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McGuire, J. T.

Publications and source records attributed to McGuire, J. T..

8 recordsLinked to original sources

Dynamic task-based reorganization of sensory-biased and supramodal working memory networks in the human cerebral cortex

Human working memory is supported by a broadly distributed set of brain networks. Content-specific networks communicate with a domain-general, supramodal network that is recruited regardless of the type of content. Here, we contrasted visual and auditory working memory tasks to examine interactions between the supramodal network and two content-specific networks. Functional connectivity among visual-biased, auditory-biased, and supramodal working memory networks was assayed by collecting task and resting-state fMRI data from 24 human participants (age 18-43; 11 men and 13 women). At rest, as found previously, the supramodal network exhibited stronger functional connectivity with the visual-biased network than with the auditory-biased network. This asymmetry raises questions about how networks communicate to support robust performance across modalities. However, during auditory task performance, dynamic changes increased auditory network connectivity with supramodal and visual-biased frontal regions, while decreasing connectivity from posterior visual areas to supramodal and frontal visual regions. In contrast, the visual task produced weak changes. Across individuals, auditory working memory precision correlated with the strength of auditory network connectivity changes, while no such brain-behavior link was observed for visual working memory. These results demonstrate an asymmetry in working memory network organization and reveal that dynamic reorganization accompanies performance of working memory tasks.

neuroscience↗

Altered perceptual integration and learning in autism revealed by games inspired by rodent operant tasks

Altered perception is a key feature of autism spectrum disorder (ASD), yet its precise nature and variability across individuals remain unclear. We developed an online video game, inspired by rodent operant tasks, to assess visual evidence integration. The game employs nonverbal, reward-based training and a pulsed stimulus design for precise control of sensory input, enabling detailed individual-level behavioral analysis. It was playable by typically developing adolescents and their autistic siblings, who spanned the spectrum, including those with profound autism. Game performance correlated with standard ASD survey scores, with ASD participants exhibiting slower learning and altered perceptual integration. Behavioral data were well fit by computational models in which perceptual and learning deficits in ASD arose from increased noise in higher- order visual processing. Our findings reveal that deficits in perceptual integration are widespread across ASD, correlate with symptom severity in social and adaptive domains, and may arise from instability of sensory representations.

neuroscience↗

Dynamic estimation of the attentional field from visual cortical activity

Navigating around the world, we must adaptively allocate attention to our surroundings based on anticipated future stimuli and events. This allocation of spatial attention boosts visuocortical representations at attended locations and locally enhances perception. Indeed, spatial attention has often been analogized to a "spotlight" shining on the item of relevance. Although the neural underpinnings of the locus of this attentional spotlight have been relatively well studied, less is known about the size of the spotlight: to what extent can the attentional field be broadened and narrowed in accordance with behavioral demands? In this study, we developed a paradigm for dynamically estimating the locus and spread of covert spatial attention, inferred from visuocortical activity using fMRI in humans. We measured BOLD activity in response to an annulus while participants (4 female, 4 male) used covert visual attention to determine whether more numbers or letters were present in a cued region of the annulus. Importantly, the width of the cued area was systematically varied, calling for different sizes of the attentional spotlight. The deployment of attention was associated with an increase in BOLD activity in corresponding retinotopic regions of visual areas V1--V3. By modeling the visuocortical attentional modulation, we could reliably recover the cued location, as well as a broadening of the attentional modulation with wider attentional cues. This modeling approach offers a useful window into the dynamics of attention and spatial uncertainty. Significance StatementThis study explores whether spatial attention can dynamically adapt by shifting and broadening the attentional field. While previous research has focused on the modulation of neural responses at attended locations, less is known about how the size of the attentional field is represented within visual cortex. Using fMRI, we developed a novel paradigm to estimate the spatial tuning of the attentional field and demonstrate that we were able to recover both the location as well as the width of the attentional field. Our findings offer new insights into the neural mechanisms underlying the deployment of spatial attention, contributing to a deeper understanding of how spatial attention supports visual perception.

neuroscience↗

Lesions to different regions of frontal cortex have dissociable effects on voluntary persistence

Deciding how long to keep waiting for uncertain future rewards is a complex problem. Previous research has shown that choosing to stop waiting results from an evaluative process that weighs the subjective value of the awaited reward against the opportunity cost of waiting. In functional neuroimaging data, activity in ventromedial prefrontal cortex (vmPFC) tracks the dynamics of this evaluation, while activation in the dorsomedial prefrontal cortex (dmPFC) and anterior insula (AI) ramps up before a decision to quit is made. Here, we provide causal evidence of the necessity of these brain regions for successful performance in a willingness-to-wait task. 28 participants with frontal lobe lesions were tested on their ability to adaptively calibrate how long they waited for monetary rewards. We grouped the participants based on the location of their lesions, which were primarily in ventromedial, dorsomedial, or lateral parts of their prefrontal cortex (vmPFC, dmPFC, and lPFC, respectively), or in the anterior insula. We compared the performance of each subset of lesion participants to behavior in a control group without lesions (n=18). Finally, we fit a newly developed computational model to the data to glean a more mechanistic understanding of how lesions affect the cognitive processes underlying choice. We found that participants with lesions to the vmPFC waited less overall, while participants with lesions to the dmPFC and anterior insula were specifically impaired at calibrating their level of persistence to the environment. These behavioral effects were accounted for by systematic differences in parameter estimates from a computational model of task performance: while the vmPFC group showed reduced initial willingness to wait, lesions to the dmPFC/anterior insula were associated with slower learning from negative feedback. These findings corroborate the notion that failures of persistence can be driven by sophisticated cost-benefit analyses rather than lapses in self-control. They also support the functional specialization of different parts of the prefrontal cortex in service of voluntary persistence.

