Flexible information routing by transient synchrony

Agostina Palmigiano; Theo Geisel; Fred Wolf; Demian Battaglia

doi:10.1038/nn.4569

journal article May 22, 2017

Flexible information routing by transient synchrony

Agostina Palmigiano Theo Geisel Fred Wolf Demian Battaglia

Nature Neuroscience Vol. 20 No. 7 pp. 1014-1022 · Springer Science and Business Media LLC

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References

66

[1]

A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information

BA Olshausen, CH Anderson, DC van Essen

The Journal of Neuroscience 1993 10.1523/jneurosci.13-11-04700.1993

[2]

Vogels, T.P. & Abbott, L.F. Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat. Neurosci. 12, 483–491 (2009). 10.1038/nn.2276

[3]

Zylberberg, A., Fernández Slezak, D., Roelfsema, P.R., Dehaene, S. & Sigman, M. The brain's router: a cortical network model of serial processing in the primate brain. PLoS Comput. Biol. 6, e1000765 (2010). 10.1371/journal.pcbi.1000765

[4]

Abeles, M., Hayon, G. & Lehmann, D. Modeling compositionality by dynamic binding of synfire chains. J. Comput. Neurosci. 17, 179–201 (2004). 10.1023/b:jcns.0000037682.18051.5f

[5]

Kumar, A., Rotter, S. & Aertsen, A. Conditions for propagating synchronous spiking and asynchronous firing rates in a cortical network model. J. Neurosci. 28, 5268–5280 (2008). 10.1523/jneurosci.2542-07.2008

[6]

Hahn, G., Bujan, A.F., Frégnac, Y., Aertsen, A. & Kumar, A. Communication through resonance in spiking neuronal networks. PLoS Comput. Biol. 10, e1003811–e1003816 (2014). 10.1371/journal.pcbi.1003811

[7]

Akam, T. & Kullmann, D.M. Oscillations and filtering networks support flexible routing of information. Neuron 67, 308–320 (2010). 10.1016/j.neuron.2010.06.019

[8]

Harnack, D., Ernst, U.A. & Pawelzik, K.R. A model for attentional information routing through coherence predicts biased competition and multistable perception. J. Neurophysiol. 114, 1593–1605 (2015). 10.1152/jn.01038.2014

[9]

A mechanism for cognitive dynamics: neuronal communication through neuronal coherence

Pascal Fries

Trends in Cognitive Sciences 2005 10.1016/j.tics.2005.08.011

[10]

High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention

Georgia G. Gregoriou, Stephen J. Gotts, Huihui Zhou et al.

Science 2009 10.1126/science.1171402

[11]

Grothe, I., Neitzel, S.D., Mandon, S. & Kreiter, A.K. Switching neuronal inputs by differential modulations of gamma-band phase-coherence. J. Neurosci. 32, 16172–16180 (2012). 10.1523/jneurosci.0890-12.2012

[12]

Burns, S.P., Xing, D. & Shapley, R.M. Is gamma-band activity in the local field potential of V1 cortex a “clock” or filtered noise? J. Neurosci. 31, 9658–9664 (2011). 10.1523/jneurosci.0660-11.2011

[13]

Xing, D. et al. Stochastic generation of gamma-band activity in primary visual cortex of awake and anesthetized monkeys. J. Neurosci. 32, 13873–13880a (2012). 10.1523/jneurosci.5644-11.2012

[14]

Jia, X., Tanabe, S. & Kohn, A. γ and the coordination of spiking activity in early visual cortex. Neuron 77, 762–774 (2013). 10.1016/j.neuron.2012.12.036

[15]

Ray, S. & Maunsell, J.H.R. Do gamma oscillations play a role in cerebral cortex? Trends Cogn. Sci. 19, 78–85 (2015). 10.1016/j.tics.2014.12.002

[16]

Ray, S. & Maunsell, J.H.R. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 67, 885–896 (2010). 10.1016/j.neuron.2010.08.004

[17]

Jia, X., Xing, D. & Kohn, A. No consistent relationship between gamma power and peak frequency in macaque primary visual cortex. J. Neurosci. 33, 17–25 (2013). 10.1523/jneurosci.1687-12.2013

[18]

Okun, M. et al. Diverse coupling of neurons to populations in sensory cortex. Nature 521, 511–515 (2015). 10.1038/nature14273

[19]

Brunel, N. & Hakim, V. Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput. 11, 1621–1671 (1999). 10.1162/089976699300016179

[20]

Brunel, N. & Wang, X.-J. What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J. Neurophysiol. 90, 415–430 (2003). 10.1152/jn.01095.2002

[21]

Bartos, M., Vida, I. & Jonas, P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8, 45–56 (2007). 10.1038/nrn2044

[22]

Roberts, M.J. et al. Robust gamma coherence between macaque V1 and V2 by dynamic frequency matching. Neuron 78, 523–536 (2013). 10.1016/j.neuron.2013.03.003

[23]

Bastos, A.M., Vezoli, J. & Fries, P. Communication through coherence with inter-areal delays. Curr. Opin. Neurobiol. 31, 173–180 (2015). 10.1016/j.conb.2014.11.001

[24]

Chakrabarti, S., Martinez-Vazquez, P. & Gail, A. Synchronization patterns suggest different functional organization in parietal reach region and dorsal premotor cortex. J. Neurophysiol. 112, 3138–3153 (2014). 10.1152/jn.00621.2013

[25]

Buschman, T.J. & Miller, E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860–1862 (2007). 10.1126/science.1138071

[26]

Measuring Information Transfer

Thomas Schreiber

Physical Review Letters 2000 10.1103/physrevlett.85.461

[27]

Wibral, M., Vicente, R. & Lizier, J.T. Directed Information Measures in Neuroscience (Springer, 2014). 10.1007/978-3-642-54474-3

[28]

Bosman, C.A. et al. Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75, 875–888 (2012). 10.1016/j.neuron.2012.06.037

[29]

Grothe, I. et al. Attention selectively gates afferent signal transmission to area V4. Preprint at https://doi.org/10.1101/019547 (2015). 10.1101/019547

[30]

Somers, D. & Kopell, N. Rapid synchronization through fast threshold modulation. Biol. Cybern. 68, 393–407 (1993). 10.1007/bf00198772

[31]

Mazzoni, A., Panzeri, S., Logothetis, N.K. & Brunel, N. Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons. PLoS Comput. Biol. 4, e1000239 (2008). 10.1371/journal.pcbi.1000239

[32]

Kreiter, A.K. & Singer, W. Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J. Neurosci. 16, 2381–2396 (1996). 10.1523/jneurosci.16-07-02381.1996

[33]

Ecker, A.S. et al. Decorrelated neuronal firing in cortical microcircuits. Science 327, 584–587 (2010). 10.1126/science.1179867

[34]

Canolty, R.T. et al. Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies. Proc. Natl. Acad. Sci. USA 107, 17356–17361 (2010). 10.1073/pnas.1008306107

[35]

Witt, A. et al. Controlling the oscillation phase through precisely timed closed-loop optogenetic stimulation: a computational study. Front. Neural Circuits 7, 49 (2013). 10.3389/fncir.2013.00049

[36]

Tiesinga, P.H. & Sejnowski, T.J. Mechanisms for phase shifting in cortical networks and their role in communication through coherence. Front. Hum. Neurosci. 4, 196 (2010). 10.3389/fnhum.2010.00196

[37]

Battaglia, D., Brunel, N. & Hansel, D. Temporal decorrelation of collective oscillations in neural networks with local inhibition and long-range excitation. Phys. Rev. Lett. 99, 238106 (2007). 10.1103/physrevlett.99.238106

[38]

Burkhalter, A. Many specialists for suppressing cortical excitation. Front. Neurosci. 2, 155–167 (2008). 10.3389/neuro.01.026.2008

[39]

Battaglia, D., Witt, A., Wolf, F. & Geisel, T. Dynamic effective connectivity of inter-areal brain circuits. PLoS Comput. Biol. 8, e1002438 (2012). 10.1371/journal.pcbi.1002438

[40]

Dotson, N.M., Salazar, R.F. & Gray, C.M. Frontoparietal correlation dynamics reveal interplay between integration and segregation during visual working memory. J. Neurosci. 34, 13600–13613 (2014). 10.1523/jneurosci.1961-14.2014

[41]

Osborne, L.C., Palmer, S.E., Lisberger, S.G. & Bialek, W. The neural basis for combinatorial coding in a cortical population response. J. Neurosci. 28, 13522–13531 (2008). 10.1523/jneurosci.4390-08.2008

[42]

Rigotti, M. et al. The importance of mixed selectivity in complex cognitive tasks. Nature 497, 585–590 (2013). 10.1038/nature12160

[43]

Harris, K.D., Csicsvari, J., Hirase, H., Dragoi, G. & Buzsáki, G. Organization of cell assemblies in the hippocampus. Nature 424, 552–556 (2003). 10.1038/nature01834

[44]

Buzsáki, G. Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68, 362–385 (2010). 10.1016/j.neuron.2010.09.023

[45]

Salazar, R.F., Dotson, N.M., Bressler, S.L. & Gray, C.M. Content-specific fronto-parietal synchronization during visual working memory. Science 338, 1097–1100 (2012). 10.1126/science.1224000

[46]

Lisman, J. The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 15, 913–922 (2005). 10.1002/hipo.20121

[47]

Colgin, L.L. et al. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462, 353–357 (2009). 10.1038/nature08573

[48]

Cannon, J. et al. Neurosystems: brain rhythms and cognitive processing. Eur. J. Neurosci. 39, 705–719 (2014). 10.1111/ejn.12453

[49]

Hipp, J.F., Hawellek, D.J., Corbetta, M., Siegel, M. & Engel, A.K. Large-scale cortical correlation structure of spontaneous oscillatory activity. Nat. Neurosci. 15, 884–890 (2012). 10.1038/nn.3101

[50]

Bastos, A.M. et al. Visual areas exert feedforward and feedback influences through distinct frequency channels. Neuron 85, 390–401 (2015). 10.1016/j.neuron.2014.12.018

Showing 50 of 66 references

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Published: May 22, 2017
Vol/Issue: 20(7)
Pages: 1014-1022
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Cite This Article

Agostina Palmigiano, Theo Geisel, Fred Wolf, et al. (2017). Flexible information routing by transient synchrony. Nature Neuroscience, 20(7), 1014-1022. https://doi.org/10.1038/nn.4569

Flexible information routing by transient synchrony

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