required to observe significant improvements. Recently, transcranial random noise stimulation (tRNS) has been successfully used to boost PL in low-level foveal tasks (e.g., contrast detection, orientation) in both healthy and clinical populations. However, no studies so far combined tRNS with PL in peripheral vision during higher-level tasks. Thus, we investigated the effect of tRNS on PL and transfer in peripheral high-level visual tasks. We trained two groups (tRNS and sham) of normal-sighted participants in a peripheral (8° of eccentricity) crowding task over a short number of sessions (4). We tested both learning and transfer to untrained spatial locations, orientations, and tasks (visual acuity). After training, the tRNS group showed greater learning rate with respect to the sham group. For both groups, learning generalized to the same extent to the untrained retinal location and task. Overall, this paradigm has potential applications for patients suffering from central vision loss but further research is needed to elucidate its effect (i.e., increasing transfer and learning retention).

tRNS boosts perceptual learning in peripheral vision.

The interaction between the primary visual cortex (V1) and extrastriate visual areas provides the first building blocks in our perception of the world. V2, in particular, seems to play a crucial role in shaping contextual modulation information through feedback projections to V1. However, whether this feedback is inhibitory or excitatory is still unclear. In order to test the nature of V2 feedback to V1, we used neuronavigation-guided offline inhibitory transcranial magnetic stimulation (TMS) on V2 before testing participants on collinear facilitation, a contrast detection task with lateral masking. This contextual modulation task is thought to rely on horizontal connections in V1 and possibly extrastriate feedback. Results showed that when inhibitory TMS was delivered over V2, contrast thresholds decreased for targets presented in the contralateral hemifield, consistent with the retinotopic mapping of this area, while having no effect for targets presented in the ipsilateral hemifield or after control (CZ) stimulation. These results suggest that feedback from V2 to V1 during contextual modulation is mostly inhibitory, corroborating recent observations in monkey electrophysiology and extending this mechanism to human visual system. Moreover, we provide for the first time direct evidence of the involvement of extrastriate visual areas in collinear facilitation.

TMS reveals inhibitory extrastriate cortico-cortical feedback modulation of V1 activity in humans.

Loss of central vision can be compensated for in part by increased use of peripheral vision. For example, patients with macular degeneration or those experiencing simulated central vision loss tend to develop eccentric viewing strategies for reading or other visual tasks. The factors driving this learning are still unclear and likely involve complex changes in oculomotor strategies that may differ among people and tasks. Although to date a number of studies have examined reliance on peripheral vision after simulated central vision loss, individual differences in developing peripheral viewing strategies and the extent to which they transfer to untrained tasks have received little attention. Here, we apply a recently published method of characterizing oculomotor strategies after central vision loss to understand the time course of changes in oculomotor strategies through training in 19 healthy individuals with a gaze-contingent display obstructing the central 10° of the visual field. After 10 days of training, we found mean improvements in saccadic re-referencing (the percentage of trials in which the first saccade placed the target outside the scotoma), latency of target acquisition (time interval between target presentation and a saccade putting the target outside the scotoma), and fixation stability. These results are consistent with participants developing compensatory oculomotor strategies as a result of training. However, we also observed substantial individual differences in the formation of eye movement strategies and the extent to which they transferred to an untrained task, likely reflecting both variations in learning rates and patterns of learning. This more complete characterization of peripheral looking strategies and how they change with training may help us understand individual differences in rehabilitation after central vision loss.

We don't all look the same; detailed examination of peripheral looking strategies after simulated central vision loss.

Increase (facilitation) or decrease (inhibition) of contrast sensitivity for a Gabor patch presented between two collinear flankers is a well-studied contextual modulation phenomenon. It has been suggested that this effect has its neural bases in the primary visual cortex, specifically the horizontal connections between hypercolumns with similar orientation and spatial frequency selectivity. Another typical phenomenon dependent on early visual areas is contrast adaptation, in which the neural response to a contrast stimulus is decreased after exposure. Here, we investigated the effect of contrast adaptation of the flankers on the magnitude of collinear modulation by testing whether contrast adaptation reduced collinear facilitation and collinear inhibition. Results showed dissociation in the effect of collinear flanker adaptation, which increased contrast thresholds for the target in the facilitatory configuration and reduced them in the inhibitory configuration. Moreover, the effect was specific for the collinear configuration, since contrast adaptation of orthogonal flankers did not affect the contrast of the target, pointing towards the involvement of early visual units specific for orientation. Surprisingly, the same pattern of results was also confirmed when the inhibitory configuration was tested with low-contrast flankers, indicating that the effect of adaptation does not depend on a decrease in perceived contrast of the flankers. Taken together, these results suggest that contrast adaptation disrupts collinear modulation and that contrast thresholds can be affected by adapting portions of the visual field outside the receptive field of the units processing the contrast of the target (i.e., the flankers).

