1932

Abstract

Gamma oscillations (30–70 Hz) have been hypothesized to play a role in cortical function. Most of the proposed mechanisms involve rhythmic modulation of neuronal excitability at gamma frequencies, leading to modulation of spike timing relative to the rhythm. I first show that the gamma band could be more privileged than other frequencies in observing spike–field interactions even in the absence of genuine gamma rhythmicity and discuss several biases in spike–gamma phase estimation. I then discuss the expected spike–gamma phase according to several hypotheses. Inconsistent with the phase-coding hypothesis (but not with others), the spike–gamma phase does not change with changes in stimulus intensity or attentional state, with spikes preferentially occurring 2–4 ms before the trough, but with substantial variability. However, this phase relationship is expected even when gamma is a byproduct of excitatory–inhibitory interactions. Given that gamma occurs in short bursts, I argue that the debate over the role of gamma is a matter of semantics.

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2022-09-15
2024-03-28
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Literature Cited

  1. Ainsworth M, Lee S, Cunningham MO, Traub RD, Kopell NJ, Whittington MA. 2012. Rates and rhythms: a synergistic view of frequency and temporal coding in neuronal networks. Neuron 75:4572–83
    [Google Scholar]
  2. Akam TE, Kullmann DM. 2010. Oscillations and filtering networks support flexible routing of information. Neuron 67:2308–20
    [Google Scholar]
  3. Akam TE, Kullmann DM. 2012. Efficient “communication through coherence” requires oscillations structured to minimize interference between signals. PLOS Comput. Biol. 8:11e1002760
    [Google Scholar]
  4. Akam TE, Kullmann DM. 2014. Oscillatory multiplexing of population codes for selective communication in the mammalian brain. Nat. Rev. Neurosci. 15:2111–22
    [Google Scholar]
  5. Atallah BV, Scanziani M. 2009. Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62:566–77
    [Google Scholar]
  6. Azouz R, Gray CM. 2003. Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37:3513–23
    [Google Scholar]
  7. Bartoli E, Bosking W, Chen Y, Li Y, Sheth SA et al. 2019. Functionally distinct gamma range activity revealed by stimulus tuning in human visual cortex. Curr. Biol. 29:203345–58.e7
    [Google Scholar]
  8. Bartoli E, Bosking W, Foster BL. 2020. Seeing visual gamma oscillations in a new light. Trends Cogn. Sci. 24:7501–3
    [Google Scholar]
  9. Bartos M, Vida I, Jonas P 2007. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8:145–56
    [Google Scholar]
  10. Belitski A, Gretton A, Magri C, Murayama Y, Montemurro MA et al. 2008. Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J. Neurosci. 28:5696–709
    [Google Scholar]
  11. Berens P. 2009. CircStat: a MATLAB toolbox for circular statistics. J. Stat. Softw. 31:i10
    [Google Scholar]
  12. Berens P, Keliris GA, Ecker AS, Logothetis NK, Tolias AS. 2008. Comparing the feature selectivity of the gamma-band of the local field potential and the underlying spiking activity in primate visual cortex. Front. Syst. Neurosci. 2:2
    [Google Scholar]
  13. Besserve M, Lowe SC, Logothetis NK, Schölkopf B, Panzeri S. 2015. Shifts of gamma phase across primary visual cortical sites reflect dynamic stimulus-modulated information transfer. PLOS Biol 13:9e1002257
    [Google Scholar]
  14. Bhatia A, Moza S, Bhalla US 2019. Precise excitation-inhibition balance controls gain and timing in the hippocampus. eLife 8:e43415
    [Google Scholar]
  15. Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP. 2010. Chronux: a platform for analyzing neural signals. J. Neurosci. Methods 192:1146–51
