Propagating Neocortical Gamma Bursts Are Coordinated by Traveling Alpha Waves

Bahramisharif, Ali; Gerven, Marcel A. J. van; Aarnoutse, Erik J.; Mercier, Manuel; Schwartz, Theodore H.; Foxe, John J.; Ramsey, Nick F.; Jensen, Ole

doi:10.1523/jneurosci.2455-13.2013

Cited by 155 publications

(160 citation statements)

References 41 publications

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“…Our analysis of phase shifts and Granger causality between V1 and V4 confirmed the propagation of α-waves in the feedback direction, in accordance with some (48,63) but not all (64) previous EEG-recordings in humans. At first sight, this result appears to contradict a recent finding that Granger causality between V1 and V2 in the α-range is strongest in the feedforward direction (18).…”

Section: Discussionsupporting

confidence: 90%

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Kerkoerle

Self

Dagnino

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

871

138

776

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This Feature Article is part of a series identified by the Editorial Board as reporting findings of exceptional significance.Edited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved August 8, 2014 (received for review February 22, 2014) Cognitive functions rely on the coordinated activity of neurons in many brain regions, but the interactions between cortical areas are not yet well understood. Here we investigated whether lowfrequency (α) and high-frequency (γ) oscillations characterize different directions of information flow in monkey visual cortex. We recorded from all layers of the primary visual cortex (V1) and found that γ-waves are initiated in input layer 4 and propagate to the deep and superficial layers of cortex, whereas α-waves propagate in the opposite direction. Simultaneous recordings from V1 and downstream area V4 confirmed that γ-and α-waves propagate in the feedforward and feedback direction, respectively. Microstimulation in V1 elicited γ-oscillations in V4, whereas microstimulation in V4 elicited α-oscillations in V1, thus providing causal evidence for the opposite propagation of these rhythms. Furthermore, blocking NMDA receptors, thought to be involved in feedback processing, suppressed α while boosting γ. These results provide new insights into the relation between brain rhythms and cognition.neuronal synchronization | attention | perceptual organization | phase coherence | Granger causality A reas of the visual cortex are arranged hierarchically, with low-level areas representing simple features and higher areas representing the more complex aspects of the visual world (1, 2). Neurons in many visual areas are coactive during the perception of a visual stimulus and it is difficult to disentangle the influences of lower areas onto higher areas from the effects that go in the opposite direction (3). Studies of visual cognition could benefit enormously from markers of cortical activity that distinguish between feedforward and feedback effects. One such putative marker is cortical oscillatory activity, because oscillations of different frequencies have been proposed to propagate either in feedforward or in the feedback direction (4, 5), but experimental evidence for this view is sparse (6).Low-frequency rhythms, like the α-rhythm-which is particularly pronounced in the visual cortex-have been proposed to characterize spontaneous activity (7,8) as the α-rhythm increases when the subject closes the eyes (9). More recent observations have also implicated α-oscillations in the active suppression of irrelevant, unattended information (10, 11). In contrast, the high-frequency γ-rhythm increases if visual stimuli are presented, and in particular if they are task-relevant (12, 13). One influential hypothesis has been that γ-oscillations play a role in feature binding (14), but later studies cast doubt on this proposal (15,16). A more recent hypothesis holds that γ-oscillations facilitate the communication between cortical areas (17), but both evidence in fa...

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Section: Discussionsupporting

confidence: 90%

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Kerkoerle

Self

Dagnino

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

871

138

776

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“…To date, phase-relation diversity has been demonstrated almost exclusively for low-frequency theta (Agarwal et al 2014;Lubenov and Siapas 2009;van der Meij et al 2012) and alpha (Bahramisharif et al 2013;Hindriks et al 2014;Hughes 1995;Nunez 2000) oscillations that occur in the absence of (controlled) stimulation. Here we show that this diversity is also prominent for high-frequency gamma oscillations during sustained visual stimulation (see also Maris et al 2013).…”

