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Cited by 356Functional Brain Connectivity StudiesNeural dynamics and brain functionComplex Network Analysis Techniques

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Task-Based Core-Periphery Organization of Human Brain Dynamics

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Bassett, Danielle S., Wymbs, Nicholas F., Rombach, M. Puck, Porter, Mason A., Mucha, Peter J., Grafton, Scott T.·2013·PLoS Computational Biology
DOI 10.1371/journal.pcbi.1003171PMC PMC3784512
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Abstract

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.

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Figure 1 Network organization of human brain dynamics. (A) Temporal Networks of the Human Brain. We parcellate the brain into anatomical regions that can be represented as nodes in a network, and we use the coherence between functional Magnetic Resonance Imaging (fMRI) time series of each pair of nodes over a time window to determine the weight of the network edge connecting those nodes. We determine these weights separately using approximately 10 non-overlapping time windows of 2–3 min duration and thereby construct temporal networks that represent the dynamical functional connectivity in the brain. (B) Cohesive Mesoscale Structures. (top) An example of a network with a modular organization in which high-degree nodes (brown) are often found in the center of modules or bridging distinct modules that are composed mostly of low-degree nodes (blue). (bottom) A network with a core-periphery organization in which nodes in the core (purple) are more densely connected with one another than nodes in the periphery are with one another (green).
Figure 1 Network organization of human brain dynamics. (A) Temporal Networks of the Human Brain. We parcellate the brain into anatomical regions that can be represented as nodes in a network, and we use the coherence between functional Magnetic Resonance Imaging (fMRI) time series of each pair of nodes over a time window to determine the weight of the network edge connecting those nodes. We determine these weights separately using approximately 10 non-overlapping time windows of 2–3 min duration and thereby construct temporal networks that represent the dynamical functional connectivity in the brain. (B) Cohesive Mesoscale Structures. (top) An example of a network with a modular organization in which high-degree nodes (brown) are often found in the center of modules or bridging distinct modules that are composed mostly of low-degree nodes (blue). (bottom) A network with a core-periphery organization in which nodes in the core (purple) are more densely connected with one another than nodes in the periphery are with one another (green).CC BY · PubMed Central
Figure 2 Dynamic network diagnostics change with learning. (A) Multilayer modularity, (B) number of communities, and (C) mean flexibility calculated as a function of the number of trials completed after a scanning session (see Table 1 for the relationship between the number of trials practiced and training duration and intensity). We average the values for each diagnostic over the 100 multilayer modularity optimizations, and we average flexibility over the 112 brain regions (in addition to averaging over the 100 optimizations per subject). Error bars indicate the standard error of the mean over participants.
Figure 2 Dynamic network diagnostics change with learning. (A) Multilayer modularity, (B) number of communities, and (C) mean flexibility calculated as a function of the number of trials completed after a scanning session (see Table 1 for the relationship between the number of trials practiced and training duration and intensity). We average the values for each diagnostic over the 100 multilayer modularity optimizations, and we average flexibility over the 112 brain regions (in addition to averaging over the 100 optimizations per subject). Error bars indicate the standard error of the mean over participants.CC BY · PubMed Central
Figure 3 Temporal core-periphery organization of the brain. determined using fMRI signals during the performance of a simple motor learning task. (A) The core (cyan), bulk (gold), and periphery (maroon) nodes consist, respectively, of brain regions whose mean flexibility over individuals is less than, equal to, and greater than that expected in a null model (gray shaded region). We measure flexibility based on the allegiance of nodes to putative functional modules. Error bars indicate the standard error of the mean over individuals. (B) The anatomical distribution of regions in the core, bulk, and periphery appears to be spatially contiguous. The core primarily contains sensorimotor and visual processing areas, the periphery primarily contains multimodal association areas, and the bulk contains the remainder of the brain (and is therefore composed predominantly of frontal and temporal cortex).
Figure 3 Temporal core-periphery organization of the brain. determined using fMRI signals during the performance of a simple motor learning task. (A) The core (cyan), bulk (gold), and periphery (maroon) nodes consist, respectively, of brain regions whose mean flexibility over individuals is less than, equal to, and greater than that expected in a null model (gray shaded region). We measure flexibility based on the allegiance of nodes to putative functional modules. Error bars indicate the standard error of the mean over individuals. (B) The anatomical distribution of regions in the core, bulk, and periphery appears to be spatially contiguous. The core primarily contains sensorimotor and visual processing areas, the periphery primarily contains multimodal association areas, and the bulk contains the remainder of the brain (and is therefore composed predominantly of frontal and temporal cortex).CC BY · PubMed Central
