Skip to main content
SpringerLink
Log in

Theta Oscillations Support Prefrontal-hippocampal Interactions in Sequential Working Memory

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

The prefrontal cortex and hippocampus may support sequential working memory beyond episodic memory and spatial navigation. This stereoelectroencephalography (SEEG) study investigated how the dorsolateral prefrontal cortex (DLPFC) interacts with the hippocampus in the online processing of sequential information. Twenty patients with epilepsy (eight women, age 27.6 ± 8.2 years) completed a line ordering task with SEEG recordings over the DLPFC and the hippocampus. Participants showed longer thinking times and more recall errors when asked to arrange random lines clockwise (random trials) than to maintain ordered lines (ordered trials) before recalling the orientation of a particular line. First, the ordering-related increase in thinking time and recall error was associated with a transient theta power increase in the hippocampus and a sustained theta power increase in the DLPFC (3–10 Hz). In particular, the hippocampal theta power increase correlated with the memory precision of line orientation. Second, theta phase coherences between the DLPFC and hippocampus were enhanced for ordering, especially for more precisely memorized lines. Third, the theta band DLPFC → hippocampus influence was selectively enhanced for ordering, especially for more precisely memorized lines. This study suggests that theta oscillations may support DLPFC-hippocampal interactions in the online processing of sequential information.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Chase HW, Clark L, Sahakian BJ, Bullmore ET, Robbins TW. Dissociable roles of prefrontal subregions in self-ordered working memory performance. Neuropsychologia 2008, 46: 2650–2661.

    Article  PubMed  Google Scholar 

  2. Sirigu A, Cohen L, Zalla T, Pradat-Diehl P, Van Eeckhout P, Grafman J. Distinct frontal regions for processing sentence syntax and story grammar. Cortex 1998, 34: 771–778.

    Article  CAS  PubMed  Google Scholar 

  3. Dede AJ, Frascino JC, Wixted JT, Squire LR. Learning and remembering real-world events after medial temporal lobe damage. Proc Natl Acad Sci U S A 2016, 113: 13480–13485.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hunsaker MR, Fieldsted PM, Rosenberg JS, Kesner RP. Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors. Behav Neurosci 2008, 122: 643–650.

    Article  PubMed  Google Scholar 

  5. Heuer E, Bachevalier J. Working memory for temporal order is impaired after selective neonatal hippocampal lesions in adult rhesus macaques. Behav Brain Res 2013, 239: 55–62.

    Article  PubMed  Google Scholar 

  6. Li CX, Li Z, Hu X, Zhang X, Bachevalier J. Altered hippocampal-prefrontal functional network integrity in adult macaque monkeys with neonatal hippocampal lesions. Neuroimage 2021, 227: 117645.

    Article  PubMed  Google Scholar 

  7. Eichenbaum H. Prefrontal-hippocampal interactions in episodic memory. Nat Rev Neurosci 2017, 18: 547–558.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  9. Kim J, Delcasso S, Lee I. Neural correlates of object-in-place learning in hippocampus and prefrontal cortex. J Neurosci 2011, 31: 16991–17006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Place R, Farovik A, Brockmann M, Eichenbaum H. Bidirectional prefrontal-hippocampal interactions support context-guided memory. Nat Neurosci 2016, 19: 992–994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Tavares LCS, Tort ABL. Hippocampal-prefrontal interactions during spatial decision-making. Hippocampus 2022, 32: 38–54.

    Article  PubMed  Google Scholar 

  12. Brincat SL, Miller EK. Frequency-specific hippocampal-prefrontal interactions during associative learning. Nat Neurosci 2015, 18: 576–581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tanninen SE, Nouriziabari B, Morrissey MD, Bakir R, Dayton RD, Klein RL, et al. Entorhinal tau pathology disrupts hippocampal-prefrontal oscillatory coupling during associative learning. Neurobiol Aging 2017, 58: 151–162.

    Article  CAS  PubMed  Google Scholar 

  14. Johnson EL, Adams JN, Solbakk AK, Endestad T, Larsson PG, Ivanovic J, et al. Dynamic frontotemporal systems process space and time in working memory. PLoS Biol 2018, 16: e2004274.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Kaplan R, Bush D, Bisby JA, Horner AJ, Meyer SS, Burgess N. Medial prefrontal-medial temporal Theta phase coupling in dynamic spatial imagery. J Cogn Neurosci 2017, 29: 507–519.