    [Google Scholar]
  16. Börgers C, Kopell N. 2005. Effects of noisy drive on rhythms in networks of excitatory and inhibitory neurons. Neural Comput 17:3557–608
    [Google Scholar]
  17. Börgers C, Kopell NJ. 2008. Gamma oscillations and stimulus selection. Neural Comput 20:2383–414
    [Google Scholar]
  18. Bosman CA, Schoffelen J-M, Brunet N, Oostenveld R, Bastos AM et al. 2012. Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75:5875–88
    [Google Scholar]
  19. Brunet N, Bosman CA, Roberts M, Oostenveld R, Womelsdorf T et al. 2013. Visual cortical gamma-band activity during free viewing of natural images. Cereb. Cortex 25:4918–26
    [Google Scholar]
  20. Buffalo EA, Fries P, Landman R, Buschman TJ, Desimone R. 2011. Laminar differences in gamma and alpha coherence in the ventral stream. PNAS 108:2711262–67
    [Google Scholar]
  21. Burns SP, Xing D, Shapley RM. 2011. Is gamma-band activity in the local field potential of V1 cortex a “clock” or filtered noise?. J. Neurosci. 31:269658–64
    [Google Scholar]
  22. Burns SP, Xing D, Shelley MJ, Shapley RM. 2010. Searching for autocoherence in the cortical network with a time-frequency analysis of the local field potential. J. Neurosci. 30:114033–47
    [Google Scholar]
  23. Buzsáki G, Anastassiou CA, Koch C. 2012. The origin of extracellular fields and currents—EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 13:6407–20
    [Google Scholar]
  24. Buzsáki G, Chrobak JJ. 1995. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr. Opin. Neurobiol. 5:504–10
    [Google Scholar]
  25. Buzsáki G, Wang X-J. 2012. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35:203–25
    [Google Scholar]
  26. Cardin JA. 2016. Snapshots of the brain in action: local circuit operations through the lens of γ oscillations. J. Neurosci. 36:4110496–504
    [Google Scholar]
  27. Chalk M, Herrero JL, Gieselmann MA, Delicato LS, Gotthardt S, Thiele A. 2010. Attention reduces stimulus-driven gamma frequency oscillations and spike field coherence in V1. Neuron 66:1114–25
    [Google Scholar]
  28. Chance FS, Abbott LF, Reyes AD. 2002. Gain modulation from background synaptic input. Neuron 35:773–82
    [Google Scholar]
  29. Chandran KS S, Mishra A, Shirhatti V, Ray S 2016. Comparison of matching pursuit algorithm with other signal processing techniques for computation of the time-frequency power spectrum of brain signals. J. Neurosci. 36:123399–408
    [Google Scholar]
  30. Chandran KS S, Seelamantula CS, Ray S 2017. Duration analysis using matching pursuit algorithm reveals longer bouts of gamma rhythm. J. Neurophysiol. 119:3808–21
    [Google Scholar]
  31. Churchland MM, Yu BM, Cunningham JP, Sugrue LP, Cohen MR et al. 2010. Stimulus onset quenches neural variability: a widespread cortical phenomenon. Nat. Neurosci. 13:3369–78
    [Google Scholar]
  32. Cohen MR, Kohn A. 2011. Measuring and interpreting neuronal correlations. Nat. Neurosci. 14:7811–19
    [Google Scholar]
  33. Cohen MR, Maunsell JH. 2009. Attention improves performance primarily by reducing interneuronal correlations. Nat. Neurosci. 12:1594–600
    [Google Scholar]
  34. Cole SR, Voytek B. 2017. Brain oscillations and the importance of waveform shape. Trends Cogn. Sci. 21:2137–49
    [Google Scholar]
  35. Csicsvari J, Henze DA, Jamieson B, Harris KD, Sirota A et al. 2003. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 90:21314–23
    [Google Scholar]
  36. Das A, Ray S. 2018. Effect of stimulus contrast and visual attention on spike-gamma phase relationship in macaque primary visual cortex. Front. Comput. Neurosci. 12:66
    [Google Scholar]
  37. Denève S, Machens CK. 2016. Efficient codes and balanced networks. Nat. Neurosci. 19:3375–82
