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      A theta rhythm in macaque visual cortex and its attentional modulation

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          Significance

          Theta rhythms, ≈3–8 Hz, have been found in many different parts of the brain. They are predominant in the rodent hippocampus, yet have also been described in the neocortex, primarily in frontal and parietal areas in relation to executive functions. Here, we show a ≈4-Hz theta rhythm in awake macaque monkey area V4 and primary visual cortex. This theta rhythm was spatially coextensive with visually induced gamma-band activity, and gamma power was modulated by theta phase. The strength of theta and of theta-rhythmic gamma modulation was markedly reduced by selective attention. Theta rhythmicity has been observed in microsaccade sequences, and microsaccades influence early visual activity. Yet, removing (the effects of) microsaccades did not influence the results.

          Abstract

          Theta rhythms govern rodent sniffing and whisking, and human language processing. Human psychophysics suggests a role for theta also in visual attention. However, little is known about theta in visual areas and its attentional modulation. We used electrocorticography (ECoG) to record local field potentials (LFPs) simultaneously from areas V1, V2, V4, and TEO of two macaque monkeys performing a selective visual attention task. We found a ≈4-Hz theta rhythm within both the V1–V2 and the V4–TEO region, and theta synchronization between them, with a predominantly feedforward directed influence. ECoG coverage of large parts of these regions revealed a surprising spatial correspondence between theta and visually induced gamma. Furthermore, gamma power was modulated with theta phase. Selective attention to the respective visual stimulus strongly reduced these theta-rhythmic processes, leading to an unusually strong attention effect for V1. Microsaccades (MSs) were partly locked to theta. However, neuronal theta rhythms tended to be even more pronounced for epochs devoid of MSs. Thus, we find an MS-independent theta rhythm specific to visually driven parts of V1–V2, which rhythmically modulates local gamma and entrains V4–TEO, and which is strongly reduced by attention. We propose that the less theta-rhythmic and thereby more continuous processing of the attended stimulus serves the exploitation of this behaviorally most relevant information. The theta-rhythmic and thereby intermittent processing of the unattended stimulus likely reflects the ecologically important exploration of less relevant sources of information.

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          Most cited references49

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          Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization.

          Cortical activity and perception are not driven by the external stimulus alone; rather sensory information has to be integrated with various other internal constraints such as expectations, recent memories, planned actions, etc. The question is how large scale integration over many remote and size-varying processes might be performed by the brain. We have conducted a series of EEG recordings during processes thought to involve neuronal assemblies of varying complexity. While local synchronization during visual processing evolved in the gamma frequency range, synchronization between neighboring temporal and parietal cortex during multimodal semantic processing evolved in a lower, the beta1 (12-18 Hz) frequency range, and long range fronto-parietal interactions during working memory retention and mental imagery evolved in the theta and alpha (4-8 Hz, 8-12 Hz) frequency range. Thus, a relationship seems to exist between the extent of functional integration and the synchronization-frequency. In particular, long-range interactions in the alpha and theta ranges seem specifically involved in processing of internal mental context, i.e. for top-down processing. We propose that large scale integration is performed by synchronization among neurons and neuronal assemblies evolving in different frequency ranges.
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            Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex.

            How natural speech is represented in the auditory cortex constitutes a major challenge for cognitive neuroscience. Although many single-unit and neuroimaging studies have yielded valuable insights about the processing of speech and matched complex sounds, the mechanisms underlying the analysis of speech dynamics in human auditory cortex remain largely unknown. Here, we show that the phase pattern of theta band (4-8 Hz) responses recorded from human auditory cortex with magnetoencephalography (MEG) reliably tracks and discriminates spoken sentences and that this discrimination ability is correlated with speech intelligibility. The findings suggest that an approximately 200 ms temporal window (period of theta oscillation) segments the incoming speech signal, resetting and sliding to track speech dynamics. This hypothesized mechanism for cortical speech analysis is based on the stimulus-induced modulation of inherent cortical rhythms and provides further evidence implicating the syllable as a computational primitive for the representation of spoken language.
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              Cross-frequency coupling supports multi-item working memory in the human hippocampus.

              Recent findings indicate that the hippocampus supports not only long-term memory encoding but also plays a role in working memory (WM) maintenance of multiple items; however, the neural mechanism underlying multi-item maintenance is still unclear. Theoretical work suggests that multiple items are being maintained by neural assemblies synchronized in the gamma frequency range (25-100 Hz) that are locked to consecutive phase ranges of oscillatory activity in the theta frequency range (4-8 Hz). Indeed, cross-frequency coupling of the amplitude of high-frequency activity to the phase of slower oscillations has been described both in animals and in humans, but has never been linked to a theoretical model of a cognitive process. Here we used intracranial EEG recordings in human epilepsy patients to test pivotal predictions from theoretical work. First, we show that simultaneous maintenance of multiple items in WM is accompanied by cross-frequency coupling of oscillatory activity in the hippocampus, which is recruited during multi-item WM. Second, maintenance of an increasing number of items is associated with modulation of beta/gamma amplitude with theta band activity of lower frequency, consistent with the idea that longer cycles are required for an increased number of representations by gamma cycles. This effect cannot be explained by a difference in theta or beta/gamma power. Third, we describe how the precision of cross-frequency coupling predicts individual WM performance. These data support the idea that working memory in humans depends on a neural code using phase information.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                12 June 2018
                30 May 2018
                30 May 2018
                : 115
                : 24
                : E5614-E5623
                Affiliations
                [1] aErnst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society , 60528 Frankfurt, Germany;
                [2] bDonders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen , 6525 EN Nijmegen, The Netherlands;
                [3] cSwammerdam Institute for Life Sciences, Center for Neuroscience, Faculty of Science, University of Amsterdam , 1098 XH Amsterdam, The Netherlands
                Author notes
                1To whom correspondence should be addressed. Email: pascal.fries@ 123456esi-frankfurt.de .

                Edited by Nancy Kopell, Boston University, Boston, MA, and approved May 8, 2018 (received for review November 8, 2017)

                Author contributions: G.S., C.A.B., and P.F. designed research; G.S., C.A.B., and P.F. performed research; G.S. and P.F. analyzed data; and G.S. and P.F. wrote the paper.

                Author information
                http://orcid.org/0000-0003-2433-6126
                Article
                201719433
                10.1073/pnas.1719433115
                6004461
                29848632
                53194192-cf64-4762-9aa8-0b76ad877947
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: SPP 1665
                Award Recipient : Pascal Fries
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: FOR 1847
                Award Recipient : Pascal Fries
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: FR2557/5-1-CORNET
                Award Recipient : Pascal Fries
                Categories
                PNAS Plus
                Biological Sciences
                Neuroscience
                PNAS Plus

                theta,gamma,phase-amplitude coupling,visual cortex,attention

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