Microstructural and neurochemical plasticity mechanisms interact to enhance human perceptual decision-making.

Experience and training are known to boost our skills and mold the brain's organization and function. Yet, structural plasticity and functional neurotransmission are typically studied at different scales (large-scale networks, local circuits), limiting our understanding of the adaptive interactions that support learning of complex cognitive skills in the adult brain. Here, we employ multimodal brain imaging to investigate the link between microstructural (myelination) and neurochemical (GABAergic) plasticity for decision-making. We test (in males, due to potential confounding menstrual cycle effects on GABA measurements in females) for changes in MRI-measured myelin, GABA, and functional connectivity before versus after training on a perceptual decision task that involves identifying targets in clutter. We demonstrate that training alters subcortical (pulvinar, hippocampus) myelination and its functional connectivity to visual cortex and relates to decreased visual cortex GABAergic inhibition. Modeling interactions between MRI measures of myelin, GABA, and functional connectivity indicates that pulvinar myelin plasticity interacts-through thalamocortical connectivity-with GABAergic inhibition in visual cortex to support learning. Our findings propose a dynamic interplay of adaptive microstructural and neurochemical plasticity in subcortico-cortical circuits that supports learning for optimized decision-making in the adult human brain.

Neurochemical and functional interactions for improved perceptual decisions through training.

Learning and experience are known to improve our ability to make perceptual decisions. Yet, our understanding of the brain mechanisms that support improved perceptual decisions through training remains limited. Here, we test the neurochemical and functional interactions that support learning for perceptual decisions in the context of an orientation identification task. Using magnetic resonance spectroscopy (MRS), we measure neurotransmitters (i.e., glutamate, GABA) that are known to be involved in visual processing and learning in sensory [early visual cortex (EV)] and decision-related [dorsolateral prefrontal cortex (DLPFC)] brain regions. Using resting-state functional magnetic resonance imaging (rs-fMRI), we test for functional interactions between these regions that relate to decision processes. We demonstrate that training improves perceptual judgments (i.e., orientation identification), as indicated by faster rates of evidence accumulation after training. These learning-dependent changes in decision processes relate to lower EV glutamate levels and EV-DLPFC connectivity, suggesting that glutamatergic excitation and functional interactions between visual and dorsolateral prefrontal cortex facilitate perceptual decisions. Further, anodal transcranial direct current stimulation (tDCS) in EV impairs learning, suggesting a direct link between visual cortex excitation and perceptual decisions. Our findings advance our understanding of the role of learning in perceptual decision making, suggesting that glutamatergic excitation for efficient sensory processing and functional interactions between sensory and decision-related regions support improved perceptual decisions.NEW & NOTEWORTHY Combining multimodal brain imaging [magnetic resonance spectroscopy (MRS), functional connectivity] with interventions [transcranial direct current stimulation (tDCS)], we demonstrate that glutamatergic excitation and functional interactions between sensory (visual) and decision-related (dorsolateral prefrontal cortex) areas support our ability to optimize perceptual decisions through training.

A New Remote Guided Method for Supervised Web-Based Cognitive Testing to Ensure High-Quality Data: Development and Usability Study.

BACKGROUND: The global COVID-19 pandemic has triggered a fundamental reexamination of how human psychological research can be conducted safely and robustly in a new era of digital working and physical distancing. Online web-based testing has risen to the forefront as a promising solution for the rapid mass collection of cognitive data without requiring human contact. However, a long-standing debate exists over the data quality and validity of web-based studies. This study examines the opportunities and challenges afforded by the societal shift toward web-based testing and highlights an urgent need to establish a standard data quality assurance framework for online studies. OBJECTIVE: This study aims to develop and validate a new supervised online testing methodology, remote guided testing (RGT). METHODS: A total of 85 healthy young adults were tested on 10 cognitive tasks assessing executive functioning (flexibility, memory, and inhibition) and learning. Tasks were administered either face-to-face in the laboratory (n=41) or online using remote guided testing (n=44) and delivered using identical web-based platforms (Cambridge Neuropsychological Test Automated Battery, Inquisit, and i-ABC). Data quality was assessed using detailed trial-level measures (missed trials, outlying and excluded responses, and response times) and overall task performance measures. RESULTS: The results indicated that, across all data quality and performance measures, RGT data was statistically-equivalent to in-person data collected in the lab (P>.40 for all comparisons). Moreover, RGT participants out-performed the lab group on measured verbal intelligence (P<.001), which could reflect test environment differences, including possible effects of mask-wearing on communication. CONCLUSIONS: These data suggest that the RGT methodology could help ameliorate concerns regarding online data quality-particularly for studies involving high-risk or rare cohorts-and offer an alternative for collecting high-quality human cognitive data without requiring in-person physical attendance.

Functional Interactions between Sensory and Memory Networks for Adaptive Behavior.

The brain's capacity to adapt to sensory inputs is key for processing sensory information efficiently and interacting in new environments. Following repeated exposure to the same sensory input, brain activity in sensory areas is known to decrease as inputs become familiar, a process known as adaptation. Yet, the brain-wide mechanisms that mediate adaptive processing remain largely unknown. Here, we combine multimodal brain imaging (functional magnetic resonance imaging [fMRI], magnetic resonance spectroscopy) with behavioral measures of orientation-specific adaptation (i.e., tilt aftereffect) to investigate the functional and neurochemical mechanisms that support adaptive processing. Our results reveal two functional brain networks: 1) a sensory-adaptation network including occipital and dorsolateral prefrontal cortex regions that show decreased fMRI responses for repeated stimuli and 2) a perceptual-memory network including regions in the parietal memory network (PMN) and dorsomedial prefrontal cortex that relate to perceptual bias (i.e., tilt aftereffect). We demonstrate that adaptation relates to increased occipito-parietal connectivity, while decreased connectivity between sensory-adaptation and perceptual-memory networks relates to GABAergic inhibition in the PMN. Thus, our findings provide evidence that suppressive interactions between sensory-adaptation (i.e., occipito-parietal) and perceptual-memory (i.e., PMN) networks support adaptive processing and behavior, proposing a key role of memory systems in efficient sensory processing.

