Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance

Nature Neuroscience volume 15, pages 456–462 (2012)Cite this article

Subjects

Abstract

Short-term memory requires communication between multiple brain regions that collectively mediate the encoding and maintenance of sensory information. It has been suggested that oscillatory synchronization underlies intercortical communication. Yet, whether and how distant cortical areas cooperate during visual memory remains elusive. We examined neural interactions between visual area V4 and the lateral prefrontal cortex using simultaneous local field potential (LFP) recordings and single-unit activity (SUA) in monkeys performing a visual short-term memory task. During the memory period, we observed enhanced between-area phase synchronization in theta frequencies (3–9 Hz) of LFPs together with elevated phase locking of SUA to theta oscillations across regions. In addition, we found that the strength of intercortical locking was predictive of the animals' behavioral performance. This suggests that theta-band synchronization coordinates action potential communication between V4 and prefrontal cortex that may contribute to the maintenance of visual short-term memories.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Experimental procedure, behavioral performance and power modulations in areas V4 and lPF during baseline and delay.
Figure 2: Phase locking between V4 and lPF in theta band.
Figure 3: Enhanced intra-area spike-phase locking in theta during delay.
Figure 4: Inter-area theta phase locking of V4 and prefrontal neurons during visual memory.
Figure 5: Theta-phase locking during the delay is higher for correct than for incorrect trials.
Figure 6: Correlation of phase locking with performance across single sessions.

Similar content being viewed by others

References

  1. Buzsáki, G. & Draguhn, A. Neuronal oscillations in cortical networks. Science 304, 1926–1929 (2004).

    Article  Google Scholar 

  2. Fries, P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474–480 (2005).

    Article  Google Scholar 

  3. Buzsáki, G. The hippocampo-neocortical dialogue. Cereb. Cortex 6, 81–92 (1996).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Jones, M.W. & Wilson, M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 3, e402 (2005).

    Article  Google Scholar 

  6. O'Keefe, J. Hippocampus, theta, and spatial memory. Curr. Opin. Neurobiol. 3, 917–924 (1993).

    Article  CAS  Google Scholar 

  7. Buzsáki, G. Theta oscillations in the hippocampus. Neuron 33, 325–340 (2002).

    Article  Google Scholar 

  8. Kahana, M.J. et al. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399, 781–784 (1999).

    Article  CAS  Google Scholar 

  9. Raghavachari, S. et al. Gating of human theta oscillations by a working memory task. J. Neurosci. 21, 3175–3183 (2001).

    Article  CAS  Google Scholar 

  10. Tesche, C.D. & Karhu, J. Theta oscillations index human hippocampal activation during a working memory task. Proc. Natl. Acad. Sci. USA 97, 919–924 (2000).

    Article  CAS  Google Scholar 

  11. Rutishauser, U. et al. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903–907 (2010).

    Article  CAS  Google Scholar 

  12. Sarnthein, J. et al. Synchronization between prefrontal and posterior association cortex during human working memory. Proc. Natl. Acad. Sci. USA 95, 7092–7096 (1998).

    Article  CAS  Google Scholar 

  13. Orban, G.A. Higher order visual processing in macaque extrastriate cortex. Physiol. Rev. 88, 59–89 (2008).

    Article  Google Scholar 

  14. Pasupathy, A. Neural basis of shape representation in the primate brain. Prog. Brain Res. 154, 293–313 (2006).

    Article  Google Scholar 

  15. Zeki, S. The representation of colours in the cerebral cortex. Nature 284, 412–418 (1980).

    Article  CAS  Google Scholar 

  16. Liebe, S., Logothetis, N.K. & Rainer, G. Dissociable effects of natural image structure and color on LFP and spiking activity in the lateral prefrontal cortex and extrastriate visual area V4. J. Neurosci. 31, 10215–10227 (2011).

    Article  CAS  Google Scholar 

  17. Fries, P. et al. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560–1563 (2001).

    Article  CAS  Google Scholar 

  18. Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  Google Scholar 

  19. Fuster, J.M. & Alexander, G. Neuron activity related to short-term memory. Science 173, 652 (1971).

    Article  CAS  Google Scholar 

  20. Pasternak, T. & Greenlee, M.W. Working memory in primate sensory systems. Nat. Rev. Neurosci. 6, 97–107 (2005).

    Article  CAS  Google Scholar 

  21. Pesaran, B. et al. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat. Neurosci. 5, 805–811 (2002).

    Article  CAS  Google Scholar 

  22. Hoerzer, G.M. et al. Directed coupling in local field potentials of macaque v4 during visual short-term memory revealed by multivariate autoregressive models. Front. Comput. Neurosci. 4, 14 (2010).

    PubMed  PubMed Central  Google Scholar 

  23. Lee, H. et al. Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45, 147–156 (2005).

    Article  CAS  Google Scholar 

  24. Siegel, M., Warden, M.R. & Miller, E.K. Phase-dependent neuronal coding of objects in short-term memory. Proc. Natl. Acad. Sci. USA 106, 21341–21346 (2009).

    Article  CAS  Google Scholar 

  25. Liebe, S. et al. Color and shape interactions in the recognition of natural scenes by human and monkey observers. J. Vis. 9, 14 (2009).

    Article  Google Scholar 

  26. Lachaux, J.P. et al. Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194–208 (1999).

    Article  CAS  Google Scholar 

  27. Azouz, R. & Gray, C.M. Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37, 513–523 (2003).

    Article  CAS  Google Scholar 

  28. Rainer, G. & Miller, E.K. Timecourse of object-related neural activity in the primate prefrontal cortex during a short-term memory task. Eur. J. Neurosci. 15, 1244–1254 (2002).

