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

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.

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

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.

scholarly journals Superimposed gratings induce diverse response patterns of gamma oscillations in primary visual cortex

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Bin Wang ◽  
Chuanliang Han ◽  
Tian Wang ◽  
Weifeng Dai ◽  
Yang Li ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Neural Mechanisms ◽  
Model Parameters ◽  
Response Patterns ◽  
Region Difference ◽  
High Gamma ◽  
Spiking Activity

AbstractStimulus-dependence of gamma oscillations (GAMMA, 30–90 Hz) has not been fully understood, but it is important for revealing neural mechanisms and functions of GAMMA. Here, we recorded spiking activity (MUA) and the local field potential (LFP), driven by a variety of plaids (generated by two superimposed gratings orthogonal to each other and with different contrast combinations), in the primary visual cortex of anesthetized cats. We found two distinct narrow-band GAMMAs in the LFPs and a variety of response patterns to plaids. Similar to MUA, most response patterns showed that the second grating suppressed GAMMAs driven by the first one. However, there is only a weak site-by-site correlation between cross-orientation interactions in GAMMAs and those in MUAs. We developed a normalization model that could unify the response patterns of both GAMMAs and MUAs. Interestingly, compared with MUAs, the GAMMAs demonstrated a wider range of model parameters and more diverse response patterns to plaids. Further analysis revealed that normalization parameters for high GAMMA, but not those for low GAMMA, were significantly correlated with the discrepancy of spatial frequency between stimulus and sites’ preferences. Consistent with these findings, normalization parameters and diversity of high GAMMA exhibited a clear transition trend and region difference between area 17 to 18. Our results show that GAMMAs are also regulated in the form of normalization, but that the neural mechanisms for these normalizations might differ from those of spiking activity. Normalizations in different brain signals could be due to interactions of excitation and inhibitions at multiple stages in the visual system.

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

eLife ◽  
2018 ◽  
Vol 7 ◽  
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.

Spike Timing of Lacunosom-Moleculare Targeting Interneurons and CA3 Pyramidal Cells During High-Frequency Network Oscillations In Vitro

2007 ◽  
Vol 98 (1) ◽  
pp. 96-104 ◽  
Author(s):  
Jay Spampanato ◽  
Istvan Mody
Keyword(s):  
High Frequency ◽  
Epileptiform Activity ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Spike Timing ◽  
Network Activity ◽  
Network Oscillations ◽  
Ca3 Pyramidal Cells

Network activity in the 200- to 600-Hz range termed high-frequency oscillations (HFOs) has been detected in epileptic tissue from both humans and rodents and may underlie the mechanism of epileptogenesis in experimental rodent models. Slower network oscillations including theta and gamma oscillations as well as ripples are generated by the complex spike timing and interactions between interneurons and pyramidal cells of the hippocampus. We determined the activity of CA3 pyramidal cells, stratum oriens lacunosum-moleculare (O-LM) and s. radiatum lacunosum-moleculare (R-LM) interneurons during HFO in the in vitro low-Mg2+ model of epileptiform activity in GIN mice. In these animals, interneurons can be identified prior to cell-attached recordings by the expression of green-fluorescent protein (GFP). Simultaneous local field potential recordings from s. pyramidale and on-cell recordings of individual interneurons and principal cells revealed three primary firing behaviors of the active cells: 36% of O-LM interneurons and 60% of pyramidal cells fired action potentials at high frequencies during the HFO. R-LM interneurons were biphasic in that they fired at high frequency at the beginning of the HFO but stopped firing before its end. When considering only the highest frequency component of the oscillations most pyramidal cells fired on the rising phase of the oscillation. These data provide evidence for functional distinction during HFOs within otherwise homogeneous groups of O-LM interneurons and pyramidal cells.

scholarly journals Sensory-driven and spontaneous gamma oscillations engage distinct cortical circuitry

2016 ◽  
Vol 115 (4) ◽  
pp. 1821-1835 ◽  
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.

scholarly journals Induced cortical oscillations in turtle cortex are coherent at the mesoscale of population activity, but not at the microscale of the membrane potential of neurons

2017 ◽  
Vol 118 (5) ◽  
pp. 2579-2591 ◽  
Author(s):  
Mahmood S. Hoseini ◽  
Jeff Pobst ◽  
Nathaniel Wright ◽  
Wesley Clawson ◽  
Woodrow Shew ◽  
...  
Keyword(s):  
Visual Cortex ◽  
Membrane Potential ◽  
Neural Activity ◽  
Visual Stimulation ◽  
Field Potential ◽  
Brain Regions ◽  
Large Trial ◽  
Population Activity ◽  
Potential Oscillations ◽  
Time Frequency

