Neural Fingerprints Underlying Individual Language Learning Profiles.

Human language learning differs significantly across individuals in the process and ultimate attainment. Although decades of research exploring the neural substrates of language learning have identified distinct and overlapping neural networks subserving learning of different components, the neural mechanisms that drive the large interindividual differences are still far from being understood. Here we examine to what extent the neural dynamics of multiple brain networks in men and women across sessions of training contribute to explaining individual differences in learning multiple linguistic components (i.e., vocabulary, morphology, and phrase and sentence structures) of an artificial language in a 7 d training and imaging paradigm with functional MRI. With machine-learning and predictive modeling, neural activation patterns across training sessions were highly predictive of individual learning success profiles derived from the four components. We identified four neural learning networks (i.e., the Perisylvian, frontoparietal, salience, and default-mode networks) and examined their dynamic contributions to the learning success prediction. Moreover, the robustness of the predictions systematically changes across networks depending on specific training phases and the learning components. We further demonstrate that a subset of network nodes in the inferior frontal, insular, and frontoparietal regions increasingly represent newly acquired language knowledge, while the multivariate connectivity between these representation regions is enhanced during learning for more successful learners. These findings allow us to understand why learners differ and are the first to attribute not only the degree of success but also patterns of language learning across components, to neural fingerprints summarized from multiple neural network dynamics.SIGNIFICANCE STATEMENT Individual differences in learning a language are widely observed not only within the same component of language but also across components. This study demonstrates that the dynamics of multiple brain networks across four imaging sessions of a 7 d artificial language training contribute to individual differences in learning-outcome profiles derived from four language components. With machine-learning predictive modeling, we identified four neural learning networks, including the Perisylvian, frontoparietal, salience, and default-mode networks, that contribute to predicting individual learning-outcome profiles and revealed language-component-general and component-specific prediction patterns across training sessions. These findings provide significant insights in understanding training-dependent neural dynamics underlying individual differences in learning success across language components.

A distributed dynamic brain network mediates linguistic tone representation and categorization.

Successful categorization requires listeners to represent the incoming sensory information, resolve the "blooming, buzzing confusion" inherent to noisy sensory signals, and leverage the accumulated evidence towards making a decision. Despite decades of intense debate, the neural systems underlying speech categorization remain unresolved. Here we assessed the neural representation and categorization of lexical tones by native Mandarin speakers (N = 31) across a range of acoustic and contextual variabilities (talkers, perceptual saliences, and stimulus-contexts) using functional magnetic imaging (fMRI) and an evidence accumulation model of decision-making. Univariate activation and multivariate pattern analyses reveal that the acoustic-variability-tolerant representations of tone category are observed within the middle portion of the left superior temporal gyrus (STG). Activation patterns in the frontal and parietal regions also contained category-relevant information that was differentially sensitive to various forms of variability. The robustness of neural representations of tone category in a distributed fronto-temporoparietal network is associated with trial-by-trial decision-making parameters. These findings support a hybrid model involving a representational core within the STG that operates dynamically within an extensive frontoparietal network to support the representation and categorization of linguistic pitch patterns.

Neural dynamics underlying the acquisition of distinct auditory category structures.

Despite the multidimensional and temporally fleeting nature of auditory signals we quickly learn to assign novel sounds to behaviorally relevant categories. The neural systems underlying the learning and representation of novel auditory categories are far from understood. Current models argue for a rigid specialization of hierarchically organized core regions that are fine-tuned to extracting and mapping relevant auditory dimensions to meaningful categories. Scaffolded within a dual-learning systems approach, we test a competing hypothesis: the spatial and temporal dynamics of emerging auditory-category representations are not driven by the underlying dimensions but are constrained by category structure and learning strategies. To test these competing models, we used functional Magnetic Resonance Imaging (fMRI) to assess representational dynamics during the feedback-based acquisition of novel non-speech auditory categories with identical dimensions but differing category structures: rule-based (RB) categories, hypothesized to involve an explicit sound-to-rule mapping network, and information integration (II) based categories, involving pre-decisional integration of dimensions via a procedural-based sound-to-reward mapping network. Adults were assigned to either the RB (n = 30, 19 females) or II (n = 30, 22 females) learning tasks. Despite similar behavioral learning accuracies, learning strategies derived from computational modeling and involvements of corticostriatal systems during feedback processing differed across tasks. Spatiotemporal multivariate representational similarity analysis revealed an emerging representation within an auditory sensory-motor pathway exclusively for the II learning task, prominently involving the superior temporal gyrus (STG), inferior frontal gyrus (IFG), and posterior precentral gyrus. In contrast, the RB learning task yielded distributed neural representations within regions involved in cognitive-control and attentional processes that emerged at different time points of learning. Our results unequivocally demonstrate that auditory learners' neural systems are highly flexible and show distinct spatial and temporal patterns that are not dimension-specific but reflect underlying category structures and learning strategies.