Figure 4 Geometrical core-periphery organization in brain networks. (A) Core quality (5) in the parameter plane for a typical participant (3), scanning session (1), sequence type (EXT), and experimental block (1). (B) Distribution of the and values that maximize the -score. We compute this distribution over all network layers, participants, scanning sessions, and sequence types. The parameter is much more localized (its standard deviation is 0.05) than the parameter (its standard deviation is 0.26). (C) Mean core shape. We plot the ordered vector of values. We have set the values of and to the mean values of those that maximize the -score for all network layers, participants, scanning sessions, and sequence types.
Figure 4 Geometrical core-periphery organization in brain networks. (A) Core quality (5) in the parameter plane for a typical participant (3), scanning session (1), sequence type (EXT), and experimental block (1). (B) Distribution of the and values that maximize the -score. We compute this distribution over all network layers, participants, scanning sessions, and sequence types. The parameter is much more localized (its standard deviation is 0.05) than the parameter (its standard deviation is 0.26). (C) Mean core shape. We plot the ordered vector of values. We have set the values of and to the mean values of those that maximize the -score for all network layers, participants, scanning sessions, and sequence types.CC BY · PubMed Central
Figure 5 Geometrical core scores change with learning. Variance of the distribution of mean geometrical core scores over brain regions as a function of the number of trials completed after a scanning session. (See Table 1 for the relationship between the number of trials practiced and training duration and intensity.) Error bars indicate the standard error of the mean over participants (where the data point from each participant is the mean geometrical core score over brain regions, scanning sessions, sequence types, and network layers).
Figure 5 Geometrical core scores change with learning. Variance of the distribution of mean geometrical core scores over brain regions as a function of the number of trials completed after a scanning session. (See Table 1 for the relationship between the number of trials practiced and training duration and intensity.) Error bars indicate the standard error of the mean over participants (where the data point from each participant is the mean geometrical core score over brain regions, scanning sessions, sequence types, and network layers).CC BY · PubMed Central
Figure 6 Relationship between temporal and geometrical core-periphery organizations. A strong negative correlation exists between flexibility and the geometrical core score for networks constructed from blocks of (A) extensively, (B) moderately, and (C) minimally trained sequences on scanning session 1 (day 1; circles), session 2 (after approximately 2 weeks of training; squares), session 3 (after approximately 4 weeks of training; diamonds), and session 4 (after approximately 6 weeks of training; stars). This negative correlation indicates that the temporal core-periphery organization is mimicked in the geometrical core-periphery organization and therefore that the core of dynamically stiff regions also exhibits dense connectivity. We show temporal core nodes in cyan, temporal bulk nodes in gold, and temporal periphery nodes in maroon. The darkness of data points indicates scanning session; darker colors indicate earlier scans, so the darkest colors indicate scan 1 and the lightest ones indicate scan 4. The grayscale lines indicate the best linear fits; again, darker colors indicate earlier scans, so session 1 is in gray and session 4 is in light gray. The Pearson correlation between the flexibility (averaged over 100 multilayer modularity optimizations, 20 participants, and 4 scanning sessions) and the geometrical core score (averaged over 20 participants and 4 scanning sessions) is significant for the EXT (, ), MOD (, ), and MIN (, ) data.
Figure 6 Relationship between temporal and geometrical core-periphery organizations. A strong negative correlation exists between flexibility and the geometrical core score for networks constructed from blocks of (A) extensively, (B) moderately, and (C) minimally trained sequences on scanning session 1 (day 1; circles), session 2 (after approximately 2 weeks of training; squares), session 3 (after approximately 4 weeks of training; diamonds), and session 4 (after approximately 6 weeks of training; stars). This negative correlation indicates that the temporal core-periphery organization is mimicked in the geometrical core-periphery organization and therefore that the core of dynamically stiff regions also exhibits dense connectivity. We show temporal core nodes in cyan, temporal bulk nodes in gold, and temporal periphery nodes in maroon. The darkness of data points indicates scanning session; darker colors indicate earlier scans, so the darkest colors indicate scan 1 and the lightest ones indicate scan 4. The grayscale lines indicate the best linear fits; again, darker colors indicate earlier scans, so session 1 is in gray and session 4 is in light gray. The Pearson correlation between the flexibility (averaged over 100 multilayer modularity optimizations, 20 participants, and 4 scanning sessions) and the geometrical core score (averaged over 20 participants and 4 scanning sessions) is significant for the EXT (, ), MOD (, ), and MIN (, ) data.CC BY · PubMed Central
Figure 7 Core-periphery organization of brain dynamics during learning. The relationship between temporal and geometrical core-periphery organization and their associations with learning are present in individual subjects. We represent this relationship using spirals in a plane; data points in this plane represent brain regions located at the polar coordinates (, ), where is the flexibility of the region, is the skewness of flexibility over all regions, and is the learning parameter (see the Materials and Methods) that describes each individual's relative improvement between sessions. The skewness predicts individual differences in learning; the Spearman rank correlation is and . Poor learners (straighter spirals) tend to have a low skewness (short spirals), whereas good learners (curvier spirals) tend to have high skewness (long spirals). Color indicates flexibility: blue nodes have lower flexibility, and brown nodes have higher flexibility.