    [Google Scholar]
  38. Doelling KB, Assaneo MF. 2021. Neural oscillations are a start toward understanding brain activity rather than the end. PLOS Biol. 19:5e3001234
    [Google Scholar]
  39. Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W et al. 1988. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol. Cybern. 60:2121–30
    [Google Scholar]
  40. Einevoll GT, Kayser C, Logothetis NK, Panzeri S. 2013. Modelling and analysis of local field potentials for studying the function of cortical circuits. Nat. Rev. Neurosci. 14:11770–85
    [Google Scholar]
  41. Engel AK, Konig P, Kreiter A, Singer W. 1991a. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252:50091177–79
    [Google Scholar]
  42. Engel AK, Kreiter AK, König P, Singer W. 1991b. Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. PNAS 88:146048–52
    [Google Scholar]
  43. Feingold J, Gibson DJ, DePasquale B, Graybiel AM. 2015. Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks. PNAS 112:4413687–92
    [Google Scholar]
  44. Ferguson KA, Cardin JA. 2020. Mechanisms underlying gain modulation in the cortex. Nat. Rev. Neurosci. 21:280–92
    [Google Scholar]
  45. Friedman-Hill S, Maldonado PE, Gray CM. 2000. Dynamics of striate cortical activity in the alert macaque: I. Incidence and stimulus-dependence of gamma-band neuronal oscillations. Cereb. Cortex 10:1105–16
    [Google Scholar]
  46. Fries P. 2005. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9:10474–80
    [Google Scholar]
  47. Fries P. 2009. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32:209–24
    [Google Scholar]
  48. Fries P. 2015. Rhythms for cognition: communication through coherence. Neuron 88:1220–35
    [Google Scholar]
  49. Fries P, Nikolić D, Singer W. 2007. The gamma cycle. Trends Neurosci 30:7309–16
    [Google Scholar]
  50. Fries P, Reynolds JH, Rorie AE, Desimone R. 2001. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–63
    [Google Scholar]
  51. Fries P, Womelsdorf T, Oostenveld R, Desimone R. 2008. The effects of visual stimulation and selective visual attention on rhythmic neuronal synchronization in macaque area V4. J. Neurosci. 28:184823–35
    [Google Scholar]
  52. Galindo-Leon EE, Liu RC 2010. Predicting stimulus-locked single unit spiking from cortical local field potentials. J. Comput. Neurosci. 29:3581–97
    [Google Scholar]
  53. Gielen S, Krupa M, Zeitler M. 2010. Gamma oscillations as a mechanism for selective information transmission. Biol. Cybern. 103:2151–65
    [Google Scholar]
  54. Gieselmann MA, Thiele A. 2008. Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1. Eur. J. Neurosci. 28:447–59
    [Google Scholar]
  55. Grasse DW, Moxon KA. 2010. Correcting the bias of spike field coherence estimators due to a finite number of spikes. J. Neurophysiol. 104:1548–58
    [Google Scholar]
  56. Gray CM. 1999. The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24:131–47111–25
    [Google Scholar]
  57. Gray CM, Engel AK, König P, Singer W. 1992. Synchronization of oscillatory neuronal responses in cat striate cortex: temporal properties. Vis. Neurosci. 8:4337–47
    [Google Scholar]
  58. Gray CM, König P, Engel AK, Singer W. 1989. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:6213334–37
    [Google Scholar]
  59. Gray CM, Singer W. 1989. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. PNAS 86:51698–702
    [Google Scholar]
  60. Gregoriou GG, Gotts SJ, Zhou H, Desimone R. 2009. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324:1207–10
    [Google Scholar]
  61. Grothe I, Neitzel SD, Mandon S, Kreiter AK. 2012. Switching neuronal inputs by differential modulations of gamma-band phase-coherence. J. Neurosci. 32:4616172–80
    [Google Scholar]