Fine-scale computations for adaptive processing in the human brain.

Adapting to the environment statistics by reducing brain responses to repetitive sensory information is key for efficient information processing. Yet, the fine-scale computations that support this adaptive processing in the human brain remain largely unknown. Here, we capitalise on the sub-millimetre resolution of ultra-high field imaging to examine functional magnetic resonance imaging signals across cortical depth and discern competing hypotheses about the brain mechanisms (feedforward vs. feedback) that mediate adaptive processing. We demonstrate layer-specific suppressive processing within visual cortex, as indicated by stronger BOLD decrease in superficial and middle than deeper layers for gratings that were repeatedly presented at the same orientation. Further, we show altered functional connectivity for adaptation: enhanced feedforward connectivity from V1 to higher visual areas, short-range feedback connectivity between V1 and V2, and long-range feedback occipito-parietal connectivity. Our findings provide evidence for a circuit of local recurrent and feedback interactions that mediate rapid brain plasticity for adaptive information processing.

Multimodal imaging of brain connectivity reveals predictors of individual decision strategy in statistical learning.

Successful human behaviour depends on the brain's ability to extract meaningful structure from information streams and make predictions about future events. Individuals can differ markedly in the decision strategies they use to learn the environment's statistics, yet we have little idea why. Here, we investigate whether the brain networks involved in learning temporal sequences without explicit reward differ depending on the decision strategy that individuals adopt. We demonstrate that individuals alter their decision strategy in response to changes in temporal statistics and engage dissociable circuits: extracting the exact sequence statistics relates to plasticity in motor corticostriatal circuits, while selecting the most probable outcomes relates to plasticity in visual, motivational and executive corticostriatal circuits. Combining graph metrics of functional and structural connectivity, we provide evidence that learning-dependent changes in these circuits predict individual decision strategy. Our findings propose brain plasticity mechanisms that mediate individual ability for interpreting the structure of variable environments.

Learning to optimize perceptual decisions through suppressive interactions in the human brain.

Translating noisy sensory signals to perceptual decisions is critical for successful interactions in complex environments. Learning is known to improve perceptual judgments by filtering external noise and task-irrelevant information. Yet, little is known about the brain mechanisms that mediate learning-dependent suppression. Here, we employ ultra-high field magnetic resonance spectroscopy of GABA to test whether suppressive processing in decision-related and visual areas facilitates perceptual judgments during training. We demonstrate that parietal GABA relates to suppression of task-irrelevant information, while learning-dependent changes in visual GABA relate to enhanced performance in target detection and feature discrimination tasks. Combining GABA measurements with functional brain connectivity demonstrates that training on a target detection task involves local connectivity and disinhibition of visual cortex, while training on a feature discrimination task involves inter-cortical interactions that relate to suppressive visual processing. Our findings provide evidence that learning optimizes perceptual decisions through suppressive interactions in decision-related networks.

White-Matter Pathways for Statistical Learning of Temporal Structures.

Extracting the statistics of event streams in natural environments is critical for interpreting current events and predicting future ones. The brain is known to rapidly find structure and meaning in unfamiliar streams of sensory experience, often by mere exposure to the environment (i.e., without explicit feedback). Yet, we know little about the brain pathways that support this type of statistical learning. Here, we test whether changes in white-matter (WM) connectivity due to training relate to our ability to extract temporal regularities. By combining behavioral training and diffusion tensor imaging (DTI), we demonstrate that humans adapt to the environment's statistics as they change over time from simple repetition to probabilistic combinations. In particular, we show that learning relates to the decision strategy that individuals adopt when extracting temporal statistics. We next test for learning-dependent changes in WM connectivity and ask whether they relate to individual variability in decision strategy. Our DTI results provide evidence for dissociable WM pathways that relate to individual strategy: extracting the exact sequence statistics (i.e., matching) relates to connectivity changes between caudate and hippocampus, while selecting the most probable outcomes in a given context (i.e., maximizing) relates to connectivity changes between prefrontal, cingulate and basal ganglia (caudate, putamen) regions. Thus, our findings provide evidence for distinct cortico-striatal circuits that show learning-dependent changes of WM connectivity and support individual ability to learn behaviorally-relevant statistics.

Functional brain networks for learning predictive statistics.

Making predictions about future events relies on interpreting streams of information that may initially appear incomprehensible. This skill relies on extracting regular patterns in space and time by mere exposure to the environment (i.e., without explicit feedback). Yet, we know little about the functional brain networks that mediate this type of statistical learning. Here, we test whether changes in the processing and connectivity of functional brain networks due to training relate to our ability to learn temporal regularities. By combining behavioral training and functional brain connectivity analysis, we demonstrate that individuals adapt to the environment's statistics as they change over time from simple repetition to probabilistic combinations. Further, we show that individual learning of temporal structures relates to decision strategy. Our fMRI results demonstrate that learning-dependent changes in fMRI activation within and functional connectivity between brain networks relate to individual variability in strategy. In particular, extracting the exact sequence statistics (i.e., matching) relates to changes in brain networks known to be involved in memory and stimulus-response associations, while selecting the most probable outcomes in a given context (i.e., maximizing) relates to changes in frontal and striatal networks. Thus, our findings provide evidence that dissociable brain networks mediate individual ability in learning behaviorally-relevant statistics.