Human learning is a complex phenomenon requiring flexibility to adapt existing brain function and precision in selecting new neurophysiological activities to drive desired behavior. These two attributes-flexibility and selection-must operate over multiple temporal scales as performance of a skill changes from being slow and challenging to being fast and automatic. Such selective adaptability is naturally provided by modular structure, which plays a critical role in evolution, development, and optimal network function. Using functional connectivity measurements of brain activity acquired from initial training through mastery of a simple motor skill, we investigate the role of modularity in human learning by identifying dynamic changes of modular organization spanning multiple temporal scales. Our results indicate that flexibility, which we measure by the allegiance of nodes to modules, in one experimental session predicts the relative amount of learning in a future session. We also develop a general statistical framework for the identification of modular architectures in evolving systems, which is broadly applicable to disciplines where network adaptability is crucial to the understanding of system performance.complex network | time-dependent network | fMRI | motor learning | community structure T he brain is a complex system, composed of many interacting parts, which dynamically adapts to a continually changing environment over multiple temporal scales. Over relatively short temporal scales, rapid adaptation and continuous evolution of those interactions or connections form the neurophysiological basis for behavioral adaptation or learning. At small spatial scales, stable neurophysiological signatures of learning have been best demonstrated in animal systems at the level of individual synapses between neurons (1-3). At a larger spatial scale, it is also well-known that specific regional changes in brain activity and effective connectivity accompany many forms of learning in humans-including the acquisition of motor skills (4, 5).Learning-associated adaptability is thought to stem from the principle of cortical modularity (6). Modular, or nearly decomposable (7), structures are aggregates of small subsystems (modules) that can perform specific functions without perturbing the remainder of the system. Such structure provides a combination of compartmentalization and redundancy, which reduces the interdependence of components, enhances robustness, and facilitates behavioral adaptation (8, 9). Modular organization also confers evolvability on a system by reducing constraints on change (8,(10)(11)(12). Indeed, a putative relationship between modularity and adaptability in the context of human neuroscience has recently been posited (13,14). To date, however, the existence of modularity in large-scale cortical connectivity during learning has not been tested directly.Based on the aforementioned theoretical and empirical grounds, we hypothesized that the principle of modularity would characterize the fundamental organiz...
Distributed networks of brain areas interact with one another in a time-varying fashion to enable complex cognitive and sensorimotor functions. Here we used new network-analysis algorithms to test the recruitment and integration of large-scale functional neural circuitry during learning. Using functional magnetic resonance imaging data acquired from healthy human participants, we investigated changes in the architecture of functional connectivity patterns that promote learning from initial training through mastery of a simple motor skill. Our results show that learning induces an autonomy of sensorimotor systems and that the release of cognitive control hubs in frontal and cingulate cortices predicts individual differences in the rate of learning on other days of practice. Our general statistical approach is applicable across other cognitive domains and provides a key to understanding time-resolved interactions between distributed neural circuits that enable task performance.
We describe techniques for the robust detection of community structure in some classes of timedependent networks. Specifically, we consider the use of statistical null models for facilitating the principled identification of structural modules in semi-decomposable systems. Null models play an important role both in the optimization of quality functions such as modularity and in the subsequent assessment of the statistical validity of identified community structure. We examine the sensitivity of such methods to model parameters and show how comparisons to null models can help identify system scales. By considering a large number of optimizations, we quantify the variance of network diagnostics over optimizations ("optimization variance") and over randomizations of network structure ("randomization variance"). Because the modularity quality function typically has a large number of nearly degenerate local optima for networks constructed using real data, we develop a method to construct representative partitions that uses a null model to correct for statistical noise in sets of partitions. To illustrate our results, we employ ensembles of time-dependent networks extracted from both nonlinear oscillators and empirical neuroscience data. Many social, physical, technological, and biological systems can be modeled as networks composed of numerous interacting parts. 1 As an increasing amount of time-resolved data has become available, it has become increasingly important to develop methods to quantify and characterize dynamic properties of temporal networks. 2 Generalizing the study of static networks, which are typically represented using graphs, to temporal networks entails the consideration of nodes (representing entities) and/or edges (representing ties between entities) that vary in time. As one considers data with more complicated structures, the appropriate network analyses must become increasingly nuanced. In the present paper, we discuss methods for algorithmic detection of dense clusters of nodes (i.e., communities) by optimizing quality functions on multilayer network representations of temporal networks. 3,4 We emphasize the development and analysis of different types of null-model networks, whose appropriateness depends on the structure of the networks one is studying as well as the construction of representative partitions that take advantage of a multilayer network framework. To illustrate our ideas, we use ensembles of time-dependent networks from the human brain and human behavior.