  62. Hadjipapas A, Adjamian P, Swettenham JB, Holliday IE, Barnes GR. 2007. Stimuli of varying spatial scale induce gamma activity with distinct temporal characteristics in human visual cortex. NeuroImage 35:518–30
    [Google Scholar]
  63. Haider B, Duque A, Hasenstaub AR, McCormick DA. 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26:4535–45
    [Google Scholar]
  64. Haider B, McCormick DA. 2009. Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62:2171–89
    [Google Scholar]
  65. Hasenstaub A, Otte S, Callaway E. 2016. Cell type-specific control of spike timing by gamma-band oscillatory inhibition. Cereb. Cortex 26:2797–806
    [Google Scholar]
  66. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA. 2005. Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423–35
    [Google Scholar]
  67. Havenith MN, Yu S, Biederlack J, Chen N-H, Singer W, Nikolić D. 2011. Synchrony makes neurons fire in sequence, and stimulus properties determine who is ahead. J. Neurosci. 31:238570–84
    [Google Scholar]
  68. Henrie JA, Shapley R. 2005. LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol. 94:479–90
    [Google Scholar]
  69. Henze DA, Borhegyi Z, Csicsvari J, Mamiya A, Harris KD, Buzsáki G. 2000. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J. Neurophysiol. 84:1390–400
    [Google Scholar]
  70. Hermes D, Miller KJ, Wandell BA, Winawer J. 2015. Stimulus dependence of gamma oscillations in human visual cortex. Cereb. Cortex 25:92951–59
    [Google Scholar]
  71. Hu H, Gan J, Jonas P 2014. Fast-spiking, parvalbumin+ GABAergic interneurons: from cellular design to microcircuit function. Science 345:61961255263
    [Google Scholar]
  72. Isaacson JS, Scanziani M. 2011. How inhibition shapes cortical activity. Neuron 72:2231–43
    [Google Scholar]
  73. Jadi MP, Sejnowski TJ. 2014. Regulating cortical oscillations in an inhibition-stabilized network. Proc. IEEE 102:5830–42
    [Google Scholar]
  74. Jia X, Kohn A. 2011. Gamma rhythms in the brain. PLOS Biol 9:4e1001045
    [Google Scholar]
  75. Jia X, Smith MA, Kohn A. 2011. Stimulus selectivity and spatial coherence of gamma components of the local field potential. J. Neurosci. 31:259390–403
    [Google Scholar]
  76. Jia X, Tanabe S, Kohn A. 2013a. Gamma and the coordination of spiking activity in early visual cortex. Neuron 77:4762–74
    [Google Scholar]
  77. Jia X, Xing D, Kohn A. 2013b. No consistent relationship between gamma power and peak frequency in macaque primary visual cortex. J. Neurosci. 33:117–25
    [Google Scholar]
  78. Jones SR. 2016. When brain rhythms aren't “rhythmic”: implication for their mechanisms and meaning. Curr. Opin. Neurobiol. 40:72–80
    [Google Scholar]
  79. Kajikawa Y, Schroeder CE. 2011. How local is the local field potential?. Neuron 72:5847–58
    [Google Scholar]
  80. Kanth ST, Ray S 2020. Electrocorticogram (ECoG) is highly informative in primate visual cortex. J. Neurosci. 40:122430–44
    [Google Scholar]
  81. Kayser C, Salazar RF, Konig P. 2003. Responses to natural scenes in cat V1. J. Neurophysiol. 90:31910–20
    [Google Scholar]
  82. Krishnakumaran R, Raees M, Ray S 2022. Shape analysis of gamma rhythm supports a superlinear inhibitory regime in an inhibition-stabilized network. PLOS Comput. Biol. 18:2e1009886
    [Google Scholar]
  83. Li Z, Cui D, Li X. 2016. Unbiased and robust quantification of synchronization between spikes and local field potential. J. Neurosci. Methods 269:33–38
    [Google Scholar]
  84. Lowet E, Roberts MJ, Bonizzi P, Karel J, De Weerd P. 2016. Quantifying neural oscillatory synchronization: a comparison between spectral coherence and phase-locking value approaches. PLOS ONE 11:1e0146443
    [Google Scholar]
