The human brain is intrinsically organized into dynamic, anticorrelated functional networks.
Journal: 2005/September - Proceedings of the National Academy of Sciences of the United States of America
ISSN: 0027-8424
Abstract:
During performance of attention-demanding cognitive tasks, certain regions of the brain routinely increase activity, whereas others routinely decrease activity. In this study, we investigate the extent to which this task-related dichotomy is represented intrinsically in the resting human brain through examination of spontaneous fluctuations in the functional MRI blood oxygen level-dependent signal. We identify two diametrically opposed, widely distributed brain networks on the basis of both spontaneous correlations within each network and anticorrelations between networks. One network consists of regions routinely exhibiting task-related activations and the other of regions routinely exhibiting task-related deactivations. This intrinsic organization, featuring the presence of anticorrelated networks in the absence of overt task performance, provides a critical context in which to understand brain function. We suggest that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain.
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Proc Natl Acad Sci U S A 102(27): 9673-9678

The human brain is intrinsically organized into dynamic, anticorrelated functional networks

Departments of Radiology, Neurology, Anatomy and Neurobiology, and Biomedical Engineering, Washington University, St. Louis, MO 63110
To whom correspondence should be addressed. E-mail: ude.ltsuw.gpn@mxof.
Contributed by Marcus E. Raichle, May 19, 2005
Contributed by Marcus E. Raichle, May 19, 2005

Freely available online through the PNAS open access option.

Abstract

During performance of attention-demanding cognitive tasks, certain regions of the brain routinely increase activity, whereas others routinely decrease activity. In this study, we investigate the extent to which this task-related dichotomy is represented intrinsically in the resting human brain through examination of spontaneous fluctuations in the functional MRI blood oxygen level-dependent signal. We identify two diametrically opposed, widely distributed brain networks on the basis of both spontaneous correlations within each network and anticorrelations between networks. One network consists of regions routinely exhibiting task-related activations and the other of regions routinely exhibiting task-related deactivations. This intrinsic organization, featuring the presence of anticorrelated networks in the absence of overt task performance, provides a critical context in which to understand brain function. We suggest that both task-driven neuronal responses and behavior are reflections of this dynamic, ongoing, functional organization of the brain.

Keywords: functional MRI, functional connectivity, spontaneous activity
Abstract

Functional imaging techniques such as positron emission tomography and functional MRI (fMRI) have proven to be valuable tools in the investigation of human brain function. Typically a task or stimulus is presented and changes in brain activity in response to the stimulus are recorded. For example, a flashing checkerboard stimulus is associated with spatially specific activity increases in the visual cortex and an auditory stimulus with increased activity in the auditory cortex.

During performance of attention-demanding cognitive tasks, two opposite types of responses are commonly observed. A specific set of frontal and parietal cortical regions routinely exhibit activity increases (1, 2), whereas a different set of regions, including posterior cingulate, medial and lateral parietal, and medial prefrontal cortex (MPF), routinely exhibit activity decreases (37). As the attentional demand of the task is increased, this dichotomy generally becomes more pronounced; activity in positive regions is further increased (8), whereas activity in negative regions is further decreased (6).

Activity increases in frontal and parietal regions have been associated with top-down modulation of attention and working memory (1, 2, 9), processes commonly recruited by cognitive task paradigms. Activity decreases are generally proportional to task difficulty (6), but may be attenuated by self-referential aspects of a task such as emotion (4, 10, 11) or episodic memory (12) as well as the intrusion of task-independent thoughts (13). Simply stated, the dichotomy observed in response to attention-demanding cognitive tasks involves increased activity in regions whose function supports task execution and decreased activity in regions presumably supporting unrelated or irrelevant processes.

Although the majority of researchers performing functional imaging studies continue to examine changes in brain activity associated with task performance, some now study spontaneous brain activity present in the absence of a task. These resting-state functional connectivity studies examine correlations in slow (<0.1 Hz) spontaneous fluctuations in the blood oxygen level-dependent (BOLD) signal (14). Biswal and colleagues (15) were the first to show that these spontaneous fluctuations were coherent within specific neuro-anatomical systems such as the somatomotor system (15). Their results have been confirmed and extended to several other systems, including visual, auditory, and language processing networks (1519). Important for the present study, correlated fluctuations have been demonstrated between frontal and parietal areas often observed to increase activity during task performance (19, 20) and within the network of regions commonly exhibiting activity decreases during task performance (16, 20, 21).

The collective result of the above studies is that regions similarly modulated by tasks or stimuli tend to exhibit correlated spontaneous fluctuations even in the absence of tasks or stimuli. This result holds true even at different spatial and temporal scales, for example, in orientation columns in the visual cortex (22). An important question is the extent to which task-related functionality is represented intrinsically in the brain. If regions with similar task-related responses are correlated, what is the relationship between regions with dissimilar task-related responses? Specifically, is the task-related dichotomy between regions routinely exhibiting task-positive responses and those routinely exhibiting task-negative responses represented intrinsically in the resting brain? To address this question, we examine both correlations and anticorrelations in spontaneous BOLD fluctuations associated with six predefined regions of interest. Three of these regions are known to routinely exhibit task-positive responses (activations) and three are known to routinely exhibit task-negative responses (deactivations) during attention-demanding tasks (17, 9).

vIPS, ventral intraparietal sulcus; SPreCes, superior precentral sulcus; DLPFC, dorsal lateral prefrontal cortex.

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Acknowledgments

We thank Linda Larson-Prior and John Zempel for help with data acquisition and Mike Posner, Michael Greicius, and Gyorgy Buzsaki for insightful comments and suggestions. This work was supported by National Institutes of Health Grant NS 06833.

Acknowledgments

Notes

Author contributions: M.E.R. designed research; M.D.F. and J.L.V. performed research; M.D.F., A.Z.S., and D.C.V.E. contributed new reagents/analytic tools; M.D.F., A.Z.S., J.L.V., M.C., and M.E.R. analyzed data; and M.D.F. wrote the paper.

Abbreviations: fMRI, functional MRI; BOLD, blood oxygen level-dependent; IPS, intraparietal sulcus; FEF, frontal eye field; MT, middle temporal region; MPF, medial prefrontal cortex; PCC, posterior cingulate/precuneus; LP, lateral parietal cortex; SMA, supplementary motor area.

Notes
Author contributions: M.E.R. designed research; M.D.F. and J.L.V. performed research; M.D.F., A.Z.S., and D.C.V.E. contributed new reagents/analytic tools; M.D.F., A.Z.S., J.L.V., M.C., and M.E.R. analyzed data; and M.D.F. wrote the paper.
Abbreviations: fMRI, functional MRI; BOLD, blood oxygen level-dependent; IPS, intraparietal sulcus; FEF, frontal eye field; MT, middle temporal region; MPF, medial prefrontal cortex; PCC, posterior cingulate/precuneus; LP, lateral parietal cortex; SMA, supplementary motor area.

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