Figure 7 Core-periphery organization of brain dynamics during learning. The relationship between temporal and geometrical core-periphery organization and their associations with learning are present in individual subjects. We represent this relationship using spirals in a plane; data points in this plane represent brain regions located at the polar coordinates (, ), where is the flexibility of the region, is the skewness of flexibility over all regions, and is the learning parameter (see the Materials and Methods) that describes each individual's relative improvement between sessions. The skewness predicts individual differences in learning; the Spearman rank correlation is and . Poor learners (straighter spirals) tend to have a low skewness (short spirals), whereas good learners (curvier spirals) tend to have high skewness (long spirals). Color indicates flexibility: blue nodes have lower flexibility, and brown nodes have higher flexibility.CC BY · PubMed Central
Figure 8 Trial structure and stimulus-response (S-R) mapping. (A) Each trial began with the presentation of a sequence-identity cue that remained on screen for seconds. Each of the trained sequences was paired with a unique identity cue. A discrete sequence-production (DSP) event structure was used to guide sequence production. The onset of the initial DSP stimulus (thick square, colored red in the task) served as the imperative to produce the sequence. A correct key press led to the immediate presentation of the next DSP stimulus (and so on) until the -element sequence was correctly executed. Participants received a feedback “+” to signal that a sequence was completed and to wait (approximately – seconds) for the start of the next trial. This waiting period is called the “inter-trial interval” (ITI). At any point, if an incorrect key was hit, a participant would receive an error signal (not shown in the figure) and the DSP sequence would pause until the correct response was received. (B) There was a direct S-R mapping between a conventional keyboard or an MRI-compatible button box (see the lower left of the figure) and a participant's right hand, so the leftmost DSP stimulus cued the thumb and the rightmost stimulus cued the pinky finger. Note that the button location for the thumb was positioned to the lower left to achieve maximum comfort and ease of motion.
Figure 8 Trial structure and stimulus-response (S-R) mapping. (A) Each trial began with the presentation of a sequence-identity cue that remained on screen for seconds. Each of the trained sequences was paired with a unique identity cue. A discrete sequence-production (DSP) event structure was used to guide sequence production. The onset of the initial DSP stimulus (thick square, colored red in the task) served as the imperative to produce the sequence. A correct key press led to the immediate presentation of the next DSP stimulus (and so on) until the -element sequence was correctly executed. Participants received a feedback “+” to signal that a sequence was completed and to wait (approximately – seconds) for the start of the next trial. This waiting period is called the “inter-trial interval” (ITI). At any point, if an incorrect key was hit, a participant would receive an error signal (not shown in the figure) and the DSP sequence would pause until the correct response was received. (B) There was a direct S-R mapping between a conventional keyboard or an MRI-compatible button box (see the lower left of the figure) and a participant's right hand, so the leftmost DSP stimulus cued the thumb and the rightmost stimulus cued the pinky finger. Note that the button location for the thumb was positioned to the lower left to achieve maximum comfort and ease of motion.CC BY · PubMed Central
Figure 9 Experiment timeline. Training sessions in the MRI scanner during the collection of blood-oxygen-level-dependent (BOLD) signals were interleaved with training sessions at home. Participants first practiced the sequences in the MRI scanner during a baseline training session (top). Following every approximately 10 training sessions (see Table S1), participants returned for another scanning session. During each scanning session, a participant practiced each sequence for 50 trials. Participants trained at home between the scanning sessions (bottom). During each home training session, participants practiced the sequences in a random order. (We determined a random order using the Mersenne Twister algorithm of Nishimura and Matsumoto [101] as implemented in the random number generator rand.m of Matlab version 7.1). Each EXT sequence was practiced for 64 trials, each MOD sequence was practiced for 10 trials, and each MIN sequence was practiced for 1 trial.
Figure 9 Experiment timeline. Training sessions in the MRI scanner during the collection of blood-oxygen-level-dependent (BOLD) signals were interleaved with training sessions at home. Participants first practiced the sequences in the MRI scanner during a baseline training session (top). Following every approximately 10 training sessions (see Table S1), participants returned for another scanning session. During each scanning session, a participant practiced each sequence for 50 trials. Participants trained at home between the scanning sessions (bottom). During each home training session, participants practiced the sequences in a random order. (We determined a random order using the Mersenne Twister algorithm of Nishimura and Matsumoto [101] as implemented in the random number generator rand.m of Matlab version 7.1). Each EXT sequence was practiced for 64 trials, each MOD sequence was practiced for 10 trials, and each MIN sequence was practiced for 1 trial.CC BY · PubMed Central

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Metadata

Authors
Bassett, D. S., Wymbs, N. F., Rombach, M. P., Porter, M. A., Mucha, P. J., & Grafton, S. T.
Affiliations
  • University of California, Santa Barbara (US)
  • University of Oxford (GB)
  • University of North Carolina at Chapel Hill (US)
Corresponding author
  • Bassett, Danielle S.
  • Wymbs, Nicholas F.
  • Rombach, M. Puck
  • Porter, Mason A.
  • Mucha, Peter J.
  • Grafton, Scott T.
ORCID
Venue
PLoS Computational Biology
Publisher
Public Library of Science (PLoS)
Published
2013-09-26
Volume
9
Issue
9
Pages
e1003171
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
DOI
10.1371/journal.pcbi.1003171
PMC
PMC3784512
OpenAlex
W2962725064
Cited by
356
References
124
Citations by year
2026: 12 · 2025: 15 · 2024: 24 · 2023: 23 · 2022: 28 · 2021: 32 · 2020: 29 · 2019: 31 · 2018: 37 · 2017: 51 · 2016: 34 · 2015: 21 · 2014: 15 · 2013: 4
FWCI
13.29
Type
journal article
Language
en
Update notices
correction (2014-04-11)
Open access
Licence
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Oxford University Research Archive (ORA) (University of Oxford) (acceptedVersion)
  • Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • Figshare (submittedVersion, cc-by)
  • UNC Libraries
Funders
  • David and Lucile Packard Foundation (W911NF-09-D-0001)
  • James S. McDonnell Foundation (220020177)
  • John Templeton Foundation
  • Errett Fisher Foundation
  • European Commission (FP7 ICT, 317614, ICT-2011, FP7‐ICT‐2011‐8, FP7‐ICT‐2011)
  • Engineering and Physical Sciences Research Council (EP/J001759/1, 317614, 220020177)
  • National Institute of General Medical Sciences (R21GM099493, D-0001)
  • National Institute of Neurological Disorders and Stroke (NS 44393, P01NS044393)
  • Army Research Office (#W911NF-09-D-0001, W911NF)
  • FP7 Information and Communication Technologies (FP7-ICT-2011-8)
  • Institute for Collaborative Biotechnologies (W911NF‐09‐D‐0001)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Complex Network Analysis Techniques
Keywords
brain dynamics, motor skill learning, motor sequencing, sensorimotor regions, individual differences in learning, goal-directed behavior, brain connectivity
MeSH terms
Brain, Humans, Learning, Task Performance and Analysis

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