Skip to content
naulon

No retraction, correction or concern found when last checked on Nov 1, 2026.

Gamma and beta bursts during working memory readout suggest roles in its volitional control

Mikael Lundqvist, Pawel Herman, Melissa R. Warden and 2 more

Nature Communications · 2018 · CC BY

doi:10.1101/122598

Abstract

Working memory (WM) activity is not as stationary or sustained as previously thought. There are brief bursts of gamma (~50–120 Hz) and beta (~20–35 Hz) oscillations, the former linked to stimulus information in spiking. We examined these dynamics in relation to readout and control mechanisms of WM. Monkeys held sequences of two objects in WM to match to subsequent sequences. Changes in beta and gamma bursting suggested their distinct roles. In anticipation of having to use an object for the match decision, there was an increase in gamma and spiking information about that object and reduced beta bursting. This readout signal was only seen before relevant test objects, and was related to premotor activity. When the objects were no longer needed, beta increased and gamma decreased together with object spiking information. Deviations from these dynamics predicted behavioral errors. Thus, beta could regulate gamma and the information in WM.

References 44

  1. 1.

    Fuster JM, Alexander GE. Neuron activity related to short-term memory. Science. 1971;173:652-654.

    Not in our library10.1126/science.173.3997.652

  2. 2.

    Funahashi S, Bruce CJ, Goldman-Rakic PS. Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J. Neurophysiol. 1989;61:331-349.

    Not in our library10.1152/jn.1989.61.2.331

  3. 3.

    Goldman-Rakic PS. Cellular basis of working memory. Neuron. 1995;14:477-485.

    Not in our library10.1016/0896-6273(95)90304-6

  4. 4.

    Miller EK, Erickson CA, Desimone R. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J. Neurosci. 1996;16:5154-5167.

    Not in our library10.1523/jneurosci.16-16-05154.1996

  5. 5.

    Amit DJ, Brunel N. Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. Cereb. Cortex. 1997;7:237-252.

    Not in our library10.1093/cercor/7.3.237

  6. 6.

    Lundqvist M, et al. Gamma and beta bursts underlie working memory. Neuron. 2016;90:152-164.

    Not in our library10.1016/j.neuron.2016.02.028

  7. 7.

    Lundqvist M, Herman P, Lansner A. Theta and gamma power increases and alpha/beta power decreases with memory load in an attractor network model. J. Cogn. Neurosci. 2011;23:3008-3020.

    Not in our library10.1162/jocn_a_00029

  8. 8.

    Warden MR, Miller EK. The representation of multiple objects in prefrontal neuronal delay activity. Cereb. Cortex. 2007;17(suppl 1):i41-i50.

    Not in our library10.1093/cercor/bhm070

  9. 9.

    Warden MR, Miller EK. Task-dependent changes in short-term memory in the prefrontal cortex. J. Neurosci. 2010;30:15801-15810.

    Not in our library10.1523/jneurosci.1569-10.2010

  10. 10.

    Wimmer K, Ramon M, Pasternak T, Compte A. Transitions between multiband oscillatory patterns characterize memory-guided perceptual decisions in prefrontal circuits. J. Neurosci. 2016;36:489-505.

    Not in our library10.1523/jneurosci.3678-15.2016

  11. 11.

    Rainer G, Miller EK. Timecourse of object‐related neural activity in the primate prefrontal cortex during a short‐term memory task. Eur. J. Neurosci. 2002;15:1244-1254.

    Not in our library10.1046/j.1460-9568.2002.01958.x

  12. 12.

    Hussar C, Pasternak T. Trial-to-trial variability of the prefrontal neurons reveals the nature of their engagement in a motion discrimination task. Proc. Natl Acad. Sci. USA. 2010;107:21842-21847.

    Not in our library10.1073/pnas.1009956107

  13. 13.

    Zhou X, et al. Neural correlates of working memory development in adolescent primates. Nat. Commun. 2016;7:13423.

    Not in our library10.1038/ncomms13423

  14. 14.

    Meyers EM, Qi XL, Constantinidis C. Incorporation of new information into prefrontal cortical activity after learning working memory tasks. Proc. Natl Acad. Sci. USA. 2012;109:4651-4656.

    Not in our library10.1073/pnas.1201022109

  15. 15.

    Haegens S, Nácher V, Luna R, Romo R, Jensen O. α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc. Natl Acad. Sci. USA. 2011;108:19377-19382.

    Not in our library10.1073/pnas.1117190108

  16. 16.

    Klimesch W, Sauseng P, Hanslmayr S. EEG alpha oscillations: the inhibition–timing hypothesis. Brain Res. Rev. 2007;53:63-88.

    Not in our library10.1016/j.brainresrev.2006.06.003

  17. 17.

    Ketz NA, Jensen O, O’Reilly RC. Thalamic pathways underlying prefrontal cortex–medial temporal lobe oscillatory interactions. Trends Neurosci. 2015;38:3-12.

    Not in our library10.1016/j.tins.2014.09.007

  18. 18.

    Parnaudeau S, et al. Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition. Neuron. 2013;77:1151-1162.

    Not in our library10.1016/j.neuron.2013.01.038

  19. 19.

