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Task-general and task-specifying functional brain dynamics · r = .24 p = .016 Task-general and...

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r = .24 p = .016 Task-general and task-specifying functional brain dynamics Douglas H. Schultz & Michael W. Cole Rutgers University - Newark Introduction Conclusions We recently found that the human brain’s functional networks are similar but not identical between rest and a variety of task states (Cole et al., 2014). Here we sought to characterize these changes from rest, identifying the network dynamics that likely make adaptive, task-specific behavior possible. Methods Data from the Human Connectome Project (WU-Minn consortium, N=100) was used for analysis. This involved 60 min of rest functional MRI (fMRI) data, as well as 45 min of task fMRI data split among seven highly distinct tasks (as previously described; Barch et al., 2013). We conducted a series of analyses comparing functional connectivity across previously defined brain regions and networks (Power et al., 2011). Configuration of FC is consistent across many different tasks Emotion Task 352 TRs Calculate functional connectivity (FC) between each of the 264 regions for each subject Task Gambling Task 506 TRs Language Task 632 TRs Motor Task 568 TRs Relational Task 464 TRs Social Task 548 TRs Working Memory Task 810 TRs Equivalent # of TRs Rest 50 100 150 200 250 50 100 150 200 250 Regions Regions Number of tasks showing a significant increase in FC from rest 50 100 150 200 250 50 100 150 200 250 Regions Regions Number of tasks showing a significant decrease in FC from rest Other Sensorimotor Cingulo-opercular Auditory Default Mode Visual Fronto-parietal Salience Subcortical Ventral Attention Dorsal Attention Number of tasks 0 7 How does task-general FC relate to behavior? Language Task Relational Task Working Memory Task r = .25 p = .012 r = .27 p = .006 Is the similarity between task and rest FC related to behavior? Do high fluid intelligence individuals have more effective network architectures? Relational Task r = .34 p = .001 r = .25 p = .014 Working Memory Task r = .32 p = .001 Language Task FC patterns are consistent across many different tasks Task-general FC architecture is important for task performance High performers show similar task and rest FC More efficient brain network updates Effective task network configurations related to high fluid intelligence References Barch, D.M., et al.; WU-Minn HCP Consortium (2013). Function in the human connectome: task-fMRI and individual differences in behavior. Neuroimage 80, 169–189. Cole, M.W., et al., (2014). Intrinsic and task-evoked network architectures of the human brain. Neuron, 83, 238-251. Cole, M.W., et al., (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nature Neuroscience, 16, 1348-55. Power, J.D., et al., (2011). Functional network organization of the human brain. Neuron 72, 665–678. a From Cole et al., 2013 Comparisons Task-specific FC to task-general FC (mean of other 6 tasks) Task-specific FC to rest FC Task-specific FC to mean task- specific FC (top 5 fluid intelligence) r = .31 p =.007 Language Task Relational Task Working Memory Task r = .25 p = .012 r = .23 p =.02 Similarity between task-specific FC and task-general FC is positively correlated with behavior Similarity between task-specific FC and rest FC is positively correlated with behavior Similarity (of task-specific FC) with high fluid intelligence participants is positively correlated with behavior Email address: [email protected] Lab website: www.colelab.org
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Page 1: Task-general and task-specifying functional brain dynamics · r = .24 p = .016 Task-general and task-specifying functional brain dynamics Douglas H. Schultz & Michael W. Cole Rutgers

r = .24 p = .016

Task-general and task-specifying functional brain dynamics Douglas H. Schultz & Michael W. Cole

Rutgers University - Newark

Introduction

Conclusions

We recently found that the human brain’s functional networks are similar but not identical between rest and a variety of task states (Cole et al., 2014). Here we sought to characterize these changes from rest, identifying the network dynamics that likely make adaptive, task-specific behavior possible.