    Article  PubMed  Google Scholar 

  16. Garrido MI, Barnes GR, Kumaran D, Maguire EA, Dolan RJ. Ventromedial prefrontal cortex drives hippocampal theta oscillations induced by mismatch computations. Neuroimage 2015, 120: 362–370.

    Article  PubMed  Google Scholar 

  17. D’Esposito M, Postle BR, Ballard D, Lease J. Maintenance versus manipulation of information held in working memory: An event-related fMRI study. Brain Cogn 1999, 41: 66–86.

    Article  CAS  PubMed  Google Scholar 

  18. Ye Z, Zhang G, Li S, Zhang Y, Xiao W, Zhou X, et al. Age differences in the fronto-striato-parietal network underlying serial ordering. Neurobiol Aging 2020, 87: 115–124.

    Article  PubMed  Google Scholar 

  19. Sakai K, Passingham RE. Prefrontal interactions reflect future task operations. Nat Neurosci 2003, 6: 75–81.

    Article  CAS  PubMed  Google Scholar 

  20. Kumaran D, Maguire EA. An unexpected sequence of events: Mismatch detection in the human hippocampus. PLoS Biol 2006, 4: e424.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Barnett AJ, O’Neil EB, Watson HC, Lee ACH. The human hippocampus is sensitive to the durations of events and intervals within a sequence. Neuropsychologia 2014, 64: 1–12.

    Article  PubMed  Google Scholar 

  22. Manns JR, Howard MW, Eichenbaum H. Gradual changes in hippocampal activity support remembering the order of events. Neuron 2007, 56: 530–540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Naya Y, Chen H, Yang C, Suzuki WA. Contributions of primate prefrontal cortex and medial temporal lobe to temporal-order memory. Proc Natl Acad Sci U S A 2017, 114: 13555–13560.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  24. Naya Y, Suzuki WA. Integrating what and when across the primate medial temporal lobe. Science 2011, 333: 773–776.

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Chen J, Dastjerdi M, Foster BL, LaRocque KF, Rauschecker AM, Parvizi J, et al. Human hippocampal increases in low-frequency power during associative prediction violations. Neuropsychologia 2013, 51: 2344–2351.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Amiez C, Petrides M. Selective involvement of the mid-dorsolateral prefrontal cortex in the coding of the serial order of visual stimuli in working memory. Proc Natl Acad Sci U S A 2007, 104: 13786–13791.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rowe JB, Passingham RE. Working memory for location and time: Activity in prefrontal area 46 relates to selection rather than maintenance in memory. Neuroimage 2001, 14: 77–86.

    Article  CAS  PubMed  Google Scholar 

  28. Hsieh LT, Ekstrom AD, Ranganath C. Neural oscillations associated with item and temporal order maintenance in working memory. J Neurosci 2011, 31: 10803–10810.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Roberts BM, Hsieh LT, Ranganath C. Oscillatory activity during maintenance of spatial and temporal information in working memory. Neuropsychologia 2013, 51: 349–357.

    Article  PubMed  Google Scholar 

  30. Averbeck BB, Chafee MV, Crowe DA, Georgopoulos AP. Parallel processing of serial movements in prefrontal cortex. Proc Natl Acad Sci U S A 2002, 99: 13172–13177.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  31. Xie Y, Hu P, Li J, Chen J, Song W, Wang XJ, et al. Geometry of sequence working memory in macaque prefrontal cortex. Science 2022, 375: 632–639.

    Article  ADS  CAS  PubMed  Google Scholar 

  32. Bays PM, Catalao RFG, Husain M. The precision of visual working memory is set by allocation of a shared resource. J Vis 2009, 9: 1–11.

    Article  Google Scholar 

  33. Oostenveld R, Fries P, Maris E, Schoffelen JM. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011, 2011: 156869.

    Article  PubMed  Google Scholar 

  34. Janca R, Jezdik P, Cmejla R, Tomasek M, Worrell GA, Stead M, et al. Detection of interictal epileptiform discharges using signal envelope distribution modelling: Application to epileptic and non-epileptic intracranial recordings. Brain Topogr 2015, 28: 172–183.