  85. Lowet E, Roberts MJ, Gips B, De Weerd P, Peter A 2017. A quantitative theory of gamma synchronization in macaque V1. eLife 6:e26642
    [Google Scholar]
  86. Lundqvist M, Rose J, Herman P, Brincat SL, Buschman TJ, Miller EK. 2016. Gamma and beta bursts underlie working memory. Neuron 90:1152–64
    [Google Scholar]
  87. Mallat SG, Zhang Z. 1993. Matching pursuits with time-frequency dictionaries. IEEE Trans. Signal Process. 41:3397–415
    [Google Scholar]
  88. Martin KAC, Schröder S. 2016. Phase locking of multiple single neurons to the local field potential in cat V1. J. Neurosci. 36:82494–502
    [Google Scholar]
  89. Mayo JP, Maunsell JHR. 2016. Graded neuronal modulations related to visual spatial attention. J. Neurosci. 36:195353–61
    [Google Scholar]
  90. Mazzoni A, Lindén H, Cuntz H, Lansner A, Panzeri S, Einevoll GT. 2015. Computing the local field potential (LFP) from integrate-and-fire network models. PLOS Comput. Biol. 11:12e1004584
    [Google Scholar]
  91. Mitra PP, Pesaran B. 1999. Analysis of dynamic brain imaging data. Biophys. J. 76:691–708
    [Google Scholar]
  92. Mitzdorf U. 1985. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65:37–100
    [Google Scholar]
  93. Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S. 2008. Phase-of-firing coding of natural visual stimuli in primary visual cortex. Curr. Biol. 18:375–80
    [Google Scholar]
  94. Murty DV, Manikandan K, Kumar WS, Ramesh RG, Purokayastha S et al. 2021. Stimulus-induced gamma rhythms are weaker in human elderly with mild cognitive impairment and Alzheimer's disease. eLife 10:e61666
    [Google Scholar]
  95. Murty DVPS, Shirhatti V, Ravishankar P, Ray S 2018. Large visual stimuli induce two distinct gamma oscillations in primate visual cortex. J. Neurosci. 38:112730–44
    [Google Scholar]
  96. Ni J, Wunderle T, Lewis CM, Desimone R, Diester I, Fries P. 2016. Gamma-rhythmic gain modulation. Neuron 92:1240–51
    [Google Scholar]
  97. O'Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:3317–30
    [Google Scholar]
  98. Okun M. 2017. Artefactual origin of biphasic cortical spike-LFP correlation. J. Comput. Neurosci. 42:131–35
    [Google Scholar]
  99. Okun M, Lampl I. 2008. Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat. Neurosci. 11:5535–37
    [Google Scholar]
  100. Okun M, Naim A, Lampl I. 2010. The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J. Neurosci. 30:124440–48
    [Google Scholar]
  101. Palmigiano A, Geisel T, Wolf F, Battaglia D. 2017. Flexible information routing by transient synchrony. Nat. Neurosci. 20:71014–22
    [Google Scholar]
  102. Pesaran B, Pezaris JS, Sahani M, Mitra PP, Andersen RA. 2002. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat. Neurosci. 5:8805–11
    [Google Scholar]
  103. Pesaran B, Vinck M, Einevoll GT, Sirota A, Fries P et al. 2018. Investigating large-scale brain dynamics using field potential recordings: analysis and interpretation. Nat. Neurosci. 21:7903–19
    [Google Scholar]
  104. Prakash SS, Das A, Kanth ST, Mayo JP, Ray S 2021. Decoding of attentional state using high-frequency local field potential is as accurate as using spikes. Cereb. Cortex 31:94314–28
    [Google Scholar]
  105. Rasch MJ, Gretton A, Murayama Y, Maass W, Logothetis NK. 2008. Inferring spike trains from local field potentials. J. Neurophysiol. 99:1461–76
    [Google Scholar]
  106. Ray S. 2015. Challenges in the quantification and interpretation of spike-LFP relationships. Curr. Opin. Neurobiol. 31:111–18
    [Google Scholar]
  107. Ray S, Hsiao SS, Crone NE, Franaszczuk PJ, Niebur E. 2008. Effect of stimulus intensity on the spike-local field potential relationship in the secondary somatosensory cortex. J. Neurosci. 28:7334–43
    [Google Scholar]
