The visual cortex produces gamma band echo in response to broadband visual flicker

The aim of this study is to uncover the network dynamics of the human visual cortex by driving it with a broadband random visual flicker. We here applied a broadband flicker (1–720 Hz) while measuring the MEG and then estimated the temporal response function (TRF) between the visual input and the MEG response. This TRF revealed an early response in the 40–60 Hz gamma range as well as in the 8–12 Hz alpha band. While the gamma band response is novel, the latter has been termed the alpha band perceptual echo. The gamma echo preceded the alpha perceptual echo. The dominant frequency of the gamma echo was subject-specific thereby reflecting the individual dynamical properties of the early visual cortex. To understand the neuronal mechanisms generating the gamma echo, we implemented a pyramidal-interneuron gamma (PING) model that produces gamma oscillations in the presence of constant input currents. Applying a broadband input current mimicking the visual stimulation allowed us to estimate TRF between the input current and the population response (akin to the local field potentials). The TRF revealed a gamma echo that was similar to the one we observed in the MEG data. Our results suggest that the visual gamma echo can be explained by the dynamics of the PING model even in the absence of sustained gamma oscillations.

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The visual cortex produces a signal in the gamma band in response to broadband visual flicker

10.1101/2021.01.11.426257 ◽

2021 ◽

Author(s):

Alexander Zhigalov ◽

Katharina Duecker ◽

Ole Jensen

Keyword(s):

Visual Cortex ◽

Visual Stimulation ◽

Gamma Oscillations ◽

Early Response ◽

Dominant Frequency ◽

Gamma Band ◽

Input Current ◽

Alpha Band ◽

Constant Input ◽

Gamma Range

AbstractThe aim of this study is to uncover the network dynamics of the human visual cortex by driving it with a broadband random visual flicker. We here applied a broadband flicker (1–720 Hz) while measuring the MEG and then estimated the temporal response function (TRF) between the visual input and the MEG response. This TRF revealed an early response in the 40–60 Hz gamma range as well as in the 8–12 Hz alpha band. While the gamma band response is novel, the latter has been termed the alpha band perceptual echo. The gamma echo preceded the alpha perceptual echo. The dominant frequency of the gamma echo was subject-specific thereby reflecting the individual dynamical properties of the early visual cortex. To understand the neuronal mechanisms generating the gamma echo, we implemented a pyramidal-interneuron gamma (PING) model that produces gamma oscillations in the presence of constant input currents. Applying a broadband input current mimicking the visual stimulation allowed us to estimate TRF between the input current and the population response (akin to the local field potentials). The TRF revealed a gamma echo that was similar to the one we observed in the MEG data. Our results suggest that the visual gamma echo can be explained by the dynamics of the PING model even in the absence of sustained gamma oscillations.

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A neural circuit for gamma-band coherence across the retinotopic map in mouse visual cortex

eLife ◽

10.7554/elife.28569 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 13

Author(s):

Richard Hakim ◽

Kiarash Shamardani ◽

Hillel Adesnik

Keyword(s):

Visual Cortex ◽

Neural Circuit ◽

Brain Slices ◽

Pyramidal Cells ◽

Gamma Oscillations ◽

Gamma Band ◽

Neuron Activity ◽

Mouse Visual Cortex ◽

Retinotopic Map

Cortical gamma oscillations have been implicated in a variety of cognitive, behavioral, and circuit-level phenomena. However, the circuit mechanisms of gamma-band generation and synchronization across cortical space remain uncertain. Using optogenetic patterned illumination in acute brain slices of mouse visual cortex, we define a circuit composed of layer 2/3 (L2/3) pyramidal cells and somatostatin (SOM) interneurons that phase-locks ensembles across the retinotopic map. The network oscillations generated here emerge from non-periodic stimuli, and are stimulus size-dependent, coherent across cortical space, narrow band (30 Hz), and depend on SOM neuron but not parvalbumin (PV) neuron activity; similar to visually induced gamma oscillations observed in vivo. Gamma oscillations generated in separate cortical locations exhibited high coherence as far apart as 850 μm, and lateral gamma entrainment depended on SOM neuron activity. These data identify a circuit that is sufficient to mediate long-range gamma-band coherence in the primary visual cortex.