    Article  PubMed  Google Scholar 

  35. Fischl B. FreeSurfer. Neuroimage 2012, 62: 774–781.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  37. Jaeger TF. Categorical Data Analysis: Away from ANOVAs (transformation or not) and towards Logit Mixed Models. J Mem Lang 2008, 59: 434–446.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M. Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 2004, 115: 2292–2307.

    Article  PubMed  Google Scholar 

  39. Cui J, Xu L, Bressler SL, Ding M, Liang H. BSMART: A Matlab/C toolbox for analysis of multichannel neural time series. Neural Netw 2008, 21: 1094–1104.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Dhamala M, Rangarajan G, Ding M. Estimating Granger causality from Fourier and wavelet transforms of time series data. Phys Rev Lett 2008, 100: 018701.

    Article  ADS  PubMed  Google Scholar 

  41. Mao D. Neural correlates of spatial navigation in primate hippocampus. Neurosci Bull 2023, 39: 315–327.

    Article  PubMed  Google Scholar 

  42. Ito HT. Prefrontal-hippocampal interactions for spatial navigation. Neurosci Res 2018, 129: 2–7.

    Article  PubMed  Google Scholar 

  43. Ekstrom AD, Watrous AJ. Multifaceted roles for low-frequency oscillations in bottom-up and top-down processing during navigation and memory. Neuroimage 2014, 85: 667–677.

    Article  PubMed  Google Scholar 

  44. Watrous AJ, Tandon N, Conner CR, Pieters T, Ekstrom AD. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat Neurosci 2013, 16: 349–356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Romero K, Barense MD, Moscovitch M. Coherence and congruency mediate medial temporal and medial prefrontal activity during event construction. Neuroimage 2019, 188: 710–721.

    Article  PubMed  Google Scholar 

  46. He B, Cao L, Xia X, Zhang B, Zhang D, You B, et al. Fine-grained topography and modularity of the macaque frontal pole cortex revealed by anatomical connectivity profiles. Neurosci Bull 2020, 36: 1454–1473.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Itthipuripat S, Wessel JR, Aron AR. Frontal theta is a signature of successful working memory manipulation. Exp Brain Res 2013, 224: 255–262.

    Article  PubMed  Google Scholar 

  48. Parto Dezfouli M, Davoudi S, Knight RT, Daliri MR, Johnson EL. Prefrontal lesions disrupt oscillatory signatures of spatiotemporal integration in working memory. Cortex 2021, 138: 113–126.

    Article  PubMed  Google Scholar 

  49. Johnson EL, Dewar CD, Solbakk AK, Endestad T, Meling TR, Knight RT. Bidirectional frontoparietal oscillatory systems support working memory. Curr Biol 2017, 27: 1829-1835.e4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lundqvist M, Herman P, Warden MR, Brincat SL, Miller EK. Gamma and beta bursts during working memory readout suggest roles in its volitional control. Nat Commun 2018, 9: 394.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  51. Lundqvist M, Rose J, Herman P, Brincat SL, Buschman TJ, Miller EK. Gamma and beta bursts underlie working memory. Neuron 2016, 90: 152–164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lisman JE, Jensen O. The θ-γ neural code. Neuron 2013, 77: 1002–1016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Jensen O, Lisman JE. Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends Neurosci 2005, 28: 67–72.

    Article  CAS  PubMed  Google Scholar 

  54. Watrous AJ, Miller J, Qasim SE, Fried I, Jacobs J. Phase-tuned neuronal firing encodes human contextual representations for navigational goals. Elife 2018, 7: e32554.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Reddy L, Self MW, Zoefel B, Poncet M, Possel JK, Peters JC, et al. Theta-phase dependent neuronal coding during sequence learning in human single neurons. Nat Commun 2021, 12: 4839.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  56. Yang AI, Dikecligil GN, Jiang H, Das SR, Stein JM, Schuele SU, et al. The what and when of olfactory working memory in humans. Curr Biol 2021, 31: 4499-4511.e8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hurlstone MJ, Hitch GJ, Baddeley AD. Memory for serial order across domains: An overview of the literature and directions for future research. Psychol Bull 2014, 140: 339–373.

