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:

Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval

Nature Neuroscience volume 16, pages 349–356 (2013)Cite this article

Subjects

Abstract

The medial temporal lobes, prefrontal cortex and parts of parietal cortex form the neural underpinnings of episodic memory, which includes remembering both where and when an event occurred. However, the manner in which these three regions interact during retrieval of spatial and temporal context remains untested. We employed simultaneous electrocorticographical recordings across multilobular regions in patients undergoing seizure monitoring while they retrieved spatial and temporal context associated with an episode, and we used phase synchronization as a measure of network connectivity. Successful memory retrieval was characterized by greater global connectivity compared with incorrect retrieval, with the medial temporal lobe acting as a hub for these interactions. Spatial versus temporal context retrieval resulted in prominent differences in both the spectral and temporal patterns of network interactions. These results emphasize dynamic network interactions as being central to episodic memory retrieval, providing insight into how multiple contexts underlying a single event can be recreated in the same network.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Different possible theoretical network architectures during memory retrieval.
Figure 2: PHG-parietal and PHG-prefrontal phase synchronization during correct contextual retrieval.
Figure 3: Memory-related network construction: methods for characterizing frequency and condition specific memory networks.
Figure 4: Correct and incorrect memory networks.
Figure 5: Frequency-specific synchronization during correct spatial and temporal context retrieval.
Figure 6: Differential patterns of connectivity over time during spatial and temporal context retrieval.

Similar content being viewed by others

References

  1. Eichenbaum, H., Yonelinas, A.P. & Ranganath, C. The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123–152 (2007).

    Article  CAS  Google Scholar 

  2. Mitchell, K.J. & Johnson, M.K. Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? Psychol. Bull. 135, 638–677 (2009).

    Article  Google Scholar 

  3. Ranganath, C. et al. Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia 42, 2–13 (2004).

    Article  Google Scholar 

  4. Scoville, W.B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).

    Article  CAS  Google Scholar 

  5. Squire, L.R., Stark, C.E. & Clark, R.E. The medial temporal lobe. Annu. Rev. Neurosci. 27, 279–306 (2004).

    Article  CAS  Google Scholar 

  6. Simons, J.S. & Spiers, H.J. Prefrontal and medial temporal lobe interactions in long-term memory. Nat. Rev. Neurosci. 4, 637–648 (2003).

    Article  CAS  Google Scholar 

  7. Vargha-Khadem, F. et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380 (1997).

    Article  CAS  Google Scholar 

  8. Duarte, A., Ranganath, C. & Knight, R.T. Effects of unilateral prefrontal lesions on familiarity, recollection, and source memory. J. Neurosci. 25, 8333–8337 (2005).

    Article  CAS  Google Scholar 

  9. Blumenfeld, R.S. & Ranganath, C. Prefrontal cortex and long-term memory encoding: an integrative review of findings from neuropsychology and neuroimaging. Neuroscientist 13, 280–291 (2007).

    Article  Google Scholar 

  10. Vilberg, K.L. & Rugg, M.D. Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective. Neuropsychologia 46, 1787–1799 (2008).

    Article  Google Scholar 

  11. Spaniol, J. et al. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 47, 1765–1779 (2009).

    Article  Google Scholar 

  12. Hutchinson, J.B., Uncapher, M.R. & Wagner, A.D. Posterior parietal cortex and episodic retrieval: convergent and divergent effects of attention and memory. Learn. Mem. 16, 343–356 (2009).

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Eichenbaum, H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 1, 41–50 (2000).

    Article  CAS  Google Scholar 

  15. Norman, K.A. & O′Reilly, R.C. Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning systems approach. Psychol. Rev. 110, 611–646 (2003).

    Article  Google Scholar 

  16. McClelland, J.L., McNaughton, B.L. & O′Reilly, R.C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419–457 (1995).

    Article  Google Scholar 

  17. Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997).

    Article  CAS  Google Scholar 

  18. Teyler, T.J. & DiScenna, P. The hippocampal memory indexing theory. Behav. Neurosci. 100, 147–154 (1986).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  20. Benchenane, K. et al. Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66, 921–936 (2010).

    Article  CAS  Google Scholar 

  21. 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 

  22. Sirota, A. et al. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683–697 (2008).

    Article  CAS  Google Scholar 

  23. Spiers, H.J. et al. Unilateral temporal lobectomy patients show lateralized topographical and episodic memory deficits in a virtual town. Brain 124, 2476–2489 (2001).

    Article  CAS  Google Scholar 

  24. Ekstrom, A.D., Copara, M.S., Isham, E.A., Wang, W.C. & Yonelinas, A.P. Dissociable networks involved in spatial and temporal order source retrieval. Neuroimage 56, 1803–1813 (2011).

    Article  Google Scholar 

  25. Siegel, M., Donner, T.H. & Engel, A.K. Spectral fingerprints of large-scale neuronal interactions. Nat. Rev. Neurosci. 13, 121–134 (2012).

    Article  CAS  Google Scholar 

  26. Donner, T.H. & Siegel, M. A framework for local cortical oscillation patterns. Trends Cogn. Sci. 15, 191–199 (2011).

    Article  Google Scholar 

  27. van der Meij, R., Kahana, M. & Maris, E. Phase-amplitude coupling in human electrocorticography is spatially distributed and phase diverse. J. Neurosci. 32, 111–123 (2012).

    Article  CAS  Google Scholar 

  28. Maris, E., van Vugt, M. & Kahana, M. Spatially distributed patterns of oscillatory coupling between high-frequency amplitudes and low-frequency phases in human iEEG. Neuroimage 54, 836–850 (2011).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  30. 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).

    Article  CAS  Google Scholar 

  31. Lega, B.C., Jacobs, J. & Kahana, M. Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 22, 748–761 (2011).

    Article  Google Scholar 

  32. Anderson, K.L., Rajagovindan, R., Ghacibeh, G.A., Meador, K.J. & Ding, M. Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb. Cortex 20, 1604–1612 (2010).

    Article  Google Scholar 

  33. Lavenex, P. & Amaral, D.G. Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10, 420–430 (2000).

    Article  CAS  Google Scholar 

  34. Bullmore, E. & Sporns, O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186–198 (2009).

    Article  CAS  Google Scholar 

  35. Watrous, A.J., Fried, I. & Ekstrom, A.D. Behavioral correlates of human hippocampal delta and theta oscillations during navigation. J. Neurophysiol. 105, 1747–1755 (2011).

    Article  Google Scholar 

  36. Mormann, F. et al. Independent delta/theta rhythms in the human hippocampus and entorhinal cortex. Front. Hum. Neurosci. 2, 3 (2008).

    Article  Google Scholar 

  37. Libby, L.A., Ekstrom, A.D., Ragland, J.D. & Ranganath, C. Differential connectivity of perirhinal and parahippocampal cortices within human hippocampal subregions revealed by high-resolution functional imaging. J. Neurosci. 32, 6550–6560 (2012).

    Article  CAS  Google Scholar 

  38. Rutishauser, U., Ross, I.B., Mamelak, A.N. & Schuman, E.M. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903–907 (2010).

    Article  CAS  Google Scholar 

  39. Rizzuto, D.S. et al. Reset of human neocortical oscillations during a working memory task. Proc. Natl. Acad. Sci. USA 100, 7931–7936 (2003).

    Article  CAS  Google Scholar 

  40. Rizzuto, D.S., Madsen, J.R., Bromfield, E.B., Schulze-Bonhage, A. & Kahana, M.J. Human neocortical oscillations exhibit theta phase differences between encoding and retrieval. Neuroimage 31, 1352–1358 (2006).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  42. Yonelinas, A.P. et al. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat. Neurosci. 5, 1236–1241 (2002).

    Article  CAS  Google Scholar 

  43. Zhang, H. & Ekstrom, A.D. Human neural systems underlying rigid and flexible forms of allocentric spatial representation. Hum. Brain Mapp. published online, doi:10.1002/hbm.21494 (16 January 2012).

  44. Marshuetz, C., Reuter-Lorenz, P.A., Smith, E.E., Jonides, J. & Noll, D.C. Working memory for order and the parietal cortex: an event-related functional magnetic resonance imaging study. Neuroscience 139, 311–316 (2006).

    Article  CAS  Google Scholar 

  45. Tolman, E.C. Cognitive Maps in Rats and Men. Psychol. Rev. 55, 189–208 (1948).

    Article  CAS  Google Scholar 

  46. Howard, M.W. & Kahana, M.J. A distributed representation of temporal context. J. Math. Psychol. 46, 269–299 (2002).

    Article  Google Scholar 

  47. Tulving, E. Episodic memory: from mind to brain. Annu. Rev. Psychol. 53, 1–25 (2002).

    Article  Google Scholar 

  48. Conner, C.R., Ellmore, T.M., Pieters, T.A., DiSano, M.A. & Tandon, N. Variability of the relationship between electrophysiology and BOLD-fMRI across cortical regions in humans. J. Neurosci. 31, 12855–12865 (2011).

    Article  CAS  Google Scholar 

  49. Tandon, N. Cortical mapping by electrical stimulation of subdural electrodes: language areas. in Textbook of Epilepsy Surgery (ed. Lüders, H.O.) 1001–1015 (Informa Healthcare, New York, 2008).

  50. Nunez, P.L. & Srinivasan, R. Electric Fields of the Brain: the Neurophysics of EEG (Oxford University Press, New York, 2006).

  51. Delorme, A. & Makeig, S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9–21 (2004).

    Article  Google Scholar 

  52. Vinck, M., van Wingerden, M., Womelsdorf, T., Fries, P. & Pennartz, C.M. The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization. Neuroimage 51, 112–122 (2010).

    Article  Google Scholar 

  53. Cox, R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173 (1996).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Ranganath and A. Yonelinas, as well as members of their laboratories, for helpful comments on this manuscript. This work was supported by the Sloan Foundation, a Hellman Young Investigator Award and National Institute of Neurological Disorders and Stroke grant RO1NS076856.

Author information

Authors and Affiliations

  1. Neuroscience Graduate Group, University of California, Davis, California, USA

    Andrew J Watrous & Arne D Ekstrom

  2. Center for Neuroscience, University of California, Davis, California, USA

    Andrew J Watrous & Arne D Ekstrom

  3. Department of Neurosurgery, University of Texas Medical School, Houston, Texas, USA

    Nitin Tandon, Chris R Conner & Thomas Pieters

  4. Memorial Hermann Hospital, Texas Medical Center, Houston, Texas, USA

    Nitin Tandon

  5. Department of Psychology, University of California, Davis, California, USA

    Arne D Ekstrom

Authors
  1. Andrew J Watrous
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nitin Tandon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris R Conner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas Pieters
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arne D Ekstrom
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.D.E., N.T. and A.J.W. designed the experiment. N.T., C.C. and T.P. collected the data. A.J.W. performed the data analysis. A.J.W., A.D.E. and N.T. wrote the manuscript.

Corresponding author

Correspondence to Arne D Ekstrom.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–10 and Supplementary Tables 1 and 2 (PDF 11397 kb)

Supplementary Movie 1

Dynamics over time of the spatial retrieval network at 2 Hz. Green lines represent network edges. (MPG 1320 kb)

Supplementary Movie 2

Dynamics over time of the temporal retrieval network at 8 Hz. Green lines represent network edges. (MPG 1194 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watrous, A., Tandon, N., Conner, C. et al. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat Neurosci 16, 349–356 (2013). https://doi.org/10.1038/nn.3315

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3315

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