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Sensory-driven and spontaneous gamma oscillations engage distinct cortical circuitry

Journal of Neurophysiology ◽

10.1152/jn.00137.2015 ◽

2016 ◽

Vol 115 (4) ◽

pp. 1821-1835 ◽

Cited By ~ 16

Author(s):

Cristin G. Welle ◽

Diego Contreras

Keyword(s):

Visual Cortex ◽

Visual Stimulation ◽

Oscillation Amplitude ◽

Gamma Oscillations ◽

Gamma Oscillation ◽

Inhibitory Neurons ◽

Sensory Representation ◽

Cortical Circuitry ◽

Mouse Visual Cortex

Gamma oscillations are a robust component of sensory responses but are also part of the background spontaneous activity of the brain. To determine whether the properties of gamma oscillations in cortex are specific to their mechanism of generation, we compared in mouse visual cortex in vivo the laminar geometry and single-neuron rhythmicity of oscillations produced during sensory representation with those occurring spontaneously in the absence of stimulation. In mouse visual cortex under anesthesia (isoflurane and xylazine), visual stimulation triggered oscillations mainly between 20 and 50 Hz, which, because of their similar functional significance to gamma oscillations in higher mammals, we define here as gamma range. Sensory representation in visual cortex specifically increased gamma oscillation amplitude in the supragranular (L2/3) and granular (L4) layers and strongly entrained putative excitatory and inhibitory neurons in infragranular layers, while spontaneous gamma oscillations were distributed evenly through the cortical depth and primarily entrained putative inhibitory neurons in the infragranular (L5/6) cortical layers. The difference in laminar distribution of gamma oscillations during the two different conditions may result from differences in the source of excitatory input to the cortex. In addition, modulation of superficial gamma oscillation amplitude did not result in a corresponding change in deep-layer oscillations, suggesting that superficial and deep layers of cortex may utilize independent but related networks for gamma generation. These results demonstrate that stimulus-driven gamma oscillations engage cortical circuitry in a manner distinct from spontaneous oscillations and suggest multiple networks for the generation of gamma oscillations in cortex.

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Visual Grouping and the Focusing of Attention Induce Gamma-band Oscillations at Different Frequencies in Human Magnetoencephalogram Signals

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2006.18.11.1850 ◽

2006 ◽

Vol 18 (11) ◽

pp. 1850-1862 ◽

Cited By ~ 112

Author(s):

Juan R. Vidal ◽

Maximilien Chaumon ◽

J. Kevin O'Regan ◽

Catherine Tallon-Baudry

Keyword(s):

Short Term Memory ◽

Implementation Process ◽

Visual Display ◽

Gamma Oscillations ◽

Gamma Band ◽

Visual Grouping ◽

Gamma Range ◽

High Gamma ◽

The One ◽

Attentional Filter

Neural oscillatory synchrony could implement grouping processes, act as an attentional filter, or foster the storage of information in short-term memory. Do these findings indicate that oscillatory synchrony is an unspecific epiphenomenon occurring in any demanding task, or that oscillatory synchrony is a fundamental mechanism involved whenever neural cooperation is requested? If the latter hypothesis is true, then oscillatory synchrony should be specific, with distinct visual processes eliciting different types of oscillations. We recorded magnetoencephalogram (MEG) signals while manipulating the grouping properties of a visual display on the one hand, and the focusing of attention to memorize part of this display on the other hand. Grouping-related gamma oscillations were present in all conditions but modulated by the grouping properties of the stimulus (one or two groups) in the high gamma-band (70–120 Hz) at central occipital locations. Attention-related gamma oscillations appeared as an additional component whenever attentional focusing was requested in the low gamma-band (44–66 Hz) at parietal locations. Our results thus reveal the existence of a functional specialization in the gamma range, with grouping-related oscillations showing up at higher frequencies than attention-related oscillations. The pattern of oscillatory synchrony is thus specific of the visual process it is associated with. Our results further suggest that both grouping processes and focused attention rely on a common implementation process, namely, gamma-band oscillatory synchrony, a finding that could account for the fact that coherent percepts are more likely to catch attention than incoherent ones.

