Dynamics and sources of response variability and its coordination in visual cortex

Abstract The trial-to-trial response variability in sensory cortices and the extent to which this variability can be coordinated among cortical units have strong implications for cortical signal processing. Yet, little is known about the relative contributions and dynamics of defined sources to the cortical response variability and their correlations across cortical units. To fill this knowledge gap, here we obtained and analyzed multisite local field potential (LFP) recordings from visual cortex of turtles in response to repeated naturalistic movie clips and decomposed cortical across-trial LFP response variability into three defined sources, namely, input, network, and local fluctuations. We found that input fluctuations dominate cortical response variability immediately following stimulus onset, whereas network fluctuations dominate the response variability in the steady state during continued visual stimulation. Concurrently, we found that the network fluctuations dominate the correlations of the variability during the ongoing and steady-state epochs, but not immediately following stimulus onset. Furthermore, simulations of various model networks indicated that (i) synaptic time constants, leading to oscillatory activity, and (ii) synaptic clustering and synaptic depression, leading to spatially constrained pockets of coherent activity, are both essential features of cortical circuits to mediate the observed relative contributions and dynamics of input, network, and local fluctuations to the cortical LFP response variability and their correlations across recording sites. In conclusion, these results show how a mélange of multiscale thalamocortical circuit features mediate a complex stimulus-modulated cortical activity that, when naively related to the visual stimulus alone, appears disguised as high and coordinated across-trial response variability.

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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

Journal of Neurophysiology ◽

10.1152/jn.00375.2017 ◽

2017 ◽

Vol 118 (5) ◽

pp. 2579-2591 ◽

Cited By ~ 3

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.

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Theta Phase-Dependent Modulation of Perception by Concurrent tACS and Periodic Visual Stimulation

10.1101/738906 ◽

2019 ◽

Author(s):

Elif Somer ◽

John Allen ◽

Joseph Brooks ◽

Vaughan Buttrill ◽

Amir-Homayoun Javadi

Keyword(s):

Visual Cortex ◽

Visual Stimulus ◽

Auditory Perception ◽

Visual Stimulation ◽

Sensory Perception ◽

Oscillatory Activity ◽

Matching Task ◽

Phase 0 ◽

Theta Frequency ◽

Visual Matching

AbstractBackgroundSensory perception can be modulated by the phase of neural oscillations, especially in the theta and alpha ranges. Oscillatory activity in the visual cortex can be entrained by transcranial alternating current stimulation (tACS) as well as periodic visual stimulation (i.e., flicker). Combined tACS and visual flicker stimulation modulates blood-oxygen-level-dependent (BOLD) responses and concurrent 4 Hz auditory click-trains and tACS modulates auditory perception in a phase-dependent way.ObjectiveIn the present study, we investigated if phase synchrony between concurrent tACS and periodic visual stimulation (i.e., flicker) can modulate performance on a visual matching task.MethodsParticipants completed a visual matching task on a flickering visual stimulus while receiving either in-phase (0 degree) or asynchronous (180, 90, or 270 degrees) tACS at alpha or theta frequency. Stimulation was applied over either occipital cortex or dorsolateral prefrontal cortex (DLPFC).ResultsVisual performance was significantly better during theta frequency tACS over the visual cortex when it was in-phase (0 degree) with visual stimulus flicker, compared to anti-phase (180 degree). This effect did not appear with alpha frequency flicker or with DLPFC stimulation. Furthermore, a control sham group showed no effect. There were no significant performance differences amongst the asynchronous (180, 90, and 270 degrees) phase conditions.ConclusionExtending previous studies on visual and auditory perception, our results support a crucial role of oscillatory phase in sensory perception and demonstrate a behaviourally relevant combination of visual flicker and tACS. The spatial and frequency specificity of our results have implications for research on the functional organisation of perception.

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Stereotactic electroencephalography in humans reveals multisensory signal in early visual and auditory cortices

10.1101/549733 ◽

2019 ◽

Cited By ~ 2

Author(s):

Stefania Ferraro ◽

Markus J. Van Ackeren ◽

Roberto Mai ◽

Laura Tassi ◽

Francesco Cardinale ◽

...

Keyword(s):

Visual Cortex ◽

Auditory Cortex ◽

Auditory Processing ◽

Multisensory Processing ◽

Low Frequency ◽

Event Related Potentials ◽

Stimulus Onset ◽

Oscillatory Activity ◽

Visual Responses ◽

Related Potentials

AbstractUnequivocally demonstrating the presence of multisensory signals at the earliest stages of cortical processing remains challenging in humans. In our study, we relied on the unique spatio-temporal resolution provided by intracranial stereotactic electroencephalographic (SEEG) recordings in patients with drug-resistant epilepsy to characterize the signal extracted from early visual (calcarine and pericalcarine) and auditory (Heschl’s gyrus and planum temporale) regions during a simple audio-visual oddball task. We provide evidences that both cross-modal responses (visual responses in auditory cortex or the reverse) and multisensory processing (alteration of the unimodal responses during bimodal stimulation) can be observed in intracranial event-related potentials (iERPs) and in power modulations of oscillatory activity at different temporal scales within the first 150 ms after stimulus onset. The temporal profiles of the iERPs are compatible with the hypothesis that MSI occurs by means of direct pathways linking early visual and auditory regions. Our data indicate, moreover, that MSI mainly relies on modulations of the low-frequency bands (foremost the theta band in the auditory cortex and the alpha band in the visual cortex), suggesting the involvement of feedback pathways between the two sensory regions. Remarkably, we also observed high-gamma power modulations by sounds in the early visual cortex, thus suggesting the presence of neuronal populations involved in auditory processing in the calcarine and pericalcarine region in humans.