    Gray CM, Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl Acad. Sci. USA. 1989;86:1698-1702.

    Not in our library10.1073/pnas.86.5.1698

  20. 20.

    Swann N, et al. Intracranial EEG reveals a time-and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J. Neurosci. 2009;29:12675-12685.

    Not in our library10.1523/jneurosci.3359-09.2009

  21. 21.

    Lundqvist M, Compte A, Lansner A. Bistable, irregular firing and population oscillations in a modular attractor memory network. PLoS Comput. Biol. 2010;6:e1000803.

    Not in our library10.1371/journal.pcbi.1000803

  22. 22.

    Brovelli A, et al. Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc. Natl Acad. Sci. USA. 2004;101:9849-9854.

    Not in our library10.1073/pnas.0308538101

  23. 23.

    Pfurtscheller G, Stancak A, Neuper C. Post-movement beta synchronization. A correlate of an idling motor area? Electroencephalogr. Clin. Neurophysiol. 1996;98:281-293.

    Not in our library10.1016/0013-4694(95)00258-8

  24. 24.

    Feingold J, Gibson DJ, DePasquale B, Graybiel AM. Bursts of beta oscillation differentiate postperformance activity in the striatum and motor cortex of monkeys performing movement tasks. Proc. Natl Acad. Sci. USA. 2015;112:13687-13692.

    Not in our library10.1073/pnas.1517629112

  25. 25.

    Engel AK, Fries P. Beta-band oscillations—signalling the status quo? Curr. Opin. Neurobiol. 2010;20:156-165.

    Not in our library10.1016/j.conb.2010.02.015

  26. 26.

    Fisch L, et al. Neural “ignition”: enhanced activation linked to perceptual awareness in human ventral stream visual cortex. Neuron. 2009;64:562-574.

    Not in our library10.1016/j.neuron.2009.11.001

  27. 27.

    Popov T, Kastner S, Jensen O. FEF-controlled alpha delay activity precedes stimulus-induced gamma-band activity in visual cortex. J. Neurosci. 2017;37:4117-4127.

    Not in our library10.1523/jneurosci.3015-16.2017

  28. 28.

    Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH. Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int. J. Psychophysiol. 2000;38:315-336.

    Not in our library10.1016/s0167-8760(00)00173-2

  29. 29.
  30. 30.

    Kramer MA, et al. Rhythm generation through period concatenation in rat somatosensory cortex. PLoS Comput. Biol. 2008;4:e1000169.

    Not in our library10.1371/journal.pcbi.1000169

  31. 31.
  32. 32.

    Durstewitz D, Seamans JK. Beyond bistability: biophysics and temporal dynamics of working memory. Neuroscience. 2006;139:119-133.

    Not in our library10.1016/j.neuroscience.2005.06.094

  33. 33.

    Barak O, Sussillo D, Romo R, Tsodyks M, Abbott LF. From fixed points to chaos: three models of delayed discrimination. Prog. Neurobiol. 2013;103:214-222.

    Not in our library10.1016/j.pneurobio.2013.02.002

  34. 34.
  35. 35.

    Chafee MV, Goldman-Rakic PS. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memorytask. J. Neurophysiol. 1998;79:2919-2940.

    Not in our library10.1152/jn.1998.79.6.2919

  36. 36.

    Rigotti M, et al. The importance of mixed selectivity in complex cognitive tasks. Nature. 2013;497:585-590.

    Not in our library10.1038/nature12160

  37. 37.

    Shafi M, et al. Variability in neuronal activity in primate cortex during working memory tasks. Neuroscience. 2007;146:1082-1108.

    Not in our library10.1016/j.neuroscience.2006.12.072

  38. 38.

    Cromer JA, Roy JE, Miller EK. Representation of multiple, independent categories in the primate prefrontal cortex. Neuron. 2010;66:796-807.

    Not in our library10.1016/j.neuron.2010.05.005

  39. 39.

    Hussar CR, Pasternak T. Common rules guide comparisons of speed and direction of motion in the dorsolateral prefrontal cortex. J. Neurosci. 2013;33:972-986.

    Not in our library10.1523/jneurosci.4075-12.2013

  40. 40.

    Tallon-Baudry C, Bertrand O, Delpuech C, Pernier J. Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. J. Neurosci. 1996;16:4240-4249.

    Not in our library10.1523/jneurosci.16-13-04240.1996

  41. 41.

    Thomson D. Spectrum estimation and harmonic analysis. Proc. IEEE. 1982;70:1055-1096.

    Not in our library10.1109/proc.1982.12433

  42. 42.

    Jarvis MR, Mitra PP. Sampling Properties of the spectrum and coherency of sequences of action potentials. Neural Comput. 2001;13:717-749.

    Not in our library10.1162/089976601300014312

  43. 43.

    Olejnik S, Algina J. Generalized eta and omega squared statistics: measures of effect size for some common research designs. Psychol. Methods. 2003;8:434-447.

    Not in our library10.1037/1082-989x.8.4.434

  44. 44.

    Maris E, Oostenveld R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods. 2007;164:177-190.

    Not in our library10.1016/j.jneumeth.2007.03.024

Cited by papers we hold 1

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.