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Balance between inhibitory cell types is necessary for flexible frequency switching in adult mouse visual cortex

10.1101/2020.01.18.911271 ◽

2020 ◽

Author(s):

Justin W. M. Domhof ◽

Paul H. E. Tiesinga

Keyword(s):

Visual Cortex ◽

Visual Stimulation ◽

Time Window ◽

Pyramidal Cells ◽

Gamma Oscillations ◽

Neuron Network ◽

Beta Oscillations ◽

Frequency Bands ◽

Adult Mice ◽

Gamma Rhythms

Neuronal networks in rodent primary visual cortex (V1) can generate oscillations in different frequency bands depending on the network state and the level of visual stimulation. High-frequency gamma rhythms, for example, dominate the network’s spontaneous activity in adult mice but are attenuated upon visual stimulation, during which the network switches to the beta band instead. The spontaneous LFP of juvenile mouse V1, however, mainly contains beta oscillations and presenting a stimulus does not elicit drastic changes in collective network oscillations. We study, in a spiking neuron network model, the mechanism in adult mice that allows for flexible switches between multiple frequency bands and contrast this to the network structure in juvenile mice that do not posses this flexibility. The model is comprised of excitatory pyramidal cells (PCs) and two types of inhibitory interneurons: the parvalbumin expressing (PV) interneuron, which produces gamma oscillations, and the somatostatin expressing (SOM) cell, which generates beta rhythms. Our model simulations suggest that both of these oscillations are generated by a pyramidal-interneuron gamma (PING) mechanism. Furthermore, prominent gamma and beta oscillations in, respectively, the spontaneous and visually evoked activity of the simulated network only occurred within the same network configuration when there was a balance between both types of interneurons so that SOM neurons are able to shape the dynamics of the pyramidal-PV cell subnetwork without dominating dynamics. Taken together, our results demonstrate that the effective strengths of PV and SOM cells must be balanced for experimentally observed V1 dynamics in adult mice. Moreover, since spontaneous gamma rhythms emerge during the well-known critical period, our findings support the notion that PV cells become integrated in the circuit of this cortical area during this time window and additionally indicate that this integration comprises an overall increase in their synaptic strength.

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No evidence for entrainment: endogenous gamma oscillations and rhythmic flicker responses coexist in visual cortex

10.1101/2020.09.02.279497 ◽

2020 ◽

Author(s):

Katharina Duecker ◽

Tjerk P. Gutteling ◽

Christoph S. Herrmann ◽

Ole Jensen

Keyword(s):

Visual Cortex ◽

Human Brain ◽

Visual Stimulation ◽

Gamma Oscillations ◽

Photic Stimulation ◽

Neuronal Populations ◽

Frequency Entrainment ◽

Flicker Response ◽

Neuronal Processes

AbstractMotivated by the plethora of studies associating gamma oscillations (∼30-100 Hz) with various neuronal processes, including inter-regional communication and neuroprotection, we asked if endogenous gamma oscillations in the human brain can be entrained by rhythmic photic stimulation. The photic drive produced a robust Magnetoencephalography (MEG) response in visual cortex up to frequencies of about 80 Hz. Strong, endogenous gamma oscillations were induced using moving grating stimuli as repeatedly shown in previous research. When superimposing the flicker and the gratings, there was no evidence for phase or frequency entrainment of the endogenous gamma oscillations by the photic drive. Rather – as supported by source modelling – our results show that the flicker response and the endogenous gamma oscillations coexist and are generated by different neuronal populations in visual cortex. Our findings challenge the notion that neuronal entrainment by visual stimulation generalises to cortical gamma oscillations.

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Low-frequency alternating current stimulation rhythmically suppresses stimulus-induced gamma-band oscillations in visual cortex and impairs perceptual performance

10.1101/230656 ◽

2017 ◽

Author(s):

Jim D. Herring ◽

Sophie Esterer ◽

Tom R. Marshall ◽

Ole Jensen ◽

Til O. Bergmann

Keyword(s):

