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      Single neurons may encode simultaneous stimuli by switching between activity patterns

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          Abstract

          How the brain preserves information about multiple simultaneous items is poorly understood. We report that single neurons can represent multiple stimuli by interleaving signals across time. We record single units in an auditory region, the inferior colliculus, while monkeys localize 1 or 2 simultaneous sounds. During dual-sound trials, we find that some neurons fluctuate between firing rates observed for each single sound, either on a whole-trial or on a sub-trial timescale. These fluctuations are correlated in pairs of neurons, can be predicted by the state of local field potentials prior to sound onset, and, in one monkey, can predict which sound will be reported first. We find corroborating evidence of fluctuating activity patterns in a separate dataset involving responses of inferotemporal cortex neurons to multiple visual stimuli. Alternation between activity patterns corresponding to each of multiple items may therefore be a general strategy to enhance the brain processing capacity, potentially linking such disparate phenomena as variable neural firing, neural oscillations, and limits in attentional/memory capacity.

          Abstract

          The neural mechanisms through which neurons represent simultaneously presented stimuli are not well understood. Here the authors demonstrate that the two stimuli are alternately encoded through fluctuations in the activity patterns of single neurons.

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          Most cited references68

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          Grounded cognition.

          Grounded cognition rejects traditional views that cognition is computation on amodal symbols in a modular system, independent of the brain's modal systems for perception, action, and introspection. Instead, grounded cognition proposes that modal simulations, bodily states, and situated action underlie cognition. Accumulating behavioral and neural evidence supporting this view is reviewed from research on perception, memory, knowledge, language, thought, social cognition, and development. Theories of grounded cognition are also reviewed, as are origins of the area and common misperceptions of it. Theoretical, empirical, and methodological issues are raised whose future treatment is likely to affect the growth and impact of grounded cognition.
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            The θ-γ neural code.

            Theta and gamma frequency oscillations occur in the same brain regions and interact with each other, a process called cross-frequency coupling. Here, we review evidence for the following hypothesis: that the dual oscillations form a code for representing multiple items in an ordered way. This form of coding has been most clearly demonstrated in the hippocampus, where different spatial information is represented in different gamma subcycles of a theta cycle. Other experiments have tested the functional importance of oscillations and their coupling. These involve correlation of oscillatory properties with memory states, correlation with memory performance, and effects of disrupting oscillations on memory. Recent work suggests that this coding scheme coordinates communication between brain regions and is involved in sensory as well as memory processes. Copyright © 2013 Elsevier Inc. All rights reserved.
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              The phase of ongoing EEG oscillations predicts visual perception.

              Oscillations are ubiquitous in electrical recordings of brain activity. While the amplitude of ongoing oscillatory activity is known to correlate with various aspects of perception, the influence of oscillatory phase on perception remains unknown. In particular, since phase varies on a much faster timescale than the more sluggish amplitude fluctuations, phase effects could reveal the fine-grained neural mechanisms underlying perception. We presented brief flashes of light at the individual luminance threshold while EEG was recorded. Although the stimulus on each trial was identical, subjects detected approximately half of the flashes (hits) and entirely missed the other half (misses). Phase distributions across trials were compared between hits and misses. We found that shortly before stimulus onset, each of the two distributions exhibited significant phase concentration, but at different phase angles. This effect was strongest in the theta and alpha frequency bands. In this time-frequency range, oscillatory phase accounted for at least 16% of variability in detection performance and allowed the prediction of performance on the single-trial level. This finding indicates that the visual detection threshold fluctuates over time along with the phase of ongoing EEG activity. The results support the notion that ongoing oscillations shape our perception, possibly by providing a temporal reference frame for neural codes that rely on precise spike timing.
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                Author and article information

                Contributors
                v.caruso@duke.edu
                surya.tokdar@duke.edu
                jmgroh@duke.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                13 July 2018
                13 July 2018
                2018
                : 9
                : 2715
                Affiliations
                [1 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Duke Institute for Brain Sciences, , Duke University, ; Durham, NC 27708 USA
                [2 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Center for Cognitive Neuroscience, , Duke University, ; Durham NC, 27708, USA
                [3 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Department of Psychology and Neuroscience, , Duke University, ; Durham NC, 27708, USA
                [4 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Department of Neurobiology, , Duke University, ; Durham NC, 27708, USA
                [5 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Department of Statistical Science, , Duke University, ; Durham NC, 27708, USA
                [6 ]ISNI 0000 0001 2166 1519, GRID grid.134907.8, The Rockefeller University, New York, ; New York NY, 10065, USA
                [7 ]ISNI 0000 0004 1936 7961, GRID grid.26009.3d, Department of Computer Science, , Duke University, ; Durham NC, 27708, USA
                [8 ]ISNI 0000 0004 1936 7400, GRID grid.256304.6, Department of Computer Science, , Georgia State University, ; Atlanta, GA 30302 USA
                [9 ]ISNI 0000 0001 2192 7145, GRID grid.167436.1, Department of Decision Sciences, , University of New Hampshire, ; Durham NH, 03824, USA
                [10 ]ISNI 0000 0001 2179 1970, GRID grid.21006.35, Department of Psychology, , University of Canterbury, ; Riccarton, Christchurch 8041, New Zealand
                [11 ]ISNI 000000041936754X, GRID grid.38142.3c, Present Address: Department of Statistics, , Harvard University, ; Cambridge MA, 02138, USA
                Author information
                http://orcid.org/0000-0002-3895-1296
                http://orcid.org/0000-0001-7415-9223
                http://orcid.org/0000-0002-1421-147X
                http://orcid.org/0000-0003-3270-374X
                http://orcid.org/0000-0001-8402-3522
                http://orcid.org/0000-0001-6192-757X
                Article
                5121
                10.1038/s41467-018-05121-8
                6045601
                30006598
                fa1f0e2d-a19a-4a1f-baf0-d73e823d3d63
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 12 September 2017
                : 11 June 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000001, National Science Foundation (NSF);
                Award ID: 0924750
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000009, Foundation for the National Institutes of Health (Foundation for the National Institutes of Health, Inc.);
                Award ID: 5R01DC013906- 02
                Award Recipient :
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