Cognitive, Affective, & Behavioral Neuroscience

, Volume 14, Issue 4, pp 1340–1355 | Cite as

EEG theta phase coupling during executive control of visual working memory investigated in individuals with schizophrenia and in healthy controls

  • Birgit Griesmayr
  • Barbara Berger
  • Renate Stelzig-Schoeler
  • Wolfgang Aichhorn
  • Juergen Bergmann
  • Paul Sauseng
Article

Abstract

In healthy humans, it has been shown that executive functions are associated with increased frontal-midline EEG theta activity and theta phase coupling between frontal and posterior brain regions. In individuals with schizophrenia, central executive functions are supposed to be heavily impaired. Given that theta phase coupling is causally involved in central executive functions, one would expect that patients with an executive function deficit should display abnormal EEG theta synchronization. We therefore investigated executive functioning in 21 healthy controls and 21 individuals with schizophrenia while they performed a visuospatial delayed match to sample task. The task required either high executive demands (manipulation of content in working memory [WM]) or low executive demands (retention of WM content). In addition, WM load (one vs. three items) was varied. Results indicated higher frontal theta activity for manipulation processes than for retention processes in patients with schizophrenia, as compared with healthy controls, independently of WM load. Furthermore, individuals with schizophrenia revealed a reduction in theta phase coupling during early stages of the delay period for retention, as well as for manipulation processes at high-WM loads. Deviations in theta phase coupling in individuals with schizophrenia were mainly characterized by aberrant fronto-posterior connections, but also by attenuated posterior connections during manipulation of high-WM load. To conclude, fronto-parietal theta coupling seems to be substantially involved in executive control, whereas frontal theta activity seems to reflect general task demands, such as deployment of attentional resources during WM.

Keywords

Electroencephalography Frontal midline theta activity Neural synchronization Oscillations 

Supplementary material

13415_2014_272_MOESM1_ESM.pdf (85 kb)
ESM 1(PDF 85 kb)