Visual Cortex ◽

Sensory Processing ◽

Cortical Excitability ◽

Low Frequency ◽

Gamma Oscillations ◽

Alternating Current ◽

Gamma Band ◽

Healthy Human ◽

Alpha Oscillations ◽

Retinal Stimulation

AbstractAlpha oscillations (8-12 Hz) are hypothesized to rhythmically gate sensory processing, reflected by activity in the 40-100 Hz gamma band, via the mechanism of pulsed inhibition. We applied transcranial alternating current stimulation (TACS) at individual alpha frequency (IAF) and flanking frequencies (IAF-4 Hz, IAF+4 Hz) to the occipital cortex of healthy human volunteers during concurrent magnetoencephalography (MEG), while participants performed a visual detection task inducing strong gamma-band responses. Occipital (but not frontal) TACS phasically suppressed stimulus-induced gamma oscillations in the visual cortex and impaired target detection, with stronger phase-to-amplitude coupling predicting behavioral impairments. Frontal control TACS ruled out retino-thalamo-cortical entrainment resulting from (subthreshold) retinal stimulation. All TACS frequencies tested were effective, suggesting that visual gamma-band responses can be modulated by a range of low frequency oscillations. We propose that TACS-induced cortical excitability fluctuations mimic the mechanism of pulsed inhibition, which mediates the function of alpha oscillations in gating sensory processing.

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Hippocampal gamma-band oscillopathy in a mouse model of Fragile X Syndrome

10.1101/2021.04.24.441239 ◽

2021 ◽

Author(s):

Evangelia Pollali ◽

Jan-Oliver Hollnagel ◽

Guersel Caliskan

Keyword(s):

Signaling Pathways ◽

Fragile X Syndrome ◽

Metabotropic Glutamate Receptor ◽

Fragile X ◽

Muscarinic Acetylcholine Receptor ◽

Gamma Oscillations ◽

Gamma Band ◽

Gamma Range ◽

Dependent Learning

Fragile X syndrome (FXS) is the most common inherited form of intellectual disability arising from the loss of fragile X mental retardation protein (FMRP), a protein that plays a central role in neuronal function and plasticity. FXS patients show sensory hypersensitivity, hyperarousal and hippocampus-dependent learning deficits that can be recapitulated in the FMR1 KO mice. Enhanced metabotropic glutamate receptor (mGluR) signaling and muscarinic acetylcholine receptor (mAChR) signaling in the FMR1 KO mouse are implicated as the primary causes of the disease pathogenesis. Furthermore, glutamatergic kainate receptor (KAR) function is reduced in the cortex of the FMR1 KO mice. Of note, activation of these signaling pathways leads to slow gamma-range oscillations in the hippocampus in vitro and abnormal gamma oscillations have been reported in FMR1 KO mice and patients with FXS. Thus, we hypothesized that aberrant activation of these receptors leads to the observed gamma oscillopathy. We recorded gamma oscillations induced by either cholinergic agonist carbachol (CCh), mGluR1/5 agonist Dihydroxyphenylglycine (DHPG) or ionotropic glutamatergic agonist KA from the hippocampal CA3 in WT and FMR1 KO mice in vitro. We show a specific increase in the power of DHPG- and CCh-induced gamma oscillations and reduction in the synchronicity of gamma oscillations induced by KA. We further elucidate an aberrant spiking activity during CCh-induced and kainate-induced gamma oscillations which may underlie the altered gamma oscillation synchronization in the FMR1 KO mice. Last, we also noted a reduced incidence of spontaneously-occurring hippocampal sharp wave-ripple events. Our study provides further evidence for aberrant hippocampal rhythms in the FMR1 KO mice and identifies potential signaling pathways underlying gamma band oscillopathy in FXS.

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Distinct Narrow and Broadband Gamma Responses in Human Visual Cortex

10.1101/572313 ◽

2019 ◽

Cited By ~ 4

Author(s):

Eleonora Bartoli ◽

William Bosking ◽

Ye Li ◽

Michael S. Beauchamp ◽

Daniel Yoshor ◽

...