As a person learns a new skill, distinct synapses, brain regions, and circuits are engaged and change over time. In this paper, we develop methods to examine patterns of correlated activity across a large set of brain regions. Our goal is to identify properties that enable robust learning of a motor skill. We measure brain activity during motor sequencing and characterize network properties based on coherent activity between brain regions. Using recently developed algorithms to detect time-evolving communities, we find that the complex reconfiguration patterns of the brain's putative functional modules that control learning can be described parsimoniously by the combined presence of a relatively stiff temporal core that is composed primarily of sensorimotor and visual regions whose connectivity changes little in time and a flexible temporal periphery that is composed primarily of multimodal association regions whose connectivity changes frequently. The separation between temporal core and periphery changes over the course of training and, importantly, is a good predictor of individual differences in learning success. The core of dynamically stiff regions exhibits dense connectivity, which is consistent with notions of core-periphery organization established previously in social networks. Our results demonstrate that core-periphery organization provides an insightful way to understand how putative functional modules are linked. This, in turn, enables the prediction of fundamental human capacities, including the production of complex goal-directed behavior.
Motor chunking facilitates movement production by combining motor elements into integrated units of behavior. Previous research suggests that chunking involves two processes: concatenation, aimed at the formation of motor-motor associations between elements or sets of elements; and segmentation, aimed at the parsing of multiple contiguous elements into shorter action sets. We used fMRI to measure the trial-wise recruitment of brain regions associated with these chunking processes as healthy subjects performed a cued sequence production task. A novel dynamic network analysis identified chunking structure for a set of motor sequences acquired during fMRI and collected on three days of training. Activity in the bilateral sensorimotor putamen positively correlated with chunk concatenation, whereas a left hemisphere frontoparietal network was correlated with chunk segmentation. Across subjects, there was an aggregate increase in chunk strength (concatenation) with training, suggesting that subcortical circuits play a direct role in the creation of fluid transitions across chunks.
In this study we examined the neural correlates of conflict processing in the Stroop, counting, and digit-location tasks using event-related brain potentials (ERPs). The behavioral data revealed robust interference in response time and accuracy for all tasks. The interference effect for response time was greater in the Stroop task than the other tasks; in contrast, the interference effect for response accuracy was greater in the counting tasks than the other tasks. The N450 and sustained potential (SP) were elicited in each task. Partial least-squares (PLS) analysis was used to examine the structural relationships between the ERPs, task design, and behavior. TaskPLS analysis revealed that the N450 and SP were associated with a single latent variable leading to the suggestion that a common set of neural generators was recruited during conflict processing across the tasks and that there were differences between ERPs related to early processing across the three tasks. BehavioralPLS analysis revealed that the amplitude of the SP was positively correlated with response time and accuracy, indicating that this modulation of the ERPs may be related to response selection rather than to conflict resolution.
This paper presents methods to analyze functional brain networks and signals from graph spectral perspectives. The notion of frequency and filters traditionally defined for signals supported on regular domains such as discrete time and image grids has been recently generalized to irregular graph domains, and defines brain graph frequencies associated with different levels of spatial smoothness across the brain regions. Brain network frequency also enables the decomposition of brain signals into pieces corresponding to smooth or rapid variations. We relate graph frequency with principal component analysis when the networks of interest denote functional connectivity. The methods are utilized to analyze brain networks and signals as subjects master a simple motor skill. We observe that brain signals corresponding to different graph frequencies exhibit different levels of adaptability throughout learning. Further, we notice a strong association between graph spectral properties of brain networks and the level of exposure to tasks performed, and recognize the most contributing and important frequency signatures at different levels of task familiarity.
Motor sequence learning is associated with increasing and decreasing motor system activity. Here, we ask whether sequence-specific activity is contingent upon the time interval and absolute amount of training over which the skill is acquired. We hypothesize that within each motor region, the strength of any sequence representation is a non-linear function that can be characterized by 3 timescales. We had subjects train for 6 weeks and measured brain activity with functional magnetic resonance imaging. We used repetition suppression (RS) to isolate sequence-specific representations while controlling for effects related to kinematics and general task familiarity. Following a baseline training session, primary and secondary motor regions demonstrated rapidly increasing RS. With continued training, there was evidence for skill-specific efficiency, characterized by a dramatic decrease in motor system RS. In contrast, after performance had reached a plateau, further training led to a pattern of slowly increasing RS in the contralateral sensorimotor cortex, supplementary motor area, ventral premotor cortex, and anterior cerebellum consistent with skill-specific specialization. Importantly, many motor areas show changes involving more than 1 of these 3 timescales, underscoring the capacity of the motor system to flexibly represent a sequence based on the amount of prior experience.
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