Methods Data from the Human Connectome Project (WU-Minn consortium, N=100) was used for analysis. This involved 60 min of rest functional MRI (fMRI) data, as well as 45 min of task fMRI data split among seven highly distinct tasks (as previously described; Barch et al., 2013). We conducted a series of analyses comparing functional connectivity across previously defined brain regions and networks (Power et al., 2011).

Configuration of FC is consistent across many different tasks

Emotion Task 352 TRs

Calculate functional connectivity (FC) between each of the 264 regions for each

subject Task

Gambling Task 506 TRs

Language Task 632 TRs

Motor Task 568 TRs

Relational Task 464 TRs

Social Task 548 TRs

Working Memory Task 810 TRs Equivalent # of TRs

Rest

50

100

150

200

250

50 100 150 200 250Regions

Regions

01234567

Number of tasks showing a significant increase in FC from rest

50

100

150

200

250

50 100 150 200 250Regions

Regions

01234567

Number of tasks showing a significant decrease in FC from rest

Other

Sensorimotor

Cingulo-opercular

Auditory

Default Mode

Visual

Fronto-parietal

Salience

Subcortical Ventral Attention

Dorsal Attention

50100

150

200

250

50100

150

200

250

Regions

Regions

0 1 2 3 4 5 6 750100

150

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250

50100

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250

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Regions

0 1 2 3 4 5 6 7

Number of tasks

0 7

How does task-general FC relate to behavior? Language Task Relational Task Working Memory Task

r = .25 p = .012

r = .27 p = .006

Is the similarity between task and rest FC related to behavior?

Do high fluid intelligence individuals have more effective network architectures?

Relational Task

r = .34 p = .001

r = .25 p = .014

Working Memory Task

r = .32 p = .001

Language Task

u FC patterns are consistent across many different tasks

u Task-general FC architecture is important for task performance

u High performers show similar task and rest FC u More efficient brain network updates

u Effective task network configurations related to high fluid intelligence

References Barch, D.M., et al.; WU-Minn HCP Consortium (2013). Function in the human connectome: task-fMRI and individual differences in behavior. Neuroimage 80, 169–189. Cole, M.W., et al., (2014). Intrinsic and task-evoked network architectures of the human brain. Neuron, 83, 238-251. Cole, M.W., et al., (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nature Neuroscience, 16, 1348-55. Power, J.D., et al., (2011). Functional network organization of the human brain. Neuron 72, 665–678.

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across the full set of task rule domains (logical decision, sensory semantic and motor response rules) and across the entire FPN as an integrated network.

To carry out these investigations, we relied on advances in techniques for identifying the brain’s functional networks and the regions that comprise these net-works. Specifically, it is now possible to partition the brain into a set of intrinsic functional networks independent of any particular task state9,28. We used a previously described network partitioning scheme9 that identifies the FPN as one of ten major functional net-works in the human brain (Fig. 3a), independently of the current data set and the 64 task states. We then estimated task-state functional connectivity patterns among the regions that comprise these networks (Fig. 3b) to test for the existence of flexible hubs in the FPN. Flexible hubs were identified as regions with functional connectivity patterns that met two key criteria: consistent variability across many task states and consistent variability across many brain networks. This is in con-trast with most previous definitions of hubs, which involve static or non-dynamic (resting-state functional or anatomical connectivity) estimates of global connectivity and therefore do not address the pos-sible task-dependent dynamics of these highly connected regions22,23 (although there has been some characterization of hub dynamics dur-ing resting state29).

In summary, we hypothesized that the FPN would involve greater variable connectivity across networks and across tasks than other networks. Furthermore, we expected that these connectivity changes would map systematically to the currently implemented task compo-nents. We examined compositional coding by first testing whether connectivity patterns encoded the similarity relationships between tasks, and then testing whether these distributed connectivity pat-terns could be used to reliably decode which task was being per-formed. Lastly, we examined whether such adaptive connectivity patterns could be used to implement practiced-to-novel transfer in task state classification. Confirmation of the presence of both global variable connectivity and compositional coding in the FPN would provide strong support for the idea that this brain network implements core flexible hub mechanisms. As such, we hoped to provide a more comprehensive account of how the human brain, via interactions between the FPN and other brain networks, might enable cognitive control across a wide variety of distinct task demands.