Keyword(s):

Visual Cortex ◽

Critical Role ◽

Visual Stimuli ◽

Field Potential ◽

Gamma Oscillations ◽

Systematic Change ◽

Human Visual Cortex ◽

Gamma Range ◽

High Gamma ◽

Differential Properties

AbstractHigh frequency activity (> 30 Hz) in the neocortical local field potential, typically referred to as the ‘gamma’ range, is thought to have a critical role in visual perception and cognition more broadly. Historically, animal studies recording from visual cortex documented clear narrowband gamma oscillations (NBG; ∼20-60 Hz) in response to visual stimuli. However, invasive measurements from human neocortex have highlighted a different broadband or ‘high’ gamma response (BBG; ∼70-150+ Hz). Growing evidence suggests these two forms of gamma response are distinct, but often conceptually or analytically conflated as the same ‘gamma’ response. Furthermore, recent debate has highlighted that both the occurrence and spectral properties of gamma band activity in visual cortex appears to be dependent on the attributes and class of presented visual stimuli. Using high-density intracranial recordings from human visual cortex, we integrate and extend these findings, dissociating the spectral, temporal and functional properties of NBG and BBG activity. We report results from two experiments, manipulating visual stimulus attributes (contrast-varying gratings) and class (object categories) dissecting the differential properties of NBG and BBG responses. NBG oscillations were only reliably recorded for grating stimuli, while their peak frequency varied with contrast level. Whereas BBG activity was observed in response to all stimulus classes tested, with no systematic change in its spectral features. Temporally, induced NBG was sustained throughout stimulus presentation, in opposition to a more transient response for the BBG. These findings challenge the ubiquity of ‘gamma’ activity in visual cortex, by clearly dissociating oscillatory and broadband effects.Significance StatementNeocortical narrowband gamma oscillations (∼20-60 Hz) have been implicated in vision and cognition as a mechanism for synchronizing brain regions. Efforts to study this phenomenon have revealed an additional ‘high-gamma’ range response (∼70-150+ Hz), which is broadband and non-oscillatory. These different gamma range activities are often conflated in support of the same functional role. Using invasive recordings from human visual cortex, we show that narrow and broadband gamma can be dissociated by spectral, temporal and functional response properties. While broadband gamma responses were more transient to the presentation of all stimuli, narrowband gamma responses were sustained and only occurred reliably to grating stimuli. These differences have important implications for the study, analysis and interpretation of neocortical gamma range activity.

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Flexible Frequency Switching in Adult Mouse Visual Cortex Is Mediated by Competition between Parvalbumin and Somatostatin Expressing Interneurons

Neural Computation ◽

10.1162/neco_a_01369 ◽

2021 ◽

pp. 1-41

Author(s):

Justin W. M. Domhof ◽

Paul H. E. Tiesinga

Keyword(s):

Visual Cortex ◽

Network Model ◽

Visual Stimulation ◽

Field Potential ◽

Pyramidal Cells ◽

Gamma Oscillations ◽

Neuron Network ◽

Frequency Bands ◽

Adult Mice ◽

Beta Rhythms

Neuronal networks in rodent primary visual cortex (V1) can generate oscillations in different frequency bands depending on the network state and the level of visual stimulation. High-frequency gamma rhythms, for example, dominate the network's spontaneous activity in adult mice but are attenuated upon visual stimulation, during which the network switches to the beta band instead. The spontaneous local field potential (LFP) of juvenile mouse V1, however, mainly contains beta rhythms and presenting a stimulus does not elicit drastic changes in network oscillations. We study, in a spiking neuron network model, the mechanism in adult mice allowing for flexible switches between multiple frequency bands and contrast this to the network structure in juvenile mice that lack this flexibility. The model comprises excitatory pyramidal cells (PCs) and two types of interneurons: the parvalbumin-expressing (PV) and the somatostatinexpressing (SOM) interneuron. In accordance with experimental findings, the pyramidal-PV and pyramidal-SOM cell subnetworks are associated with gamma and beta oscillations, respectively. In our model, they are both generated via a pyramidal-interneuron gamma (PING) mechanism, wherein the PCs drive the oscillations. Furthermore, we demonstrate that large but not small visual stimulation activates SOM cells, which shift the frequency of resting-state gamma oscillations produced by the pyramidal-PV cell subnetwork so that beta rhythms emerge. Finally, we show that this behavior is obtained for only a subset of PV and SOM interneuron projection strengths, indicating that their influence on the PCs should be balanced so that they can compete for oscillatory control of the PCs. In sum, we propose a mechanism by which visual beta rhythms can emerge from spontaneous gamma oscillations in a network model of the mouse V1; for this mechanism to reproduce V1 dynamics in adult mice, balance between the effective strengths of PV and SOM cells is required.

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