Bursts of oscillatory neural activity have been hypothesized to be a core mechanism by which remote brain regions can communicate. Such a hypothesis raises the question to what extent oscillations are coherent across spatially distant neural populations. To address this question, we obtained local field potential (LFP) and membrane potential recordings from the visual cortex of turtle in response to visual stimulation of the retina. The time-frequency analysis of these recordings revealed pronounced bursts of oscillatory neural activity and a large trial-to-trial variability in the spectral and temporal properties of the observed oscillations. First, local bursts of oscillations varied from trial to trial in both burst duration and peak frequency. Second, oscillations of a given recording site were not autocoherent; i.e., the phase did not progress linearly in time. Third, LFP oscillations at spatially separate locations within the visual cortex were more phase coherent in the presence of visual stimulation than during ongoing activity. In contrast, the membrane potential oscillations from pairs of simultaneously recorded pyramidal neurons showed smaller phase coherence, which did not change when switching from black screen to visual stimulation. In conclusion, neuronal oscillations at distant locations in visual cortex are coherent at the mesoscale of population activity, but coherence is largely absent at the microscale of the membrane potential of neurons. NEW & NOTEWORTHY Coherent oscillatory neural activity has long been hypothesized as a potential mechanism for communication across locations in the brain. In this study we confirm the existence of coherent oscillations at the mesoscale of integrated cortical population activity. However, at the microscopic level of neurons, we find no evidence for coherence among oscillatory membrane potential fluctuations. These results raise questions about the applicability of the communication through coherence hypothesis to the level of the membrane potential.

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

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.

scholarly journals Comparison of tuning properties of gamma and high-gamma power in local field potential (LFP) versus electrocorticogram (ECoG) in visual cortex

2019 ◽  
Author(s):  
Agrita Dubey ◽  
Supratim Ray
Keyword(s):  
Visual Cortex ◽  
Local Field ◽  
Local Field Potential ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Orientation Contrast ◽  
High Gamma ◽  
Gamma Power ◽  
Electrocorticogram Ecog ◽  
Local Field Potential Lfp

AbstractElectrocorticogram (ECoG), obtained from macroelectrodes placed on the cortex, is typically used in drug-resistant epilepsy patients, and is increasingly being used to study cognition in humans. These studies often use power in gamma (30-70 Hz) or high-gamma (>80 Hz) ranges to make inferences about neural processing. However, while the stimulus tuning properties of gamma/high-gamma power have been well characterized in local field potential (LFP; obtained from microelectrodes), analogous characterization has not been done for ECoG. Using a hybrid array containing both micro and ECoG electrodes implanted in the primary visual cortex of two female macaques, we compared the stimulus tuning preferences of gamma/high-gamma power in LFP versus ECoG and found them to be surprisingly similar. High-gamma power, thought to index the average firing rate around the electrode, was highest for the smallest stimulus (0.3° radius), and decreased with increasing size in both LFP and ECoG, suggesting local origins of both signals. Further, gamma oscillations were similarly tuned in LFP and ECoG to stimulus orientation, contrast and spatial frequency. This tuning was significantly weaker in electroencephalogram (EEG), suggesting that ECoG is more like LFP than EEG. Overall, our results validate the use of ECoG in clinical and basic cognitive research.

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

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.

scholarly journals Multichannel brain recordings in behaving Drosophila reveal oscillatory activity and local coherence in response to sensory stimulation and circuit activation

2013 ◽  
Vol 110 (7) ◽  
pp. 1703-1721 ◽  
Author(s):  
Angelique C. Paulk ◽  
Yanqiong Zhou ◽  
Peter Stratton ◽  
Li Liu ◽  
Bruno van Swinderen
Keyword(s):  
Visual Stimulation ◽  
Sensory Modality ◽  
Field Potential ◽  
Brain Regions ◽  
Oscillatory Activity ◽  
Insect Brain ◽  
Sensory Stimuli ◽  
Multichannel Recording ◽  
Frequency Bands

Neural networks in vertebrates exhibit endogenous oscillations that have been associated with functions ranging from sensory processing to locomotion. It remains unclear whether oscillations may play a similar role in the insect brain. We describe a novel “whole brain” readout for Drosophila melanogaster using a simple multichannel recording preparation to study electrical activity across the brain of flies exposed to different sensory stimuli. We recorded local field potential (LFP) activity from >2,000 registered recording sites across the fly brain in >200 wild-type and transgenic animals to uncover specific LFP frequency bands that correlate with: 1) brain region; 2) sensory modality (olfactory, visual, or mechanosensory); and 3) activity in specific neural circuits. We found endogenous and stimulus-specific oscillations throughout the fly brain. Central (higher-order) brain regions exhibited sensory modality-specific increases in power within narrow frequency bands. Conversely, in sensory brain regions such as the optic or antennal lobes, LFP coherence, rather than power, best defined sensory responses across modalities. By transiently activating specific circuits via expression of TrpA1, we found that several circuits in the fly brain modulate LFP power and coherence across brain regions and frequency domains. However, activation of a neuromodulatory octopaminergic circuit specifically increased neuronal coherence in the optic lobes during visual stimulation while decreasing coherence in central brain regions. Our multichannel recording and brain registration approach provides an effective way to track activity simultaneously across the fly brain in vivo, allowing investigation of functional roles for oscillations in processing sensory stimuli and modulating behavior.

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