Cortical Gamma-band Resonance Preferentially Transmits Coherent Input

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2021 May 5

PMID 33951439

Citations 16

Authors

Christopher Murphy Lewis

Jianguang Ni

Thomas Wunderle

Patrick Jendritza

Andreea Lazar

Ilka Diester

Pascal Fries

Affiliations

Soon will be listed here.

Abstract

Synchronization has been implicated in neuronal communication, but causal evidence remains indirect. We use optogenetics to generate depolarizing currents in pyramidal neurons of the cat visual cortex, emulating excitatory synaptic inputs under precise temporal control, while measuring spike output. The cortex transforms constant excitation into strong gamma-band synchronization, revealing the well-known cortical resonance. Increasing excitation with ramps increases the strength and frequency of synchronization. Slow, symmetric excitation profiles reveal hysteresis of power and frequency. White-noise input sequences enable causal analysis of network transmission, establishing that the cortical gamma-band resonance preferentially transmits coherent input components. Models composed of recurrently coupled excitatory and inhibitory units uncover a crucial role of feedback inhibition and suggest that hysteresis can arise through spike-frequency adaptation. The presented approach provides a powerful means to investigate the resonance properties of local circuits and probe how these properties transform input and shape transmission.

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References

Fries P, Womelsdorf T, Oostenveld R, Desimone R . The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4. J Neurosci. 2008; 28(18):4823-35. PMC: 3844818. DOI: 10.1523/JNEUROSCI.4499-07.2008. View

Akam T, Kullmann D . Oscillations and filtering networks support flexible routing of information. Neuron. 2010; 67(2):308-20. PMC: 3125699. DOI: 10.1016/j.neuron.2010.06.019. View

Grothe I, Neitzel S, Mandon S, Kreiter A . Switching neuronal inputs by differential modulations of gamma-band phase-coherence. J Neurosci. 2012; 32(46):16172-80. PMC: 6794021. DOI: 10.1523/JNEUROSCI.0890-12.2012. View

Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann D . Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling. Nat Neurosci. 2012; 15(5):763-8. PMC: 3378654. DOI: 10.1038/nn.3081. View

Gray C, Engel A, Konig P, Singer W . Synchronization of oscillatory neuronal responses in cat striate cortex: temporal properties. Vis Neurosci. 1992; 8(4):337-47. DOI: 10.1017/s0952523800005071. View

Rohenkohl G, Bosman C, Fries P . Gamma Synchronization between V1 and V4 Improves Behavioral Performance. Neuron. 2018; 100(4):953-963.e3. PMC: 6250574. DOI: 10.1016/j.neuron.2018.09.019. View

Onorato I, Neuenschwander S, Hoy J, Lima B, Rocha K, Broggini A . A Distinct Class of Bursting Neurons with Strong Gamma Synchronization and Stimulus Selectivity in Monkey V1. Neuron. 2019; 105(1):180-197.e5. DOI: 10.1016/j.neuron.2019.09.039. View

van Kerkoerle T, Self M, Dagnino B, Gariel-Mathis M, Poort J, van der Togt C . Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex. Proc Natl Acad Sci U S A. 2014; 111(40):14332-41. PMC: 4210002. DOI: 10.1073/pnas.1402773111. View

Adesnik H, Scanziani M . Lateral competition for cortical space by layer-specific horizontal circuits. Nature. 2010; 464(7292):1155-60. PMC: 2908490. DOI: 10.1038/nature08935. View

10.

Hadjipapas A, Lowet E, Roberts M, Peter A, De Weerd P . Parametric variation of gamma frequency and power with luminance contrast: A comparative study of human MEG and monkey LFP and spike responses. Neuroimage. 2015; 112:327-340. DOI: 10.1016/j.neuroimage.2015.02.062. View

11.

Schoffelen J, Oostenveld R, Fries P . Neuronal coherence as a mechanism of effective corticospinal interaction. Science. 2005; 308(5718):111-3. DOI: 10.1126/science.1107027. View

12.

Womelsdorf T, Lima B, Vinck M, Oostenveld R, Singer W, Neuenschwander S . Orientation selectivity and noise correlation in awake monkey area V1 are modulated by the gamma cycle. Proc Natl Acad Sci U S A. 2012; 109(11):4302-7. PMC: 3306673. DOI: 10.1073/pnas.1114223109. View

13.

Fries P . A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci. 2005; 9(10):474-80. DOI: 10.1016/j.tics.2005.08.011. View

14.

Michalareas G, Vezoli J, van Pelt S, Schoffelen J, Kennedy H, Fries P . Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas. Neuron. 2016; 89(2):384-97. PMC: 4871751. DOI: 10.1016/j.neuron.2015.12.018. View

15.

Borgers C, Epstein S, Kopell N . Background gamma rhythmicity and attention in cortical local circuits: a computational study. Proc Natl Acad Sci U S A. 2005; 102(19):7002-7. PMC: 1100794. DOI: 10.1073/pnas.0502366102. View

16.

Roberts M, Lowet E, Brunet N, Ter Wal M, Tiesinga P, Fries P . Robust gamma coherence between macaque V1 and V2 by dynamic frequency matching. Neuron. 2013; 78(3):523-36. DOI: 10.1016/j.neuron.2013.03.003. View

17.

Lee J, Whittington M, Kopell N . Top-down beta rhythms support selective attention via interlaminar interaction: a model. PLoS Comput Biol. 2013; 9(8):e1003164. PMC: 3738471. DOI: 10.1371/journal.pcbi.1003164. View

18.

Pesaran B, Pezaris J, Sahani M, Mitra P, Andersen R . Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci. 2002; 5(8):805-11. DOI: 10.1038/nn890. View

19.

Iaccarino H, Singer A, Martorell A, Rudenko A, Gao F, Gillingham T . Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nature. 2016; 540(7632):230-235. PMC: 5656389. DOI: 10.1038/nature20587. View

20.

Wang X, Buzsaki G . Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci. 1996; 16(20):6402-13. PMC: 6578902. View