References

  1. Axmacher, N., Henseler, M. M., Jensen, O., Weinreich, I., Elger, C. E., & Fell, J. (2010). Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 107, 1–6. doi:10.1073/pnas.0911531107 CrossRefGoogle Scholar
  2. Badcock, J. C., Badcock, D. R., Read, C., & Jablensky, A. (2008). Examining encoding imprecision in spatial working memory in schizophrenia. Schizophrenia Research, 100(1), 144–152.PubMedCrossRefGoogle Scholar
  3. Baddeley, A. (1996). The fractionation of working memory. Proceedings of the National Academy of Sciences of the United States of America, 93(24), 13468–13472.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Baddeley, A., & Della Sala, S. (1998). Working memory and executive control. In A. C. Roberts, T. W. Robbins, & L. Weiskrantz (Eds.), The prefrontal cortex (pp. 9–21). Oxford: Oxford University Press.CrossRefGoogle Scholar
  5. Barch, D. M., & Smith, E. (2008). The cognitive neuroscience of working memory: Relevance to CNTRICS and Schizophrenia. Biological Psychiatry, 64(1), 11–17. doi:10.1016/j.biopsych.2008.03.003 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B: Methodological, 57, 289–300.Google Scholar
  7. Callicott, J. H., Mattay, V. S., Verchinski, B. A., Marenco, S., Egan, M. F., & Weinberger, D. R. (2003). Complexity of prefrontal cortical dysfunction in schizophrenia: More than up or down. American Journal of Psychiatry, 160, 2209–2215.PubMedCrossRefGoogle Scholar
  8. Cannon, T. D., Glahn, D. C., Kim, J., van Erp, T., Karlsgodt, K., Cohen, J. D., … Shirinyan, D. (2005). Dorsolateral prefrontal cortex activity during maintenance and manipulation of information in working memory in patients with schizophrenia. Archives of General Psychiatry, 62, 1071–1080.Google Scholar
  9. Canolty, R. T., Edwards, E., Dalal, S. S., Soltani, M., Nagarajan, S. S., Kirsch, H. E., … Knight, R. T. (2006). High gamma power is phase-locked to theta oscillations in human neocortex. Science, 313(5793), 1626–1628. doi:10.1126/science.1128115
  10. Champod, A. S., & Petrides, M. (2007). Dissociable roles of the posterior parietal and the prefrontal cortex in manipulation and monitoring processes. Proceedings of the National Academy of Sciences of the United States of America, 104(37), 14837–14842. doi:10.1073/pnas.0607101104 PubMedCentralPubMedCrossRefGoogle Scholar
  11. Cho, R. Y., Konecky, R. O., & Carter, C. S. (2006). Impairments in frontal cortical γ synchrony and cognitive control in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 103(52), 19878–19883. doi:10.1073/pnas.0609440103 PubMedCentralPubMedCrossRefGoogle Scholar
  12. Cohen, I., & Miles, R. (2000). Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus. The Journal of Physiology, 524(2), 485–502. doi:10.1111/j.1469-7793.2000.00485.x PubMedCentralPubMedCrossRefGoogle Scholar
  13. Collette, F., Salmon, E., Van der Linden, M., Chicherio, C., Belleville, S., Degueldre, C., … Franck, G. (1999). Regional brain activity during tasks devoted to the central executive of working memory. Cognitive Brain Research, 7(3), 411–417. doi:10.1016/S0926-6410(98)00045-7
  14. Demiralp, T., Bayraktaroglu, Z., Lenz, D., Junge, S., Busch, N. A., Maess, B., … Herrmann, C. S. (2007). Gamma amplitudes are coupled to theta phase in human EEG during visual perception. International Journal of Psychophysiology, 64(1), 24–30. doi:10.1016/j.ijpsycho.2006.07.005
  15. D’Esposito, M., Detre, J. A., Alsop, D. C., Shin, R. K., Atlas, S., & Grossman, M. (1995). The neural basis of the central executive system of working memory. Nature, 378(6554), 279–281. doi:10.1038/378279a0 PubMedCrossRefGoogle Scholar
  16. Diamond, A. (2011). Biological and social influences on cognitive control processes dependent on prefrontal cortex. Progress in Brain Research, 189, 319–339.PubMedCentralPubMedCrossRefGoogle Scholar
