The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave

Muller, Lyle; Reynaud, Alexandre; Chavane, Frédéric; Destexhe, Alain

doi:10.1038/ncomms4675

Cited by 208 publications

(287 citation statements)

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“…Dominant directionality could be related to the underlying connectivity profile that serves the intra-and intercortical information transfer (57). The computational implication of horizontal connections could point to a preset preferred path for information processing within a given functional domain of the neocortex (60)(61)(62). That such a directional path is "functionally" preserved in sleep could be further evidence that corticothalamic UP states replay fragments of wakefulness (63).…”

Section: Discussionmentioning

confidence: 99%

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Quyen

Muller

Teleńczuk

et al. 2016

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

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Beta (β)-and gamma (γ)-oscillations are present in different cortical areas and are thought to be inhibition-driven, but it is not known if these properties also apply to γ-oscillations in humans. Here, we analyze such oscillations in high-density microelectrode array recordings in human and monkey during the wake-sleep cycle. In these recordings, units were classified as excitatory and inhibitory cells. We find that γ-oscillations in human and β-oscillations in monkey are characterized by a strong implication of inhibitory neurons, both in terms of their firing rate and their phasic firing with the oscillation cycle. The β-and γ-waves systematically propagate across the array, with similar velocities, during both wake and sleep. However, only in slow-wave sleep (SWS) β-and γ-oscillations are associated with highly coherent and functional interactions across several millimeters of the neocortex. This interaction is specifically pronounced between inhibitory cells. These results suggest that inhibitory cells are dominantly involved in the genesis of β-and γ-oscillations, as well as in the organization of their large-scale coherence in the awake and sleeping brain. The highest oscillation coherence found during SWS suggests that fast oscillations implement a highly coherent reactivation of wake patterns that may support memory consolidation during SWS.excitation | inhibition | state-dependent firing | wave propagation | synchrony N eocortical beta (β)-and gamma (γ)-oscillations have been largely studied in the context of action/cognition during wakefulness (1-3). Although numerous studies have focused intensely on the information-processing role of β and γ during wakefulness, these rhythms do also occur during deep anesthesia and natural sleep (4-6). Additionally, although very-high-frequency allocortical oscillations (e.g., ripples at 80-200 Hz and fast ripples at 200-500 Hz in rodent/human hippocampus) have been thoroughly implicated in sleep-dependent memory consolidation (ref. 7 and reviewed in refs. 8 and 9), the occurrence and role of neocortical β-and γ-oscillations during sleep remain largely unexplored and related studies have been limited to macroscopic (whole-brain) scales (e.g., ref. 10). A recent study using microwires and intracranial electroencephalography (iEEG) recordings in the neocortex of epileptics has verified the strong presence of γ-oscillations during slow-wave sleep (SWS) (11). That study also showed a marked increase of spiking during γ, a suggestive indicator of association with cortical UP states. Here, we evaluate the presence of neocortical β-and γ-oscillations during the wake-sleep cycle at the level of local circuitry using dense 2D multielectrode recordings with identified excitatory and inhibitory cells (12, 13).Experimental and theoretical studies suggest that thalamocortical oscillations (including β and γ) are generated through a combination of intrinsic mechanisms involving the interplay between different ionic currents and extrinsic interaction of inhibitory and excitatory c...

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Section: Discussionmentioning

confidence: 99%

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Quyen

Muller

Teleńczuk

et al. 2016

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

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“…To study spatiotemporal dynamics in these neural recordings, we adapted our previously introduced method for detecting arbitrarily shaped traveling waves (Muller et al, 2014) to multisite ECoG arrays (Figure 1-figure supplements 2 and 3). This approach allowed us to characterize and classify the spatiotemporal dynamics during thousands of episodes of spindling activity in many hours of sleep recordings.…”

Section: Spatiotemporal Dynamicsmentioning

confidence: 99%

“…For the spatial gradient, derivatives are taken across the two dimensions of space and are approximated by the appropriate forward and centered finite differences. As in previous work, phase derivatives were implemented as multiplications in the complex plane (Feldman, 2011;Muller et al, 2014).…”

Section: Spatiotemporal Dynamicsmentioning

confidence: 99%

“…We study intracranial electrocorticogram (ECoG) recordings of five clinical patients in stage 2 sleep and apply recently developed computational methods (Muller et al, 2014) to classify spatiotemporal dynamics at the level of individual oscillation cycles. ECoG arrays were implanted in subjects undergoing evaluation for resective surgery of epileptogenic cortex ( Figure 1A, left).…”

Section: Introductionmentioning

confidence: 99%

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Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night

Muller

Piantoni

Koller

et al. 2016

eLife

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During sleep, the thalamus generates a characteristic pattern of transient, 11-15 Hz sleep spindle oscillations, which synchronize the cortex through large-scale thalamocortical loops. Spindles have been increasingly demonstrated to be critical for sleep-dependent consolidation of memory, but the specific neural mechanism for this process remains unclear. We show here that cortical spindles are spatiotemporally organized into circular wave-like patterns, organizing neuronal activity over tens of milliseconds, within the timescale for storing memories in large-scale networks across the cortex via spike-time dependent plasticity. These circular patterns repeat over hours of sleep with millisecond temporal precision, allowing reinforcement of the activity patterns through hundreds of reverberations. These results provide a novel mechanistic account for how global sleep oscillations and synaptic plasticity could strengthen networks distributed across the cortex to store coherent and integrated memories.

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“…Indeed, propagation of activity across visual brain areas has been demonstrated previously in MEG (Cottereau et al 2011) and may also contribute to the diversity observed here. A recent study in monkeys even points to the possibility that both scenarios take place in concert, whereby activity travels within different visual areas while maintaining stable phase delays between visual areas (Muller et al 2014).…”

Section: Discussionmentioning

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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The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave

Cited by 208 publications

References 68 publications

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

High-frequency oscillations in human and monkey neocortex during the wake–sleep cycle

Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night

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

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