Skip to main content

Slow Oscillation in Prefrontal Cortex Underlying Local Computations and Large-Scale Interactions

  • Chapter
  • First Online:
The Physics of the Mind and Brain Disorders

Part of the book series: Springer Series in Cognitive and Neural Systems ((SSCNS,volume 11))

Abstract

Slow oscillation (4–8 Hz) in the prefrontal cortex is widely observed across species during various cognitive processes such as working memory. In humans and primates, the slow oscillation observed in the frontal area is termed ‘midline-frontal theta’ (FM-theta) oscillation. In rodents, the slow oscillation in the prefrontal cortex is termed ‘4-Hz’ oscillation. Although the generation mechanisms of FM-theta and 4-Hz oscillations have not been revealed yet, it is hypothesized that FM-theta in humans and 4-Hz in rodents have similar physiological properties and functions. Here, the roles of FM–theta and 4-Hz oscillations on cognitive functions and neuronal computations within local circuits and across large-scale brain networks are described.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

References

  • Anguera JA, Boccanfuso J, Rintoul JL, Al-Hashimi O, Faraji F, Janowich J, Kong E, Larraburo Y, Rolle C, Johnston E, Gazzaley A (2013) Video game training enhances cognitive control in older adults. Nature 501:97–101

    CAS  Google Scholar 

  • Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (2010) Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci U S A 107:3228–3233

    CAS  Google Scholar 

  • Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4:829–839

    CAS  Google Scholar 

  • Brandon MP, Bogaard AR, Schultheiss NW, Hasselmo ME (2013) Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat Neurosci 16:739–748

    CAS  Google Scholar 

  • Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325–340

    CAS  Google Scholar 

  • Buzsáki G (2006) Rhythms of the brain. Oxford University Press, Oxford

    Google Scholar 

  • Buzsaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304:1926–1929

    CAS  Google Scholar 

  • Buzsaki G, Wang XJ (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225

    CAS  Google Scholar 

  • Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506–515

    Google Scholar 

  • Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628

    CAS  Google Scholar 

  • Canolty RT, Ganguly K, Kennerley SW, Cadieu CF, Koepsell K, Wallis JD, Carmena JM (2010) Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies. Proc Natl Acad Sci U S A 107:17356–17361

    CAS  Google Scholar 

  • Cavanagh JF, Frank MJ (2014) Frontal theta as a mechanism for cognitive control. Trends Cogn Sci 18:414–421

    Google Scholar 

  • Cavanagh JF, Cohen MX, Allen JJ (2009) Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring. J Neurosci 29:98–105

    CAS  Google Scholar 

  • Cavanagh JF, Frank MJ, Klein TJ, Allen JJ (2010) Frontal theta links prediction errors to behavioral adaptation in reinforcement learning. NeuroImage 49:3198–3209

    Google Scholar 

  • Cavanagh JF, Wiecki TV, Cohen MX, Figueroa CM, Samanta J, Sherman SJ, Frank MJ (2011) Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nat Neurosci 14:1462–1467

    CAS  Google Scholar 

  • Cavanagh JF, Zambrano-Vazquez L, Allen JJ (2012) Theta lingua franca: a common mid-frontal substrate for action monitoring processes. Psychophysiology 49:220–238

    Google Scholar 

  • Cavanagh JF, Eisenberg I, Guitart-Masip M, Huys Q, Frank MJ (2013) Frontal theta overrides pavlovian learning biases. J Neurosci 33:8541–8548

    CAS  Google Scholar 

  • Cohen MX (2014) A neural microcircuit for cognitive conflict detection and signaling. Trends Neurosci 37:480–490

    CAS  Google Scholar 

  • Cohen MX, van Gaal S (2013) Dynamic interactions between large-scale brain networks predict behavioral adaptation after perceptual errors. Cereb Cortex 23:1061–1072

    Google Scholar 

  • Dejean C, Courtin J, Karalis N, Chaudun F, Wurtz H, Bienvenu TC, Herry C (2016) Prefrontal neuronal assemblies temporally control fear behaviour. Nature 535:420–424

    CAS  Google Scholar 

  • Fell J, Axmacher N (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12:105–118

    CAS  Google Scholar 

  • Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224

    CAS  Google Scholar 

  • Fujisawa S, Buzsaki G (2011) A 4 Hz oscillation adaptively synchronizes prefrontal, VTA, and hippocampal activities. Neuron 72:153–165

    CAS  Google Scholar 

  • Fujisawa S, Amarasingham A, Harrison MT, Buzsaki G (2008) Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci 11:823–833

    CAS  Google Scholar 

  • Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 7:374–385

    CAS  Google Scholar 

  • Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14:477–485

    CAS  Google Scholar 

  • Hanslmayr S, Pastotter B, Bauml KH, Gruber S, Wimber M, Klimesch W (2008) The electrophysiological dynamics of interference during the Stroop task. J Cogn Neurosci 20:215–225

    Google Scholar 

  • Herry C, Johansen JP (2014) Encoding of fear learning and memory in distributed neuronal circuits. Nat Neurosci 17:1644–54

    Google Scholar 

  • Holroyd CB, Coles MG (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109:679–709

    Google Scholar 

  • Hutchison RM, Womelsdorf T, Allen EA, Bandettini PA, Calhoun VD, Corbetta M, Della Penna S, Duyn JH, Glover GH, Gonzalez-Castillo J et al (2013) Dynamic functional connectivity: promise, issues, and interpretations. NeuroImage 80:360–378

    Google Scholar 

  • Jensen O, Colgin LL (2007) Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci 11:267–269