    Article  PubMed  Google Scholar 

  58. Liu W, Wang C, He T, Su M, Lu Y, Zhang G, et al. Substantia nigra integrity correlates with sequential working memory in Parkinson’s disease. J Neurosci 2021, 41: 6304–6313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Berdyyeva TK, Olson CR. Rank signals in four areas of macaque frontal cortex during selection of actions and objects in serial order. J Neurophysiol 2010, 104: 141–159.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Berdyyeva TK, Olson CR. Relation of ordinal position signals to the expectation of reward and passage of time in four areas of the macaque frontal cortex. J Neurophysiol 2011, 105: 2547–2559.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Kornysheva K, Bush D, Meyer SS, Sadnicka A, Barnes G, Burgess N. Neural competitive queuing of ordinal structure underlies skilled sequential action. Neuron 2019, 101: 1166-1180.e3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hasz BM, Redish AD. Dorsomedial prefrontal cortex and hippocampus represent strategic context even while simultaneously changing representation throughout a task session. Neurobiol Learn Mem 2020, 171: 107215.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Kaefer K, Nardin M, Blahna K, Csicsvari J. Replay of behavioral sequences in the medial prefrontal cortex during rule switching. Neuron 2020, 106: 154-165.e6.

    Article  CAS  PubMed  Google Scholar 

  64. Chao OY, de Souza Silva MA, Yang YM, Huston JP. The medial prefrontal cortex - hippocampus circuit that integrates information of object, place and time to construct episodic memory in rodents: Behavioral, anatomical and neurochemical properties. Neurosci Biobehav Rev 2020, 113: 373–407.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Rajasethupathy P, Sankaran S, Marshel JH, Kim CK, Ferenczi E, Lee SY, et al. Projections from neocortex mediate top-down control of memory retrieval. Nature 2015, 526: 653–659.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  66. Jayachandran M, Linley SB, Schlecht M, Mahler SV, Vertes RP, Allen TA. Prefrontal pathways provide top-down control of memory for sequences of events. Cell Rep 2019, 28: 640-654.e6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Li J, Cao D, Dimakopoulos V, Shi W, Yu S, Fan L, et al. Anterior-posterior hippocampal dynamics support working memory processing. J Neurosci 2022, 42: 443–453.

    Article  CAS  PubMed  Google Scholar 

  68. D’Argembeau A, Jeunehomme O, Majerus S, Bastin C, Salmon E. The neural basis of temporal order processing in past and future thought. J Cogn Neurosci 2015, 27: 185–197.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. Yingying Tan for her advice on data analysis and Qiong Ding and Chao Zhang for their assistance with data acquisition. This work was primarily supported by the STI2030-Major Project (2021ZD0203600), with additional support from the Shanghai Municipal Science and Technology Commission (2018SHZDZX05 and 2018ZR1406500), the Shanghai Pujiang Program (19PJ1407500), the Shanghai Jiao Tong University Medical and Engineering Cross Research Fund (YG2019QNA31), the Shanghai Municipal Health Commission Clinical Study Special Fund (20194Y0067), and the Ruijin Hospital Guangci Excellence Youth Training Program (GCQN-2019-B10).

Author information

Author notes

  1. Minghong Su and Kejia Hu contributed equally to this work.

Authors and Affiliations

  1. Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China

    Minghong Su

  2. Department of Psychology, University of Chinese Academy of Sciences, Beijing, 100049, China

    Minghong Su

  3. Department of Neurosurgery, Center for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, 200025, China

    Kejia Hu, Wei Liu, Yunhao Wu, Tao Wang, Chunyan Cao, Bomin Sun & Shikun Zhan

  4. Institute of Neuroscience, Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, 200031, China

    Zheng Ye

Authors
  1. Minghong Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kejia Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yunhao Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunyan Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bomin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shikun Zhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zheng Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Shikun Zhan or Zheng Ye.

Ethics declarations

Conflict of interest

The authors claim that there are no conflicts of interest.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Su, M., Hu, K., Liu, W. et al. Theta Oscillations Support Prefrontal-hippocampal Interactions in Sequential Working Memory. Neurosci. Bull. 40, 147–156 (2024). https://doi.org/10.1007/s12264-023-01134-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-023-01134-6

Keywords

Search

Navigation