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

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.

2021 ◽  
pp. 1-41
Author(s):  
Justin W. M. Domhof ◽  
Paul H. E. Tiesinga

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.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Richard Hakim ◽  
Kiarash Shamardani ◽  
Hillel Adesnik

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.


2016 ◽  
Vol 115 (4) ◽  
pp. 1821-1835 ◽  
Author(s):  
Cristin G. Welle ◽  
Diego Contreras

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.


2020 ◽  
Author(s):  
Katharina Duecker ◽  
Tjerk P. Gutteling ◽  
Christoph S. Herrmann ◽  
Ole Jensen

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.


2021 ◽  
Author(s):  
Alexander Zhigalov ◽  
Katharina Duecker ◽  
Ole Jensen

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.


2021 ◽  
Vol 17 (6) ◽  
pp. e1009046
Author(s):  
Alexander Zhigalov ◽  
Katharina Duecker ◽  
Ole Jensen

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.


PLoS ONE ◽  
2020 ◽  
Vol 15 (12) ◽  
pp. e0243237
Author(s):  
Gavin Perry ◽  
Nathan W. Taylor ◽  
Philippa C. H. Bothwell ◽  
Colette C. Milbourn ◽  
Georgina Powell ◽  
...  

It has recently been demonstrated through invasive electrophysiology that visual stimulation with extended patches of uniform colour generates pronounced gamma oscillations in the visual cortex of both macaques and humans. In this study we sought to discover if this oscillatory response to colour can be measured non-invasively in humans using magnetoencephalography. We were able to demonstrate increased gamma (40–70 Hz) power in response to full-screen stimulation with four different colour hues and found that the gamma response is particularly strong for long wavelength (i.e. red) stimulation, as was found in previous studies. However, we also found that gamma power in response to colour was generally weaker than the response to an identically sized luminance-defined grating. We also observed two additional responses in the gamma frequency: a lower frequency response around 25–35 Hz that showed fewer clear differences between conditions than the gamma response, and a higher frequency response around 70–100 Hz that was present for red stimulation but not for other colours. In a second experiment we sought to test whether differences in the gamma response between colour hues could be explained by their chromatic separation from the preceding display. We presented stimuli that alternated between each of the three pairings of the three primary colours (red, green, blue) at two levels of chromatic separation defined in the CIELUV colour space. We observed that the gamma response was significantly greater to high relative to low chromatic separation, but that at each level of separation the response was greater for both red-blue and red-green than for blue-green stimulation. Our findings suggest that the stronger gamma response to red stimulation cannot be wholly explained by the chromatic separation of the stimuli.


2019 ◽  
Vol 29 (11) ◽  
pp. 4785-4802 ◽  
Author(s):  
L Chauvière ◽  
W Singer

Abstract In humans, neurofeedback (NFB) training has been used extensively and successfully to manipulate brain activity. Feedback signals were derived from EEG, fMRI, MEG, and intracranial recordings and modifications were obtained of the BOLD signal, of the power of oscillatory activity in distinct frequency bands and of single unit activity. The purpose of the present study was to examine whether neuronal activity could also be controlled by NFB in early sensory cortices whose activity is thought to be influenced mainly by sensory input rather than volitional control. We trained 2 macaque monkeys to enhance narrow band gamma oscillations in the primary visual cortex by providing them with an acoustic signal that reflected the power of gamma oscillations in a preselected band and rewarding increases of the feedback signal. Oscillations were assessed from local field potentials recorded with chronically implanted microelectrodes. Both monkeys succeeded to raise gamma activity in the absence of visual stimulation in the selected frequency band and at the site from which the NFB signal was derived. This suggests that top–down signals are not confined to just modulate stimulus induced responses but can actually drive or facilitate the gamma generating microcircuits even in a primary sensory area.


2001 ◽  
Vol 18 (1) ◽  
pp. 9-24 ◽  
Author(s):  
JAIME G. MANCILLA ◽  
PHILIP S. ULINSKI

The visual cortex of freshwater turtles contains pyramidal cells, which have a regular spiking (RS) firing pattern, and several categories of aspiny, inhibitory interneurons. The interneurons show diverse firing patterns, including the fast spiking (FS) pattern. Postsynaptic potentials (PSPs) evoked in FS cells by visual stimulation of the retina reach their peak amplitudes as much as 200 ms before PSPs in RS cells (Mancilla et al., 1998). FS cells could, consequently, control the amplitudes of light-evoked PSPs in RS cells by producing disynaptic, feedforward inhibitory postsynaptic potentials (IPSPs) that overlap in time with geniculocortical excitatory postsynaptic potentials (EPSPs). Since FS cells receive recurrent, excitatory inputs from RS cells, they could also control the amplitudes of light-evoked PSPs in RS cells via polysynaptic, feedback inhibition. The in vitro geniculocortical preparation of Pseudemys scripta was used to characterize the temporal relationships of EPSPs and IPSPs produced in RS cells by electrical activation of geniculate afferents and by diffuse light flashes presented to the retina. GABAA receptor-mediated inhibition was blocked using extracellular application of bicuculline (3.5 mM) or intracellular perfusion of picrotoxin (1 μM) in individual RS cells. Electrical stimulation of thalamic afferents produced compound PSPs. Blockade of GABAA receptor-mediated IPSPs with either bicuculline or picrotoxin provided evidence for both early and late IPSPs in RS cells. Analysis of the apparent reversal potentials of light-evoked PSPs indicated the existence of early IPSPs during the first 140–300 ms following light onset. Light responses of cells perfused with picrotoxin diverged from control light responses at about 300 ms after light onset and had maximum amplitudes that were significantly different from control light responses. These experiments indicate that the responses of RS cells to both electrical and natural stimulation of geniculate afferents are controlled by both early and late IPSPs, consistent with activation of both feedforward and feedback pathways.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Bin Wang ◽  
Chuanliang Han ◽  
Tian Wang ◽  
Weifeng Dai ◽  
Yang Li ◽  
...  

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.


Sign in / Sign up

Export Citation Format

Share Document