  108. Ray S, Maunsell JHR. 2010. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 67:5885–96
    [Google Scholar]
  109. Ray S, Maunsell JHR. 2011a. Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLOS Biol 9:4e1000610
    [Google Scholar]
  110. Ray S, Maunsell JHR. 2011b. Network rhythms influence the relationship between spike-triggered local field potential and functional connectivity. J. Neurosci. 31:3512674–82
    [Google Scholar]
  111. Ray S, Maunsell JHR. 2015. Do gamma oscillations play a role in cerebral cortex?. Trends Cogn. Sci. 19:278–85
    [Google Scholar]
  112. Rohenkohl G, Bosman CA, Fries P. 2018. Gamma synchronization between V1 and V4 improves behavioral performance. Neuron 100:4953–63.e3
    [Google Scholar]
  113. Rols G, Tallon-Baudry C, Girard P, Bertrand O, Bullier J. 2001. Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey. Vis. Neurosci. 18:527–40
    [Google Scholar]
  114. Schmolesky MT, Wang Y, Hanes DP, Thompson KG, Leutgeb S et al. 1998. Signal timing across the macaque visual system. J. Neurophysiol. 79:63272–78
    [Google Scholar]
  115. Schneider M, Broggini AC, Dann B, Tzanou A, Uran C et al. 2021. A mechanism for inter-areal coherence through communication based on connectivity and oscillatory power. Neuron 109:244050–67.e12
    [Google Scholar]
  116. Shadlen MN, Movshon JA. 1999. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24:167–77111–25
    [Google Scholar]
  117. Sherman MA, Lee S, Law R, Haegens S, Thorn CA et al. 2016. Neural mechanisms of transient neocortical beta rhythms: converging evidence from humans, computational modeling, monkeys, and mice. PNAS 113:33E4885–94
    [Google Scholar]
  118. Shirhatti V, Borthakur A, Ray S. 2016. Effect of reference scheme on power and phase of the local field potential. Neural Comput. 28:5882–913
    [Google Scholar]
  119. Shirhatti V, Ray S. 2018. Long-wavelength (reddish) hues induce unusually large gamma oscillations in the primate primary visual cortex. PNAS 115:174489–94
    [Google Scholar]
  120. Shu Y, Hasenstaub A, McCormick DA. 2003. Turning on and off recurrent balanced cortical activity. Nature 423:288–93
    [Google Scholar]
  121. Singer W. 1999. Neuronal synchrony: a versatile code for the definition of relations?. Neuron 24:149–65111–25
    [Google Scholar]
  122. Singer W, Gray CM. 1995. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18:555–86
    [Google Scholar]
  123. Smith MA, Kohn A. 2008. Spatial and temporal scales of neuronal correlation in primary visual cortex. J. Neurosci. 28:12591–603
    [Google Scholar]
  124. Sohal VS. 2016. How close are we to understanding what (if anything) γ oscillations do in cortical circuits?. J. Neurosci. 36:4110489–95
    [Google Scholar]
  125. Sohal VS, Rubenstein JLR. 2019. Excitation-inhibition balance as a framework for investigating mechanisms in neuropsychiatric disorders. Mol. Psychiatry 24:91248–57
    [Google Scholar]
  126. Srinath R, Ray S. 2014. Effect of amplitude correlations on coherence in the local field potential. J. Neurophysiol. 112:4741–51
    [Google Scholar]
  127. Tiesinga PH, Fellous J-M, Salinas E, Jose JV, Sejnowski TJ. 2004. Inhibitory synchrony as a mechanism for attentional gain modulation. J. Physiol. 98:296–314
    [Google Scholar]
  128. Tiesinga PH, Sejnowski TJ. 2009. Cortical enlightenment: Are attentional gamma oscillations driven by ING or PING?. Neuron 63:6727–32
    [Google Scholar]
  129. Tiesinga PH, Sejnowski TJ. 2010. Mechanisms for phase shifting in cortical networks and their role in communication through coherence. Front. Hum. Neurosci. 4:196
    [Google Scholar]
  130. Traub RD, Whittington MA, Stanford IM, Jefferys JGR. 1996. A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:6601621–24
