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Global dynamics of selective attention and its lapses in primary auditory cortex

Nature Neuroscience volume 19, pages 1707–1717 (2016)Cite this article

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Abstract

Previous research demonstrated that while selectively attending to relevant aspects of the external world, the brain extracts pertinent information by aligning its neuronal oscillations to key time points of stimuli or their sampling by sensory organs. This alignment mechanism is termed oscillatory entrainment. We investigated the global, long-timescale dynamics of this mechanism in the primary auditory cortex of nonhuman primates, and hypothesized that lapses of entrainment would correspond to lapses of attention. By examining electrophysiological and behavioral measures, we observed that besides the lack of entrainment by external stimuli, attentional lapses were also characterized by high-amplitude alpha oscillations, with alpha frequency structuring of neuronal ensemble and single-unit operations. Entrainment and alpha-oscillation-dominated periods were strongly anticorrelated and fluctuated rhythmically at an ultra-slow rate. Our results indicate that these two distinct brain states represent externally versus internally oriented computational resources engaged by large-scale task-positive and task-negative functional networks.

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Figure 1: Intermodal selective attention task.
Figure 2: Recording technique and ITC.
Figure 3: Long-timescale dynamics of oscillatory entrainment during a continuous selective intermodal attention task.
Figure 4: Slow counterphase fluctuation of delta oscillatory entrainment and alpha amplitude.
Figure 5: Entrainment-correlated patterns of cross-frequency coupling.
Figure 6: Distinct brain-state-dependent patterns of single-unit activity.
Figure 7: Entrainment-correlated changes in laminar delta and alpha coherence.

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Acknowledgements

Support for this work was provided by NIH grant R01DC012947 from the NIDCD (P.L.) and R01MH109289 from the NIMH (D.C.J.).

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Authors and Affiliations

  1. Cognitive Neuroscience and Schizophrenia Program, Nathan Kline Institute, Orangeburg, New York, USA

    Peter Lakatos, Annamaria Barczak, Tammy McGinnis, Deborah Ross, Daniel C Javitt & Monica Noelle O'Connell

  2. Department of Psychiatry, New York University School of Medicine, New York, New York, USA

    Peter Lakatos

  3. Department of Physiology & Pharmacology, SUNY Downstate Medical Center, Brooklyn, New York, USA

    Samuel A Neymotin

  4. Department of Neuroscience, Yale University School of Medicine, New Haven, Connecticut, USA

    Samuel A Neymotin

  5. Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, New York, USA

    Daniel C Javitt

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Contributions

P.L. and M.N.O. designed the study. M.N.O., T.M. and D.R. performed the experiments. P.L. and D.C.J. designed the analyses. P.L., M.N.O., A.B. and S.A.N. performed the analyses. P.L. wrote the manuscript with input from all authors.

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Correspondence to Peter Lakatos.

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Lakatos, P., Barczak, A., Neymotin, S. et al. Global dynamics of selective attention and its lapses in primary auditory cortex. Nat Neurosci 19, 1707–1717 (2016). https://doi.org/10.1038/nn.4386

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