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Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved October 21, 2013 (received for review April 29, 2013)
Significance
Humans have the remarkable ability to flexibly attend to stimuli in the environment and seamlessly shift behaviors, depending on sensory conditions and internal goals. Neuroimaging studies have shown that tasks involving particular cognitive domains consistently recruit specific broadly distributed functional brain networks. A fundamental question in neuroscience is how the brain flexibly manages communication within and between these brain networks, allowing task-relevant regions to interact while minimizing the influence of task-irrelevant activity. In this report we show that low-frequency neuronal oscillations, which reflect fluctuations in neuronal excitability, are modulated selectively within task-relevant, but not -irrelevant brain networks. This modulation of oscillatory activity may coordinate the selective routing of neuronal information within the brain during everyday behavior.
Abstract
Selective attention allows us to filter out irrelevant information in the environment and focus neural resources on information relevant to our current goals. Functional brain-imaging studies have identified networks of broadly distributed brain regions that are recruited during different attention processes; however, the dynamics by which these networks enable selection are not well understood. Here, we first used functional MRI to localize dorsal and ventral attention networks in human epileptic subjects undergoing seizure monitoring. We subsequently recorded cortical physiology using subdural electrocorticography during a spatial-attention task to study network dynamics. Attention networks become selectively phase-modulated at low frequencies (δ, θ) during the same task epochs in which they are recruited in functional MRI. This mechanism may alter the excitability of task-relevant regions or their effective connectivity. Furthermore, different attention processes (holding vs. shifting attention) are associated with synchrony at different frequencies, which may minimize unnecessary cross-talk between separate neuronal processes.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: adaitch{at}wustl.edu.
↵2E.C.L. and M.C. contributed equally to this work.
Author contributions: A.L.D., G.L.S., E.C.L., and M.C. designed research; A.L.D., M.S., J.L.R., S.V.A., D.T.B., and C.M.G. performed research; A.L.D. and A.Z.S. contributed new reagents/analytic tools; A.L.D. analyzed data; and A.L.D., G.L.S., E.C.L., and M.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1307947110/-/DCSupplemental.
- Amy L. Daitcha,1,
- Mohit Sharmaa,
- Jarod L. Rolandb,
- Serguei V. Astafievc,
- David T. Bundya,
- Charles M. Gaonaa,
- Abraham Z. Snyderc,d,
- Gordon L. Shulmanc,
- Eric C. Leuthardta,b,2, and
- Maurizio Corbettac,d,e,2
- aDepartment of Biomedical Engineering,
- bDepartment of Neurological Surgery,
- cDepartment of Neurology,
- dDepartment of Radiology, and
- eDepartment of Anatomy and Neurobiology, Washington University in St. Louis, St. Louis, MO 63110
Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved October 21, 2013 (received for review April 29, 2013)
Significance
Humans have the remarkable ability to flexibly attend to stimuli in the environment and seamlessly shift behaviors, depending on sensory conditions and internal goals. Neuroimaging studies have shown that tasks involving particular cognitive domains consistently recruit specific broadly distributed functional brain networks. A fundamental question in neuroscience is how the brain flexibly manages communication within and between these brain networks, allowing task-relevant regions to interact while minimizing the influence of task-irrelevant activity. In this report we show that low-frequency neuronal oscillations, which reflect fluctuations in neuronal excitability, are modulated selectively within task-relevant, but not -irrelevant brain networks. This modulation of oscillatory activity may coordinate the selective routing of neuronal information within the brain during everyday behavior.
Abstract
Selective attention allows us to filter out irrelevant information in the environment and focus neural resources on information relevant to our current goals. Functional brain-imaging studies have identified networks of broadly distributed brain regions that are recruited during different attention processes; however, the dynamics by which these networks enable selection are not well understood. Here, we first used functional MRI to localize dorsal and ventral attention networks in human epileptic subjects undergoing seizure monitoring. We subsequently recorded cortical physiology using subdural electrocorticography during a spatial-attention task to study network dynamics. Attention networks become selectively phase-modulated at low frequencies (δ, θ) during the same task epochs in which they are recruited in functional MRI. This mechanism may alter the excitability of task-relevant regions or their effective connectivity. Furthermore, different attention processes (holding vs. shifting attention) are associated with synchrony at different frequencies, which may minimize unnecessary cross-talk between separate neuronal processes.
Footnotes
- ↵1To whom correspondence should be addressed. E-mail: adaitch{at}wustl.edu.
↵2E.C.L. and M.C. contributed equally to this work.
Author contributions: A.L.D., G.L.S., E.C.L., and M.C. designed research; A.L.D., M.S., J.L.R., S.V.A., D.T.B., and C.M.G. performed research; A.L.D. and A.Z.S. contributed new reagents/analytic tools; A.L.D. analyzed data; and A.L.D., G.L.S., E.C.L., and M.C. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1307947110/-/DCSupplemental.
Low-frequency oscillations link attention networks
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