    [Google Scholar]
  131. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL. 1997. Paradoxical effects of external modulation of inhibitory interneurons. J. Neurosci. 17:114382–88
    [Google Scholar]
  132. Uhlhaas PJ, Singer W. 2010. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 11:2100–13
    [Google Scholar]
  133. Uhlhaas PJ, Singer W. 2012. Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron 75:6963–80
    [Google Scholar]
  134. van Ede F, Quinn AJ, Woolrich MW, Nobre AC. 2018. Neural oscillations: sustained rhythms or transient burst-events?. Trends Neurosci. 41:7415–17
    [Google Scholar]
  135. van Pelt S, Fries P. 2013. Visual stimulus eccentricity affects human gamma peak frequency. NeuroImage 78:439–47
    [Google Scholar]
  136. Veit J, Hakim R, Jadi MP, Sejnowski TJ, Adesnik H. 2017. Cortical gamma band synchronization through somatostatin interneurons. Nat. Neurosci. 20:7951–59
    [Google Scholar]
  137. Vinck M, Battaglia FP, Womelsdorf T, Pennartz C. 2012. Improved measures of phase-coupling between spikes and the local field potential. J. Comput. Neurosci. 33:153–75
    [Google Scholar]
  138. Vinck M, Lima B, Womelsdorf T, Oostenveld R, Singer W et al. 2010a. Gamma-phase shifting in awake monkey visual cortex. J. Neurosci. 30:41250–57
    [Google Scholar]
  139. Vinck M, van Wingerden M, Womelsdorf T, Fries P, Pennartz CMA. 2010b. The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization. NeuroImage 51:1112–22
    [Google Scholar]
  140. Vinck M, Womelsdorf T, Buffalo EA, Desimone R, Fries P. 2013. Attentional modulation of cell-class-specific gamma-band synchronization in awake monkey area V4. Neuron 80:41077–89
    [Google Scholar]
  141. Vogels TP, Abbott LF. 2009. Gating multiple signals through detailed balance of excitation and inhibition in spiking networks. Nat. Neurosci. 12:4483–91
    [Google Scholar]
  142. Wang X-J. 2010. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 90:31195–268
    [Google Scholar]
  143. Wehr M, Zador AM. 2003. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:6965442–46
    [Google Scholar]
  144. Welle CG, Contreras D. 2016. Sensory-driven and spontaneous gamma oscillations engage distinct cortical circuitry. J. Neurophysiol. 115:41821–35
    [Google Scholar]
  145. Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH. 2000. Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int. J. Psychophysiol. 38:315–36
    [Google Scholar]
  146. Wilson HR, Cowan JD. 1972. Excitatory and inhibitory interactions in localized populations of model neurons. Biophys. J. 12:11–24
    [Google Scholar]
  147. Womelsdorf T, Schoffelen J-M, Oostenveld R, Singer W, Desimone R et al. 2007. Modulation of neuronal interactions through neuronal synchronization. Science 316:58311609–12
    [Google Scholar]
  148. Xing D, Shen Y, Burns S, Yeh C-I, Shapley R, Li W. 2012a. Stochastic generation of gamma-band activity in primary visual cortex of awake and anesthetized monkeys. J. Neurosci. 32:4013873–80
    [Google Scholar]
  149. Xing D, Yeh C-I, Burns S, Shapley RM. 2012b. Laminar analysis of visually evoked activity in the primary visual cortex. PNAS 109:3413871–76
    [Google Scholar]
  150. Zandvakili A, Kohn A. 2015. Coordinated neuronal activity enhances corticocortical communication. Neuron 87:4827–39
    [Google Scholar]
  151. Zanos TP, Mineault PJ, Pack CC. 2011. Removal of spurious correlations between spikes and local field potentials. J. Neurophysiol. 105:1474–86
    [Google Scholar]
  152. Zhou S, Yu Y. 2018. Synaptic E-I balance underlies efficient neural coding. Front. Neurosci. 12:46
    [Google Scholar]
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