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

Journal of Neurophysiology ◽

10.1152/jn.00414.2013 ◽

2013 ◽

Vol 110 (7) ◽

pp. 1703-1721 ◽

Cited By ~ 19

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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Visual Cortex Local Field Potential (LFP)nin the Mouse are Linked to Respiration and Visual Stimulation

Proceedings of the International Conference on Education, Management, Commerce and Society ◽

10.2991/emcs-15.2015.130 ◽

2015 ◽

Cited By ~ 1

Author(s):

Ran Zhai ◽

Junhui Cui ◽

Hongwei Ding ◽

Long Wang

Keyword(s):

Visual Cortex ◽

Local Field ◽

Local Field Potential ◽

Visual Stimulation ◽

Field Potential ◽

Local Field Potential Lfp

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Detection of a Weak Somatosensory Stimulus: Role of the Prestimulus Mu Rhythm and Its Top–Down Modulation

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2009.21247 ◽

2010 ◽

Vol 22 (2) ◽

pp. 307-322 ◽

Cited By ~ 63

Author(s):

Yan Zhang ◽

Mingzhou Ding

Keyword(s):

Field Potential ◽

Electrical Stimulus ◽

Stimulus Onset ◽

Oscillatory Activity ◽

Somatosensory Processing ◽

Causality Analysis ◽

Mu Rhythm ◽

Potential Oscillations ◽

Scalp Electroencephalogram ◽

The Right

The ongoing neural activity in human primary somatosensory cortex (SI) is characterized by field potential oscillations in the 7–13 Hz range known as the mu rhythm. Recent work has shown that the magnitude of the mu oscillation immediately preceding the onset of a weak stimulus has a significant impact on its detection. The neural mechanisms mediating this impact remain not well understood. In particular, whether and how somatosensory mu rhythm is modulated by executive areas prior to stimulus onset for improved behavioral performance has not been investigated. We addressed these issues by recording 128-channel scalp electroencephalogram from normal volunteers performing a somatosensory perception experiment in which they reported the detection of a near-threshold electrical stimulus (∼50% detection rate) delivered to the right index finger. Three results were found. First, consistent with numerous previous reports, the N1 component (∼140 msec) of the somatosensory-evoked potential was significantly enhanced for perceived stimulus compared to unperceived stimulus. Second, the prestimulus mu power and the evoked N1 amplitude exhibited an inverted-U relationship, suggesting that an intermediate level of prestimulus mu oscillatory activity is conducive to stimulus processing and perception. Third, a Granger causality analysis revealed that the prestimulus causal influence in the mu band from prefrontal cortex to SI was significantly higher for perceived stimulus than for unperceived stimulus, indicating that frontal executive structures, via ongoing mu oscillations, exert cognitive control over posterior sensory cortices to facilitate somatosensory processing.

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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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Neurofeedback Training of Gamma Oscillations in Monkey Primary Visual Cortex

Cerebral Cortex ◽

10.1093/cercor/bhz013 ◽

2019 ◽

Vol 29 (11) ◽

pp. 4785-4802 ◽

Cited By ~ 4

Author(s):

L Chauvière ◽

W Singer

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Stimulation ◽

Brain Activity ◽

Gamma Oscillations ◽

Gamma Activity ◽

Oscillatory Activity ◽

Feedback Signal ◽

Sensory Cortices ◽

Distinct Frequency

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.

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Alternating Periods of High and Low-Entropy Neural Ensemble Activity During Image Processing in the Primary Visual Cortex of Rats

The Open Biomedical Engineering Journal ◽

10.2174/1874120701610010051 ◽

2016 ◽

Vol 10 (1) ◽

pp. 51-61

Author(s):

Xiaoyuan Li ◽

Qiwei Li ◽

Li Shi ◽

Liucheng Jiao

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Processing ◽

Visual Stimulation ◽

Visual Stimuli ◽

Field Potential ◽

Discrete Wavelet ◽

Neural Ensemble ◽

Highly Nonlinear ◽

Ensemble Activity

The response properties of individual neurons in the primary visual cortex (V1) are among the most thoroughly described in the mammalian central nervous system, but they reveal less about higher-order processes like visual perception. Neural activity is highly nonlinear and non-stationary over time, greatly complicating the relationships among the spatiotemporal characteristics of visual stimuli, local field potential (LFP) signal components, and the underlying neuronal activity patterns. We applied discrete wavelet transformation to detect new features of the LFP that may better describe the association between visual input and neural ensemble activity. The relative wavelet energy (RWE), wavelet entropy (WS), and the mean WS were computed from LFPs recorded in rat V1 during three distinct visual stimuli: low ambient light, a uniform grey computer screen, and simple pictures of common scenes. The time evolution of the RWE within the γ band (31-62.5 Hz) was the dominant component over certain periods during visual stimulation. Mean WS decreased with increasing complexity of the visual image, and the time-dependent WS alternated between periods of highly ordered and disordered population activity. In conclusion, these alternating periods of high and low WS may correspond to different aspects of visual processing, such as feature extraction and perception.

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