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

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.

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.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Janelle MP Pakan ◽  
Scott C Lowe ◽  
Evelyn Dylda ◽  
Sander W Keemink ◽  
Stephen P Currie ◽  
...  

Cortical responses to sensory stimuli are modulated by behavioral state. In the primary visual cortex (V1), visual responses of pyramidal neurons increase during locomotion. This response gain was suggested to be mediated through inhibitory neurons, resulting in the disinhibition of pyramidal neurons. Using in vivo two-photon calcium imaging in layers 2/3 and 4 in mouse V1, we reveal that locomotion increases the activity of vasoactive intestinal peptide (VIP), somatostatin (SST) and parvalbumin (PV)-positive interneurons during visual stimulation, challenging the disinhibition model. In darkness, while most VIP and PV neurons remained locomotion responsive, SST and excitatory neurons were largely non-responsive. Context-dependent locomotion responses were found in each cell type, with the highest proportion among SST neurons. These findings establish that modulation of neuronal activity by locomotion is context-dependent and contest the generality of a disinhibitory circuit for gain control of sensory responses by behavioral state.


2018 ◽  
Vol 8 (1) ◽  
Author(s):  
Waja Wegner ◽  
Alexander C. Mott ◽  
Seth G. N. Grant ◽  
Heinz Steffens ◽  
Katrin I. Willig

2019 ◽  
Vol 11 (480) ◽  
pp. eaan0457 ◽  
Author(s):  
Vikram Jakkamsetti ◽  
Isaac Marin-Valencia ◽  
Qian Ma ◽  
Levi B. Good ◽  
Tyler Terrill ◽  
...  

Glucose is the ultimate substrate for most brain activities that use carbon, including synthesis of the neurotransmitters glutamate and γ-aminobutyric acid via mitochondrial tricarboxylic acid (TCA) cycle. Brain metabolism and neuronal excitability are thus interdependent. However, the principles that govern their relationship are not always intuitive because heritable defects of brain glucose metabolism are associated with the paradoxical coexistence, in the same individual, of episodic neuronal hyperexcitation (seizures) with reduced basal cerebral electrical activity. One such prototypic disorder is pyruvate dehydrogenase (PDH) deficiency (PDHD). PDH is central to metabolism because it steers most of the glucose-derived flux into the TCA cycle. To better understand the pathophysiology of PDHD, we generated mice with brain-specific reduced PDH activity that paralleled salient human disease features, including cerebral hypotrophy, decreased amplitude electroencephalogram (EEG), and epilepsy. The mice exhibited reductions in cerebral TCA cycle flux, glutamate content, spontaneous, and electrically evoked in vivo cortical field potentials and gamma EEG oscillation amplitude. Episodic decreases in gamma oscillations preceded most epileptiform discharges, facilitating their prediction. Fast-spiking neuron excitability was decreased in brain slices, contributing to in vivo action potential burst prolongation after whisker pad stimulation. These features were partially reversed after systemic administration of acetate, which augmented cerebral TCA cycle flux, glutamate-dependent synaptic transmission, inhibition and gamma oscillations, and reduced epileptiform discharge duration. Thus, our results suggest that dysfunctional excitability in PDHD is consequent to reduced oxidative flux, which leads to decreased neuronal activation and impaired inhibition, and can be mitigated by an alternative metabolic substrate.


Author(s):  
Andreas J. Keller ◽  
Mario Dipoppa ◽  
Morgane M. Roth ◽  
Matthew S. Caudill ◽  
Alessandro Ingrosso ◽  
...  

Context guides perception by influencing the saliency of sensory stimuli. Accordingly, in visual cortex, responses to a stimulus are modulated by context, the visual scene surrounding the stimulus. Responses are suppressed when stimulus and surround are similar but not when they differ. The mechanisms that remove suppression when stimulus and surround differ remain unclear. Here we use optical recordings, manipulations, and computational modelling to show that a disinhibitory circuit consisting of vasoactive-intestinal-peptide-expressing (VIP) and somatostatin-expressing (SOM) inhibitory neurons modulates responses in mouse visual cortex depending on the similarity between stimulus and surround. When the stimulus and the surround are similar, VIP neurons are inactive and SOM neurons suppress excitatory neurons. However, when the stimulus and the surround differ, VIP neurons are active, thereby inhibiting SOM neurons and relieving excitatory neurons from suppression. We have identified a canonical cortical disinhibitory circuit which contributes to contextual modulation and may regulate perceptual saliency.


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.


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.


Sign in / Sign up

Export Citation Format

Share Document