  17. Dosenbach, N. U., Fair, D. A., Cohen, A. L., Schlaggar, B. L., & Petersen, S. E. (2008). A dual-networks architecture of top-down control. Trends in Cognitive Sciences, 12(3), 99–105.PubMedCentralPubMedCrossRefGoogle Scholar
  18. Ford, J. M., Mathalon, D. H., Whitfield, S., Faustman, W. O., & Roth, W. T. (2002). Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biological Psychiatry, 51(6), 485–492.PubMedCrossRefGoogle Scholar
  19. Foucher, J. R., Lacambre, M., Pham, B. T., Giersch, A., & Elliott, M. A. (2007). Low time resolution in schizophrenia: Lengthened windows of simultaneity for visual, auditory and bimodal stimuli. Schizophrenia Research, 97(1–3), 118–127. doi:10.1016/j.schres.2007.08.013 PubMedCrossRefGoogle Scholar
  20. Franke, G. H. (2000). BSI. Brief Symptom Inventory von L. R. Derogatis - Deutsche Version. Beltz: Göttingen.Google Scholar
  21. Friston, K. J. (1998). The disconnection hypothesis. Schizophrenia Research, 30(2), 115–125. doi:10.1016/S0920-9964(97)00140-0 PubMedCrossRefGoogle Scholar
  22. Gevins, A., Smith, M. E., 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. Cerebral Cortex, 7(4), 374–385. doi:10.1093/cercor/7.4.374 PubMedCrossRefGoogle Scholar
  23. Haenschel, C., Bittner, R. A., Haertling, F., Rotarska-Jagiela, A., Maurer, K., Singer, W., & Linden, D. E. J. (2007a). Contribution of impaired early-stage visual processing to working memory dysfunctions in adolescents with schizophrenia. Archives of General Psychiatry, 64, 1229–1240.PubMedCrossRefGoogle Scholar
  24. Haenschel, C., Bittner, R. A., Waltz, J., Haertling, F., Wibral, M., Singer, W., … Rodriguez, E. (2009). Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia. The Journal of Neuroscience, 29(30), 9481–9489. doi:10.1523/jneurosci.1428-09.2009
  25. Haenschel, C., Uhlhaas, P. J., & Singer, W. (2007b). Synchronous oscillatory activity and working memory in schizophrenia. Pharmacopsychiatry, 40, S54–S61.CrossRefGoogle Scholar
  26. Hanslmayr, S., Pastötter, B., Bäuml, K.-H., Gruber, S., Wimber, M., & Klimesch, W. (2007). The electrophysiological dynamics of interference during the stroop task. Journal of Cognitive Neuroscience, 20(2), 215–225. doi:10.1162/jocn.2008.20020 CrossRefGoogle Scholar
  27. Hartman, M., Steketee, M. C., Silva, S., Lanning, K., & McCann, H. (2002). Working memory and schizophrenia: Evidence for slowed encoding. Schizophrenia Research, 59, 99–113.CrossRefGoogle Scholar
  28. Jensen, O., & Tesche, C. D. (2002). Frontal theta activity in humans increases with memory load in a working memory task. European Journal of Neuroscience, 15(8), 1395–1399. doi:10.1046/j.1460-9568.2002.01975.x PubMedCrossRefGoogle Scholar
  29. Junghee, L., & Sohee, P. (2005). Working memory impairments in schizophrenia: A meta-analysis. Journal of Abnormal Psychology, 114(4), 599–611.CrossRefGoogle Scholar
  30. Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261–276. doi:10.1093/schbul/13.2.261 PubMedCrossRefGoogle Scholar
  31. Kim, J., Glahn, D. C., Nuechterlein, K. H., & Cannon, T. D. (2004). Maintenance and manipulation of information in schizophrenia: Further evidence for impairment in the central executive component of working memory. Schizophrenia Research, 68(2–3), 173–187. doi:10.1016/S0920-9964(03)00150-6 PubMedCrossRefGoogle Scholar
  32. Kim, J.-J., Kwon, J. S., Park, H. J., Youn, T., Kang, D. H. K., Lee, D. S., & Lee, M. C. (2003). Functional Disconnection between the prefrontal and parietal cortices during working memory processing in schizophrenia: A [15O]H2O PET study. American Journal of Psychiatry, 160, 919–923.PubMedCrossRefGoogle Scholar
  33. Lachaux, J.-P., Rodriguez, E., Martinerie, J., & Varela, F. J. (1999). Measuring phase synchrony in brain signals. Human Brain Mapping, 8(4), 194–208. doi:10.1002/(SICI)1097-0193(1999)8:4<194::AID-HBM4>3.0.CO;2-C PubMedCrossRefGoogle Scholar
  34. Lakatos, P., Shah, A. S., Knuth, K. H., Ulbert, I., Karmos, G., & Schroeder, C. E. (2005). An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. Journal of Neurophysiology, 94(3), 1904–1911. doi:10.1152/jn.00263.2005 PubMedCrossRefGoogle Scholar
  35. Manoach, D. S. (2003). Prefrontal cortex dysfunction during working memory performance in schizophrenia: Reconciling discrepant findings. Schizophrenia Research, 60, 285–298.PubMedCrossRefGoogle Scholar
  36. Micheloyannis, S., Pachou, E., Stam, C. J., Breakspear, M., Bitsios, P., Vourkas, M., … Zervakis, M. (2006). Small-world networks and disturbed functional connectivity in schizophrenia. Schizophrenia Research, 87(1–3), 60–66. doi:10.1016/j.schres.2006.06.028
  37. Mizuhara, H., & Yamaguchi, Y. (2007). Human cortical circuits for central executive function emerge by theta phase synchronization. NeuroImage, 36(1), 232–244. doi:10.1016/j.neuroimage.2007.02.026 PubMedCrossRefGoogle Scholar
  38. Möller, H.-J., Müller, W. E., & Volz, H.-P. (2000). Psychopharmakotherapie. Ein Leitfaden für Klinik und Praxis. Stuttgart: Kohlhammer.Google Scholar
  39. Onton, J., Delorme, A., & Makeig, S. (2005). Frontal midline EEG dynamics during working memory. NeuroImage, 27(2), 341–356. doi:10.1016/j.neuroimage.2005.04.014 PubMedCrossRefGoogle Scholar
  40. Postle, B. R., Stern, C. E., Rosen, B. R., & Corkin, S. (2000). An fMRI investigation of cortical contributions to spatial and nonspatial visual working memory. NeuroImage, 11(5), 409–423. doi:10.1006/nimg.2000.0570 PubMedCrossRefGoogle Scholar
  41. Reichenberg, A., & Harvey, P. D. (2007). Neuropsychological impairments in schizophrenia: Integration of performance-based and brain imaging findings. Psychological Bulletin, 133, 833–858.PubMedCrossRefGoogle Scholar
  42. Sarnthein, J., Petsche, H., Rappelsberger, P., Shaw, G. L., & Von Stein, A. (1998). Synchronization between prefrontal and posterior association cortex during human working memory. Proceedings of the National Academy of Sciences of the United States of America, 95(12), 7092–7096.PubMedCentralPubMedCrossRefGoogle Scholar
  43. Sauseng, P., Griesmayr, B., Freunberger, R., & Klimesch, W. (2010). Control mechanisms in working memory: A possible function of EEG theta oscillations. Neuroscience and Biobehavioral Reviews, 34(7), 1015–1022. doi:10.1016/j.neubiorev.2009.12.006 PubMedCrossRefGoogle Scholar
  44. Sauseng, P., Hoppe, J., Klimesch, W., Gerloff, C., & Hummel, F. C. (2007). Dissociation of sustained attention from central executive functions: Local activity and interregional connectivity in the theta range. European Journal of Neuroscience, 25(2), 587–593. doi:10.1111/j.1460-9568.2006.05286.x PubMedCrossRefGoogle Scholar
  45. Sauseng, P., Klimesch, W., Freunberger, R., Pecherstorfer, T., Hanslmayr, S., & Doppelmayr, M. (2006). Relevance of EEG alpha and theta oscillations during task switching. Experimental Brain Research, 170(3), 295–301. doi:10.1007/s00221-005-0211-y PubMedCrossRefGoogle Scholar
  46. Sauseng, P., Klimesch, W., Heise, K. F., Gruber, W. R., Holz, E., Karim, A. A., … Hummel, F. C. (2009). Brain oscillatory substrates of visual short-term memory capacity. Current Biology, 19(21), 1846–1852. doi:10.1016/j.cub.2009.08.062
  47. 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. International Journal of Psychophysiology, 57(2), 97–103. doi:10.1016/j.ijpsycho.2005.03.018 PubMedCrossRefGoogle Scholar
  48. Smith, E. E., & Jonides, J. (1998). Neuroimaging analyses of human working memory. Proceedings of the National Academy of Sciences of the United States of America, 95(20), 12061–12068. doi:10.1073/pnas.95.20.12061 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Smith, E. E., & Jonides, J. (1999). Storage and executive processes in the frontal lobes. Science, 283(5408), 1657–1661. doi:10.1126/science.283.5408.1657 PubMedCrossRefGoogle Scholar