    Article  Google Scholar 

  29. Schack, B. et al. Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. Int. J. Psychophysiol. 44, 143–163 (2002).

    Article  CAS  Google Scholar 

  30. Weiss, S., Muller, H.M. & Rappelsberger, P. Theta synchronization predicts efficient memory encoding of concrete and abstract nouns. Neuroreport 11, 2357–2361 (2000).

    Article  CAS  Google Scholar 

  31. Klimesch, W. Memory processes, brain oscillations and EEG synchronization. Int. J. Psychophysiol. 24, 61–100 (1996).

    Article  CAS  Google Scholar 

  32. Tiesinga, P., Fellous, J.M. & Sejnowski, T.J. Regulation of spike timing in visual cortical circuits. Nat. Rev. Neurosci. 9, 97–107 (2008).

    Article  CAS  Google Scholar 

  33. Volgushev, M., Chistiakova, M. & Singer, W. Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience 83, 15–25 (1998).

    Article  CAS  Google Scholar 

  34. Womelsdorf, T. et al. Modulation of neuronal interactions through neuronal synchronization. Science 316, 1609–1612 (2007).

    Article  CAS  Google Scholar 

  35. Fuentemilla, L. et al. Theta-coupled periodic replay in working memory. Curr. Biol. 20, 606–612 (2010).

    Article  CAS  Google Scholar 

  36. Fell, J. et al. Phase-locking within human mediotemporal lobe predicts memory formation. Neuroimage 43, 410–419 (2008).

    Article  Google Scholar 

  37. Guderian, S. & Duzel, E. Induced theta oscillations mediate large-scale synchrony with mediotemporal areas during recollection in humans. Hippocampus 15, 901–912 (2005).

    Article  Google Scholar 

  38. Pavlides, C. et al. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res. 439, 383–387 (1988).

    Article  CAS  Google Scholar 

  39. Huerta, P.T. & Lisman, J.E. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in Ca1 in vitro. Neuron 15, 1053–1063 (1995).

    Article  CAS  Google Scholar 

  40. Lynch, M.A. Long-term potentiation and memory. Physiol. Rev. 84, 87–136 (2004).

    Article  CAS  Google Scholar 

  41. Shadlen, M.N. & Newsome, W.T. Neural basis of a perceptual decision i the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001).

    Article  CAS  Google Scholar 

  42. Jensen, O. & Lisman, J.E. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci. 28, 67–72 (2005).

    Article  CAS  Google Scholar 

  43. Mongillo, G., Barak, O. & Tsodyks, M. Synaptic theory of working memory. Science 319, 1543–1546 (2008).

    Article  CAS  Google Scholar 

  44. Mehta, M.R., Quirk, M.C. & Wilson, M.A. Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron 25, 707–715 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  46. Towe, A.L. & Harding, G.W. Extracellular microelectrode sampling bias. Exp. Neurol. 29, 366–381 (1970).

    Article  CAS  Google Scholar 

  47. Graimann, B. & Pfurtscheller, G. Quantification and visualization of event-related changes in oscillatory brain activity in the time-frequency domain. Prog. Brain Res. 159, 79–97 (2006).

    Article  Google Scholar 

  48. Tallon-Baudry, C. & Bertrand, O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3, 151–162 (1999).

    Article  CAS  Google Scholar 

  49. Siapas, A.G., Lubenov, E.V. & Wilson, M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46, 141–151 (2005).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank J. Macke for discussions regarding analyses, and T. Mrsic-Flogel and J. Macke for useful comments on the manuscript. We also thank A.-L. Keller for help with histology. S.L. was supported by the Deutsche Forschungsgemeinschaft Sonderforschungsbereich 550 and a doctoral Fellowship of the Max Planck Society. G.M.H. was supported by projects FP7-231267 (“Self-Organized Recurrent Neural Learning for Language Processing”, ORGANIC) and FP7-506778 (Pattern Analysis, Statistical Modeling and Computational Learning, PASCAL2 ) of the European Union. G.R. is a European Science Foundation European Young Investigator.

Author information

Author notes

  1. Stefanie Liebe

    Present address: Present address: Department of Physiology, Pharmacology and Neuroscience, University College London, London, UK.,

Authors and Affiliations

  1. Department of Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, Tuebingen, Germany

    Stefanie Liebe, Nikos K Logothetis & Gregor Rainer

  2. Institute for Theoretical Computer Science, Graz University of Technology, Graz, Austria

    Gregor M Hoerzer

  3. The University of Manchester, Faculty of Medical and Human Sciences, Manchester, UK

    Nikos K Logothetis

  4. Department of Medicine, University of Fribourg, Switzerland

    Gregor Rainer

Authors
  1. Stefanie Liebe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gregor M Hoerzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nikos K Logothetis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gregor Rainer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.L. and G.R. designed the experiments. S.L. conducted the experiments. S.L. and G.M.H. analyzed the data. S.L. wrote the manuscript with contributions from G.M.H. and G.R. N.K.L. and G.R. supervised the study.

Corresponding authors

Correspondence to Stefanie Liebe or Gregor Rainer.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–9 (PDF 3841 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liebe, S., Hoerzer, G., Logothetis, N. et al. Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance. Nat Neurosci 15, 456–462 (2012). https://doi.org/10.1038/nn.3038

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3038

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing