Visual Stimulus Content in V4 Is Conveyed by Gamma-Rhythmic Information Packages

Lisitsyn, Dmitriy; Grothe, Iris; Kreiter, Andreas K.; Ernst, Udo

doi:10.1523/jneurosci.0689-20.2020

Cited by 6 publications

(3 citation statements)

References 67 publications

(102 reference statements)

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“…Gamma phase also modulates orientation selectivity and correlated variability between neurons [68]. This enhancement is modulated by attention [69]. Our results indicate that these effects reflect shifts in somatic sensitivity to excitatory synaptic inputs.…”

Section: Discussionmentioning

confidence: 73%

Spatially targeted inhibitory rhythms differentially affect neuronal integration

Headley,

Latimer,

Aberbach

et al. 2024

Preprint

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Pyramidal neurons form dense recurrently connected networks with multiple types of inhibitory interneurons. A major differentiator between interneuron subtypes is whether they synapse onto perisomatic or dendritic regions. They can also engender local inhibitory rhythms, beta (12-35 Hz) and gamma (40-80 Hz). The interaction between the rhythmicity of inhibition and its spatial targeting on the neuron may determine how it regulates neuronal integration. Thus, we sought to understand how rhythmic perisomatic and distal dendritic inhibition impacted integration in a layer 5 pyramidal neuron model with elaborate dendrites and Na+, NMDA, and Ca2+dendritic spikes. We found that inhibition regulated the coupling between dendritic spikes and action potentials in a location and rhythm-dependent manner. Perisomatic inhibition principally regulated action potential generation, while distal dendritic inhibition regulated the incidence of dendritic spikes and their temporal coupling with action potentials. Perisomatic inhibition was most effective when provided at gamma frequencies, while distal dendritic inhibition functioned best at beta. Moreover, beta modulated responsiveness to apical inputs in a phase-dependent manner, while gamma did so for basal inputs. These results may provide a functional interpretation for the reported association of soma-targeting parvalbumin positive interneurons with gamma, and dendrite-targeting somatostatin interneurons with beta.

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Section: Discussionmentioning

confidence: 73%

Spatially targeted inhibitory rhythms differentially affect neuronal integration

Headley,

Latimer,

Aberbach

et al. 2024

Preprint

View full text Add to dashboard Cite

show abstract

“…Indeed, numerous studies have observed systematic changes in the spatiotemporal structure of neuronal activity, such as selective synchronization and desynchronization of oscillatory activity, during cognitive processes such as perception or selective attention that imply meaningful changes in information processing 4,27,28,30,31,42,43 . Therefore, γphase-dependent modulation of neuronal interactions appears to be a widely employed basic mechanism supporting flexible signal and information routing, and network configuration 5,44,45 .…”

Section: Discussionmentioning

confidence: 99%

Neuronal information processing causally depends on gamma phase synchrony

Drebitz,

Rausch,

Kreiter

2023

Preprint

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Successful behaviour relies on the brain’s ability to flexibly process relevant information while suppressing irrelevant information1. Visual neurons show functional flexibility by selectively responding to subsets of inputs representing attended objects while ignoring those conveying information about irrelevant objects2–5. Several neuronal mechanisms underlying such attention-dependent processing have been proposed. However, causation has not yet been proven6–9. We show that the spike arrival time with respect to the receiving neurons’ γ-oscillatory activity is causal to the spikes’ impact on these neurons and behaviour. We performed intracortical microstimulation (ICM) in area V2 of macaque monkeys to evoke spikes. These ICM-evoked spikes caused a significant increase in the spiking activity of receiving V4 neurons and a significant delay in monkeys’ responses. These effects were observed only when ICM-evoked spikes arrived close to the peak of the neurons’ excitability cycle, with no effects observed during other phases of the V4 γ-cycle. Our results demonstrate that phase synchronization between input spikes and receiver neurons is causal for selective signal routing and required for flexible network configuration. These results are significant for future theoretical and experimental research on selective information processing and brain-computer interfaces.

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“…To heighten task difficulty, the stimulus luminance changed randomly with each frame of the screen. For this, a random, integer gray pixel value was selected before each frame update [0 255] corresponding to luminance changes from 0.02 – 45.4 Cd/m 2 , on average 3.8 Cd/m 2 (for details: Grothe et al, 2018; Lisitsyn et al, 2020). From trial initiation until lever release, monkeys had to hold their gaze within a window of 1° diameter centered on the fixation square.…”

Section: Methodsmentioning

confidence: 99%

Three distinct gamma oscillatory networks within cortical columns in macaque monkeys’ area V1

Drebitz,

Rausch,

Gil

et al. 2023

Preprint

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A fundamental property of the neocortex is its columnar organization in many species. Generally, neurons of the same column share stimulus preferences and have strong anatomical connections across layers. These features suggest that neurons within a column operate as one unified network. Other features, like the different patterns of input and output connections of neurons located in separate layers and systematic differences in feature tuning, hint at a more segregated and possibly flexible functional organization of neurons within a column. To distinguish between these views of columnar processing, we conducted laminar recordings in macaques’ area V1 while they performed a demanding attention task. We found three separate regions with strong gamma oscillatory current source density (CSD) signals, one each in the supragranular, granular, and infragranular laminar domains. Their characteristics differed significantly in terms of their dominant gamma frequency and attention-dependent modulation of their gramma power and gamma frequency. In line, spiking activity in the supragranular, infragranular, and upper part of the granular domain exhibited strong phase coherence with their domain’s CSD signals but showed much weaker coherence with the other domains’ CSD signals. These results indicate that columnar processing involves a certain degree of independence between neurons in the three laminar domains, consistent with the assumption of multiple, separate intracolumnar ensembles. Such a functional organization offers various possibilities for dynamic network configuration, indicating that neurons in a column are not restricted to operate as one unified network. Thus, the findings open interesting new possibilities for future concepts and investigations on flexible, dynamic cortical ensemble formation and selective information processing.

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Visual Stimulus Content in V4 Is Conveyed by Gamma-Rhythmic Information Packages

Cited by 6 publications

References 67 publications

Spatially targeted inhibitory rhythms differentially affect neuronal integration

Spatially targeted inhibitory rhythms differentially affect neuronal integration

Neuronal information processing causally depends on gamma phase synchrony

Three distinct gamma oscillatory networks within cortical columns in macaque monkeys’ area V1

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