neuroscience↗

Assessing evidence accumulation and rule learning in humans with an online game

Evidence accumulation, how the brain integrates sensory information over time, is an essential component of perception and decision making. In humans, evidence accumulation is commonly modeled as a diffusion process in which noise accumulates linearly with the incoming evidence. However, recent studies in rodents have shown that during perceptual decision making, noise scales non-linearly with the strength of accumulated evidence. The question of whether nonlinear noise scaling also holds for humans has been clouded by differences in the methodologies typically used to collect and analyze human and rodent data. For example, whereas humans are typically given explicit instructions in these tasks, rodents are trained using feedback. Therefore, to evaluate how perceptual noise scales with accumulated evidence, we developed an online evidence accumulation game and nonverbal training pipeline for humans inspired by pulse-based evidence accumulation tasks for rodents. Using this game, we collected and analyzed behavioral data from hundreds of participants trained either with an explicit description of the relevant decision rule or merely with experiential feedback. Across all participants, performance was well described by an accumulation process, in which stimuli were integrated equally across time. Participants trained using feedback alone learned the game rules rapidly and used similar strategies to those who received explicit instructions. Decisions in both groups were influenced in similar ways by biases and perceptual noise, suggesting that explicit instructions did not reduce bias or noise in pulse-based accumulation tasks. Finally, by leveraging data across all participants, we show that perceptual noise during evidence accumulation was best described by a non-linear model of noise scaling, consistent with previous animal studies, but inconsistent with diffusion models widely used in human studies. These results challenge the conventional description of humans accumulation process and suggest that online games inspired by evidence accumulation tasks provide a valuable large-scale behavioral assessment platform to examine perceptual decision making and learning in humans. In addition, the feedback-based training pipeline developed for this game may be useful for evaluating perceptual decision making in human populations with difficulty following verbal instructions. HighlightsO_LIDevelopment and validation of an online video game to measure perceptual decision making. C_LIO_LIHumans trained using a feedback-based pipeline exhibit similar strategies and performance compared with those receiving instructions. C_LIO_LIPerceptual noise increases superlinearly with sensory evidence. C_LI

animal behavior and cognition↗

Functional brain network reconfiguration during learning in a dynamic environment

When learning about dynamic and uncertain environments, people should update their beliefs most strongly when new evidence is most informative, such as when the environment undergoes a surprising change or existing beliefs are highly uncertain. Here we show that modulations of surprise and uncertainty are encoded in a particular, temporally dynamic pattern of whole-brain functional connectivity, and this encoding is enhanced in individuals that adapt their learning dynamics more appropriately in response to these factors. The key feature of this whole-brain pattern of functional connectivity is stronger connectivity, or functional integration, between the fronto-parietal and other functional systems. Our results provide new insights regarding the association between dynamic adjustments in learning and dynamic, large-scale changes in functional connectivity across the brain.

neuroscience↗

Individual heterogeneity in the functional network topography of medial prefrontal cortex

Regions of human medial prefrontal cortex (mPFC) and posterior cingulate cortex (PCC) are part of the default network (DN), and additionally are implicated in diverse cognitive functions ranging from autobiographical memory to subjective valuation. Our ability to interpret the apparent co-localization of task-related effects with DN-regions is constrained by a limited understanding of the individual-level heterogeneity in mPFC/PCC functional organization. Here we used cortical surface-based meta-analysis to identify a parcel in human PCC that was more strongly associated with the DN than with valuation effects. We then used resting-state fMRI data and a data-driven network analysis algorithm, spectral partitioning, to partition mPFC and PCC into \"DN\" and \"non-DN\" subdivisions in individual participants (n = 100 from the Human Connectome Project). The spectral partitioning algorithm identified individual-level cortical subdivisions that varied markedly across individuals, especially in mPFC, and were reliable across test/retest datasets. Our results point toward new strategies for assessing whether distinct cognitive functions engage common or distinct mPFC subregions at the individual level.\n\nHighlightsO_LIThe topography of Default Network cortical regions varies across individuals.\nC_LIO_LIA community detection algorithm, spectral partitioning, was applied to rs-fMRI data.\nC_LIO_LIThe algorithm identified individualized Default Network regions in mPFC and PCC.\nC_LIO_LIDefault Network topography varied across individuals in mPFC, moreso than in PCC.\nC_LIO_LIOverlap of task effects with DN regions should be assessed at the individual level.\nC_LI

neuroscience↗

Dissociable forms of uncertainty-driven representational change across the human brain.

Environmental change can lead decision makers to shift rapidly among different behavioral regimes. These behavioral shifts can be accompanied by rapid changes in the firing pattern of neural networks. However, it is unknown what the populations of neurons that participate in such \"network reset\" phenomena are representing. Here we examined 1) whether and where rapid changes in multivariate activity patterns are observable with fMRI during periods of rapid behavioral change, and 2) what types of representations give rise to these phenomena. We did so by examining fluctuations in multi-voxel patterns of BOLD activity from human subjects making sequential inferences about the state of a partially observable and discontinuously changing variable. We found that, within the context of this sequential inference task, the multivariate patterns of activity in a number of cortical regions contain representations that change more rapidly during periods of uncertainty following a change in behavioral context. In motor cortex, this phenomenon was indicative of discontinuous change in behavioral outputs, whereas in visual regions the same basic phenomenon was evoked by tracking of salient environmental changes. In most other cortical regions, including dorsolateral prefrontal and anterior cingulate cortex, the phenomenon was most consistent with directly encoding the degree of uncertainty. However, in a few other regions, including orbitofrontal cortex, the phenomenon was best explained by representations of a shifting context that evolve more rapidly during periods of rapid learning. These representations may provide a dynamic substrate for learning that facilitates rapid disengagement from learned responses during periods of change.

neuroscience↗