Section: Discussionmentioning

confidence: 99%

“…However, to date, the demonstration of such diversity has been largely restricted to low-frequency oscillations that are prominent in the absence of sensory processing (e.g., Agarwal et al 2014;Bahramisharif et al 2013;Hindriks et al 2014;Hughes 1995;Nunez 2000;Lubenov and Siapas 2009;van der Meij et al 2012). In fact, in a prominent review article on the subject, a central claim is that this type of diversity is "typically present during periods outside of stimulation, while synchronous activity dominates in the presence of a strong stimulus" (Ermentrout and Kleinfeld 2001).…”

mentioning

confidence: 99%

Both ongoing alpha and visually induced gamma oscillations show reliable diversity in their across-site phase-relations

Ede

Pelt

Maris

2015

Journal of Neurophysiology

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van Ede F, van Pelt S, Fries P, Maris E. Both ongoing alpha and visually induced gamma oscillations show reliable diversity in their across-site phase-relations. J Neurophysiol 113: 1556 -1563, 2015. First published December 10, 2014 doi:10.1152/jn.00788.2014.-Neural oscillations have emerged as one of the major electrophysiological phenomena investigated in cognitive and systems neuroscience. These oscillations are typically studied with regard to their amplitude, phase, and/or phase coupling. Here we demonstrate the existence of another property that is intrinsic to neural oscillations but has hitherto remained largely unexplored in cognitive and systems neuroscience. This pertains to the notion that these oscillations show reliable diversity in their phase-relations between neighboring recording sites (phase-relation diversity). In contrast to most previous work, we demonstrate that this diversity is restricted neither to low-frequency oscillations nor to periods outside of sensory stimulation. On the basis of magnetoencephalographic (MEG) recordings in humans, we show that this diversity is prominent not only for ongoing alpha oscillations (8 -12 Hz) but also for gamma oscillations (50 -70 Hz) that are induced by sustained visual stimulation. We further show that this diversity provides a dimension within electrophysiological data that, provided a sufficiently high signal-to-noise ratio, does not covary with changes in amplitude. These observations place phase-relation diversity on the map as a prominent and general property of neural oscillations that, moreover, can be studied with noninvasive methods in healthy human volunteers. This opens important new avenues for investigating how neural oscillations contribute to the neural implementation of cognition and behavior. gamma oscillations; human; magnetoencephalography; neural oscillations; phase-relation OVER THE PAST 20 YEARS, neural oscillations have come to the foreground in the scientific study of the neural implementation of cognition and behavior. Indeed, these oscillations have now been implicated in a multitude of neural and cognitive computations (as reviewed in, e.g., Buzsáki and Draguhn 2004;Fries 2005;Hari and Salmelin 1997;Jensen et al. 2007).To date, most studies have investigated neural oscillations with regard to one or more of the following three properties: amplitude, phase, and/or phase coupling (such as between two distant sources or between field oscillations and action potentials). In this report, we demonstrate the existence of a fourth property that is intrinsic to oscillatory neural activity. This property pertains to the observation that the phase-relations between oscillations recorded at neighboring sites are highly and reliably diverse. We term this property phase-relation diversity.Several previous studied have already alluded to the notion of phase-relation diversity in the context of "traveling waves," and recent studies have pointed to important computational roles for such diversity (Agarwal et al. 2014;Lubenov and Siapas ...

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“…As previously described (see Chapter 4a), we re-referenced our data to an average reference of all hippocampal contacts, similar to other studies (Alexander, Jurica, Trengove, & Nikolaev, 2013;Bahramisharif et al, 2013;Massimini, Huber, Ferrarelli, & Hill, 2004;Meij, Kahana, & Maris, 2012;Munck, Goncalves, Huijboom, & Kuijer, 2007;Patten, Rennie, Robinson, & Gong, 2012;Zhang & Jacobs, 2015). One of the reasons for this is to have a reasonable amount of contacts along an axis.…”

Section: Methodsmentioning

confidence: 72%

“…There is also evidence showing bursts of gamma activity propagating over neocortex. These propagating gamma bursts are locked to the phase of traveling alpha waves, suggesting that alpha oscillations serve to coordinate gamma activity not only in time, but also in space (Bahramisharif et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Mechanisms underlying memory enhancement in humans

Granados¹,

Mar²

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Propagating Neocortical Gamma Bursts Are Coordinated by Traveling Alpha Waves

Cited by 155 publications

References 41 publications

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Both ongoing alpha and visually induced gamma oscillations show reliable diversity in their across-site phase-relations

Mechanisms underlying memory enhancement in humans

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