Contrast adaptation of flankers reduces collinear facilitation and inhibition.

After loss of central vision following retinal pathologies such as macular degeneration (MD), patients often adopt compensatory strategies including developing a "preferred retinal locus" (PRL) to replace the fovea in tasks involving fixation. A key question is whether patients develop multi-purpose PRLs or whether their oculomotor strategies adapt to the demands of the task. While most MD patients develop a PRL, clinical evidence suggests that patients may develop multiple PRLs and switch between them according to the task at hand. To understand this, we examined a model of central vision loss in normally seeing individuals and tested whether they used the same or different PRLs across tasks after training. Nineteen participants trained for 10 sessions on contrast detection while in conditions of gaze-contingent, simulated central vision loss. Before and after training, peripheral looking strategies were evaluated during tasks measuring visual acuity, reading abilities and visual search. To quantify strategies in these disparate, naturalistic tasks, we measured and compared the amount of task-relevant information at each of 8 equally spaced, peripheral locations, while participants performed the tasks. Results showed that some participants used consistent viewing strategies across tasks whereas other participants' strategies differed depending on task. This novel method allows quantification of peripheral vision use even in relatively ecological tasks. These results represent one of the first examinations of peripheral viewing strategies across tasks in simulated vision loss. Results suggest that individual differences in peripheral looking strategies following simulated central vision loss may model those developed in pathological vision loss.

Consistency of preferred retinal locus across tasks and participants trained with a simulated scotoma.

Collinear modulation represents a fundamental building block of our perceptual world, and its study has enhanced our understanding of contrast sensitivity, spatial integration, and neural plasticity in the visual system. In this phenomenon, the visibility of a target is influenced by collinear elements. Four key factors modulate this effect: the distance between target and flankers, the contrast of the flankers, retinal eccentricity, and spatial frequency. Each of these elements affects collinear modulation, increasing or reducing the target's visibility. Short target-to-flankers separations decrease contrast sensitivity, while larger separations increase it. However, this pattern holds for high contrast flankers, whereas low contrast flankers increase contrast sensitivity at short separations, while the effect is weaker or absent at large separations. Moreover, eccentricity appears to increase the spatial extent of inhibition. Across three experiments, we systematically varied these key factors. In Experiments 1 and 2, we manipulated spatial frequency, flankers' separation, and flankers' contrast in foveal vision. In Experiment 3, we varied flankers' separation and flankers' contrast in peripheral vision. The results reveal a complex pattern that may help reconcile previously conflicting findings in both healthy participants and clinical populations, offering an updated framework for the study of neural plasticity in the visual system.

Article	Year
Towards a whole brain model of Perceptual Learning. Current opinion in behavioral sciences\| PubMed ID: 29457054	2018
tRNS boosts perceptual learning in peripheral vision. Neuropsychologia\| PubMed ID: 30721741	2019
TMS reveals inhibitory extrastriate cortico-cortical feedback modulation of V1 activity in humans. Brain structure & function\| PubMed ID: 31624907	2019
We don't all look the same; detailed examination of peripheral looking strategies after simulated central vision loss. Journal of vision\| PubMed ID: 33284309	2020
Contrast adaptation of flankers reduces collinear facilitation and inhibition. Vision research\| PubMed ID: 34999351	2022
Consistency of preferred retinal locus across tasks and participants trained with a simulated scotoma. Vision research\| PubMed ID: 36527839	2023
Characterization of contrast-mediated collinear interactions in the human visual system. Scientific reports\| PubMed ID: 40195330	2025

Marcello Maniglia

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