Answer: TRUE(Left index finger)

Answer: TRUE(Right middle finger)

SAMESWEET

LEFT INDEX

InstructionsTrials

LeafDynamite

Trials

GeckoLeaf

Answer: FALSE(Left middle finger)Trials

Task 1

SECONDLOUD

RIGHT MIDDLE

Instructions

Task 2

JUST ONEGREEN

LEFT INDEX

Instructions

Task 64

Task 1 description:If the answer to ‘is it SWEET?’is the SAME for both words,press your LEFT INDEX finger

Task 2 description:If the answer to ‘is it LOUD?’is yes for the second word,press your RIGHT MIDDLE finger

Task 64 description:If the answer to ‘is it GREEN?’is yes for JUST ONE of the words,press your LEFT INDEX finger[opposite finger on same hand if false]

3 s 2 s each

Practiced tasks:Trained in prior 2-h sessionFour per participant, 60 across participantsAll 12 rules included for each participant

Novel tasks:Never seen before60 per participant, 64 across participantsAll 12 rules included for each participant

GrapeApple

Figure 2 The permuted rule operations behavioral procedure, in combination with recent advances in task-state connectivity methods, allows detection of flexible connectivity across a wide variety of task states. The procedure was designed to efficiently visit a variety of task states (60 novel and four practiced previously per subject) while controlling for extraneous factors across those task states (for example, input and output modalities, task timing, and stimuli). Tasks were defined as unique combinations of rules, such that the same stimuli would elicit a distinct set of cognitive operations across distinct tasks. We included 12 rules across three qualitatively distinct domains, allowing for a well-controlled sampling of a moderately sized space of possible task states spanning multiple cognitive (logical decision rules), sensory (sensory semantic rules) and motor (motor response rules) processes. Participants were over 90% accurate for both novel and practiced tasks7.

a

b

NetworksFPN (fronto-parietal)CON (cingulo-opercular)SAN (salience)DAN (dorsal attention)VAN (ventral attention)DMN (default-mode)Motor and somatosensoryAuditoryVisualSubcortical

Context-independent connectivity

Mean task activity(64 tasks)

Context-dependent connectivity (64 tasks)

y = 0S + 1T1 + ... + 64T64 + 65 (S × bin(T1)) + ... + 129 (S × bin(T64))

Figure 3 Graph theoretical brain network partition and context-dependent functional connectivity estimation. (a) Network partition of 264 putative functional regions described previously9. The ten major networks (node communities) are labeled on the right. (b) The linear regression model equation (gPPI8) used to estimate context-dependent functional connectivity (between each pair of the 264 regions) while controlling for mean activation and context-independent functional connectivity. S is the ‘seed’ region’s time series and T is a given task’s timing (convolved with a hemodynamic response function). S × bin(T) is the seed time series multiplied by the binary version of a given task’s timing (all values above 0 set to 1), which results in the simple linear regression fitting of one region’s time series to another during each task context. Similar to the standard definition used for resting-state functional connectivity MRI46, functional connectivity is defined here as the linear association between two brain regions’ neural activity time series (likely reflecting direct or indirect communication), measured indirectly here using blood oxygen level–dependent fMRI (Online Methods).

From Cole et al., 2013

Comparisons Task-specific FC to task-general

FC (mean of other 6 tasks)

Task-specific FC to rest FC

Task-specific FC to mean task-

specific FC (top 5 fluid intelligence)

r = .31 p =.007

Language Task Relational Task Working Memory Task

r = .25 p = .012

r = .23 p =.02

Similarity between task-specific FC and task-general FC is positively correlated with behavior

Similarity between task-specific FC and rest FC is positively correlated with behavior

Similarity (of task-specific FC) with high fluid intelligence participants is positively correlated with behavior

Email address: [email protected] Lab website: www.colelab.org

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