Task-General and Acoustic-Invariant Neural Representation of Speech Categories in the Human Brain.

A significant neural challenge in speech perception includes extracting discrete phonetic categories from continuous and multidimensional signals despite varying task demands and surface-acoustic variability. While neural representations of speech categories have been previously identified in frontal and posterior temporal-parietal regions, the task dependency and dimensional specificity of these neural representations are still unclear. Here, we asked native Mandarin participants to listen to speech syllables carrying 4 distinct lexical tone categories across passive listening, repetition, and categorization tasks while they underwent functional magnetic resonance imaging (fMRI). We used searchlight classification and representational similarity analysis (RSA) to identify the dimensional structure underlying neural representation across tasks and surface-acoustic properties. Searchlight classification analyses revealed significant "cross-task" lexical tone decoding within the bilateral superior temporal gyrus (STG) and left inferior parietal lobule (LIPL). RSA revealed that the LIPL and LSTG, in contrast to the RSTG, relate to 2 critical dimensions (pitch height, pitch direction) underlying tone perception. Outside this core representational network, we found greater activation in the inferior frontal and parietal regions for stimuli that are more perceptually similar during tone categorization. Our findings reveal the specific characteristics of fronto-tempo-parietal regions that support speech representation and categorization processing.

Functional magnetic resonance imaging data for the neural dynamics underlying the acquisition of distinct auditory categories.

How people learn and represent auditory categories in the brain is a fundamental question in auditory neuroscience. Answering this question could provide insights into our understanding of the neurobiology of speech learning and perception. However, the neural mechanisms underlying auditory category learning are far from understood. We have revealed that the neural representations of auditory categories emerge during category training, and the type of category structures drives the emerging dynamics of the representations [1]. The dataset introduced here was derived from [1], where we collected to examine the neural dynamics underlying the acquisition of two distinct category structures: rule-based (RB) and information-integration (II) categories. Participants were trained to categorize these auditory categories with trial-by-trial corrective feedback. The functional magnetic resonance imaging (fMRI) technique was used to assess the neural dynamics related to the category learning process. Sixty adult Mandarin native speakers were recruited for the fMRI experiment. They were assigned to either the RB (n = 30, 19 females) or II (n = 30, 22 females) learning task. Each task consisted of six training blocks where each consisting of 40 trials. Spatiotemporal multivariate representational similarity analysis has been used to examine the emerging patterns of neural representations during learning [1]. This open-access dataset could potentially be reused to investigate a range of neural mechanisms (e.g., functional network organizations underlying learning of different structures of categories and neuromarkers associated with individual behavioral learning success) involved in auditory category learning.

Distribution-dependent representations in auditory category learning and generalization.

A fundamental objective in Auditory Sciences is to understand how people learn to generalize auditory category knowledge in new situations. How we generalize to novel scenarios speaks to the nature of acquired category representations and generalization mechanisms in handling perceptual variabilities and novelty. The dual learning system (DLS) framework proposes that auditory category learning involves an explicit, hypothesis-testing learning system, which is optimal for learning rule-based (RB) categories, and an implicit, procedural-based learning system, which is optimal for learning categories requiring pre-decisional information integration (II) across acoustic dimensions. Although DLS describes distinct mechanisms of two types of category learning, it is yet clear the nature of acquired representations and how we transfer them to new contexts. Here, we conducted three experiments to examine differences between II and RB category representations by examining what acoustic and perceptual novelties and variabilities affect learners' generalization success. Learners can successfully categorize different sets of untrained sounds after only eight blocks of training for both II and RB categories. The category structures and novel contexts differentially modulated the generalization success. The II learners significantly decreased generalization performances when categorizing new items derived from an untrained perceptual area and in a context with more distributed samples. In contrast, RB learners' generalizations are resistant to changes in perceptual regions but are sensitive to changes in sound dispersity. Representational similarity modeling revealed that the generalization in the more dispersed sampling context was accomplished differently by II and RB learners. II learners increased representations of perceptual similarity and decision distance to compensate for the decreased transfer of category representations, whereas the RB learners used a more computational cost strategy by default, computing the decision-bound distance to guide generalization decisions. These results suggest that distinct representations emerged after learning the two types of category structures and using different computations and flexible mechanisms in resolving generalization challenges when facing novel perceptual variability in new contexts. These findings provide new evidence for dissociated representations of auditory categories and reveal novel generalization mechanisms in resolving variabilities to maintain perceptual constancy.