    Google Scholar 

  • Jensen O, Tesche CD (2002) Frontal theta activity in humans increases with memory load in a working memory task. Eur J Neurosci 15:1395–1399

    Google Scholar 

  • Jung MW, Qin Y, McNaughton BL, Barnes CA (1998) Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb Cortex 8:437–450

    CAS  Google Scholar 

  • Karalis N, Dejean C, Chaudun F, Khoder S, Rozeske RR, Wurtz H, Bagur S, Benchenane K, Sirota A, Courtin J, Herry C (2016) 4-Hz oscillations synchronize prefrontal-amygdala circuits during fear behavior. Nat Neurosci 19:605–612

    CAS  Google Scholar 

  • Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320:110–113

    CAS  Google Scholar 

  • Liebe S, Hoerzer GM, Logothetis NK, Rainer G (2012) Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance. Nat Neurosci 15(456–462):S451–S452

    Google Scholar 

  • Luo H, Poeppel D (2007) Phase patterns of neuronal responses reliably discriminate speech in human auditory cortex. Neuron 54:1001–1010

    CAS  Google Scholar 

  • Luu P, Tucker DM, Makeig S (2004) Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation. Clin Neurophysiol 115:1821–1835

    Google Scholar 

  • McNab F, Klingberg T (2008) Prefrontal cortex and basal ganglia control access to working memory. Nat Neurosci 11:103–107

    CAS  Google Scholar 

  • Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202

    CAS  Google Scholar 

  • Missonnier P, Deiber MP, Gold G, Millet P, Gex-Fabry Pun M, Fazio-Costa L, Giannakopoulos P, Ibanez V (2006) Frontal theta event-related synchronization: comparison of directed attention and working memory load effects. J Neural Transm (Vienna) 113:1477–1486

    CAS  Google Scholar 

  • Mitchell DJ, McNaughton N, Flanagan D, Kirk IJ (2008) Frontal-midline theta from the perspective of hippocampal “theta”. Prog Neurobiol 86:156–185

    Google Scholar 

  • Narayanan NS, Cavanagh JF, Frank MJ, Laubach M (2013) Common medial frontal mechanisms of adaptive control in humans and rodents. Nat Neurosci 16:1888–1895

    CAS  Google Scholar 

  • von Nicolai C, Engler G, Sharott A, Engel AK, Moll CK, Siegel M (2014) Corticostriatal coordination through coherent phase-amplitude coupling. J Neurosci 34:5938–5948

    Google Scholar 

  • Nigbur R, Ivanova G, Sturmer B (2011) Theta power as a marker for cognitive interference. Clin Neurophysiol 122:2185–2194

    Google Scholar 

  • Onton J, Delorme A, Makeig S (2005) Frontal midline EEG dynamics during working memory. NeuroImage 27:341–356

    Google Scholar 

  • Parker KL, Chen KH, Kingyon JR, Cavanagh JF, Narayanan NS (2014) D1-dependent 4 Hz oscillations and ramping activity in rodent medial frontal cortex during interval timing. J Neurosci 34:16774–16783

    Google Scholar 

  • Payne L, Kounios J (2009) Coherent oscillatory networks supporting short-term memory retention. Brain Res 1247:126–132

    CAS  Google Scholar 

  • Raghavachari S, Kahana MJ, Rizzuto DS, Caplan JB, Kirschen MP, Bourgeois B, Madsen JR, Lisman JE (2001) Gating of human theta oscillations by a working memory task. J Neurosci 21:3175–3183

    CAS  Google Scholar 

  • Roux F, Uhlhaas PJ (2014) Working memory and neural oscillations: alpha-gamma versus theta-gamma codes for distinct WM information? Trends Cogn Sci 18:16–25

    Google Scholar 

  • Saleh M, Reimer J, Penn R, Ojakangas CL, Hatsopoulos NG (2010) Fast and slow oscillations in human primary motor cortex predict oncoming behaviorally relevant cues. Neuron 65:461–471

    CAS  Google Scholar 

  • Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A (1998) Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci U S A 95:7092–7096

    CAS  Google Scholar 

  • Sauseng P, Klimesch W, Schabus M, Doppelmayr M (2005) Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. Int J Psychophysiol 57:97–103

    Google Scholar 

  • Sauseng P, Hoppe J, Klimesch W, Gerloff C, Hummel FC (2007) Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range. Eur J Neurosci 25:587–593

    CAS  Google Scholar 

  • Scheeringa R, Petersson KM, Oostenveld R, Norris DG, Hagoort P, Bastiaansen MC (2009) Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance. NeuroImage 44:1224–1238

    Google Scholar 

  • Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9–18

    CAS  Google Scholar 

  • Schultz W, Dickinson A (2000) Neuronal coding of prediction errors. Annu Rev Neurosci 23:473–500

    CAS  Google Scholar 

  • Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12:154–167

    CAS  Google Scholar 

  • Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121–134

    CAS  Google Scholar 

  • Tort AB, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ (2008) Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A 105:20517–20522

    CAS  Google Scholar 

  • Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229–239

    CAS  Google Scholar 

  • van de Vijver I, Ridderinkhof KR, Cohen MX (2011) Frontal oscillatory dynamics predict feedback learning and action adjustment. J Cogn Neurosci 23:4106–4121

    Google Scholar 

  • Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609–1612

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shigeyoshi Fujisawa .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Fujisawa, S. (2017). Slow Oscillation in Prefrontal Cortex Underlying Local Computations and Large-Scale Interactions. In: Opris, I., Casanova, M.F. (eds) The Physics of the Mind and Brain Disorders. Springer Series in Cognitive and Neural Systems, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-319-29674-6_11

Download citation

Publish with us

Policies and ethics