  50. Spencer, K. M., Nestor, P. G., Perlmutter, R., Niznikiewicz, M. A., Klump, M. C., Frumin, M., … McCarley, R. W. (2004). Neural synchrony indexes disordered perception and cognition in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 101(49), 17288–17293. doi: 10.1073/pnas.0406074101
  51. Tan, H. Y., Callicott, J. H., & Weinberger, D. R. (2007). Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cerebral Cortex, 17, 171–181.CrossRefGoogle Scholar
  52. Trujillo, L. T., Peterson, M. A., Kaszniak, A. W., & Allen, J. J. B. (2005). EEG phase synchrony differences across visual perception conditions may depend on recording and analysis methods. Clinical Neurophysiology, 116(1), 172–189.PubMedCrossRefGoogle Scholar
  53. Tschacher, W., & Bergomi, C. (2011). Cognitive binding in schizophrenia: Weakened integration of temporal intersensory information. Schizophrenia Bulletin, 37(suppl 2), S13–S22. doi:10.1093/schbul/sbr074 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Tsujimoto, T., Shimazu, H., & Isomura, Y. (2006). Direct recording of theta oscillations in primate prefrontal and anterior cingulate cortices. Journal of Neurophysiology, 95(5), 2987–3000. doi:10.1152/jn.00730.2005 PubMedCrossRefGoogle Scholar
  55. Uhlhaas, P. J., Linden, D. E. J., Singer, W., Haenschel, C., Lindner, M., Maurer, K., & Rodriguez, E. (2006). Dysfunctional long-range coordination of neural activity during gestalt perception in schizophrenia. The Journal of Neuroscience, 26(31), 8168–8175. doi:10.1523/jneurosci.2002-06.2006 PubMedCrossRefGoogle Scholar
  56. Uhlhaas, P. J., Roux, F., Singer, W., Haenschel, C., Sireteanu, R., & Rodriguez, E. (2009). The development of neural synchrony reflects late maturation and restructuring of functional networks in humans. Proceedings of the National Academy of Sciences of the United States of America, 106(24), 9866–9871. doi:10.1073/pnas.0900390106 PubMedCentralPubMedCrossRefGoogle Scholar
  57. Uhlhaas, P. J., & Singer, W. (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nature Reviews Neuroscience, 11(2), 100–113. doi:10.1038/nrn2774. http://www.nature.com/nrn/journal/v11/n2/suppinfo/nrn2774_S1.html.PubMedCrossRefGoogle Scholar
  58. van Assche, M., & Giersch, A. (2011). Visual organization processes in schizophrenia. Schizophrenia Bulletin, 37(2), 394–404. doi:10.1093/schbul/sbp084 PubMedCentralPubMedCrossRefGoogle Scholar
  59. von Stein, A., & Sarnthein, J. (2000). Different frequencies for different scales of cortical integration: From local gamma to long range alpha/theta synchronization. International Journal of Psychophysiology, 38(3), 301–313. doi:10.1016/S0167-8760(00)00172-0 CrossRefGoogle Scholar
  60. Woods, S. W. (2003). Chlorpromazine equivalent doses for the newer atypical antipsychotics. Journal of Clinical Psychiatry, 64, 663–667.PubMedCrossRefGoogle Scholar
  61. Wu, X., Chen, X., Li, Z., Han, S., & Zhang, D. (2007). Binding of verbal and spatial information in human working memory involves large-scale neural synchronization at theta frequency. NeuroImage, 35(4), 1654–1662. doi:10.1016/j.neuroimage.2007.02.011 PubMedCrossRefGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2014

Authors and Affiliations

  • Birgit Griesmayr
    • 1
    • 2
  • Barbara Berger
    • 2
  • Renate Stelzig-Schoeler
    • 3
  • Wolfgang Aichhorn
    • 3
  • Juergen Bergmann
    • 4
  • Paul Sauseng
    • 2
  1. 1.Department of PsychologyUniversity of SalzburgSalzburgAustria
  2. 2.Department of PsychologyUniversity of SurreyGuildfordUK
  3. 3.Department of Psychiatry and Psychotherapy I, Christian-Doppler-ClinicParacelsus Medical UniversitySalzburgAustria
  4. 4.Neuroscience Institute & Centre for Neurocognitive Research, Christian-Doppler-ClinicParacelsus Medical UniversitySalzburgAustria

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