Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-26T20:06:17.586Z Has data issue: false hasContentIssue false
  • English
  • Français

Measurement and Modulation of Working Memory-Related Oscillatory Abnormalities

Published online by Cambridge University Press:  30 July 2019

Brian C. Kavanaugh Open the ORCID record for Brian C. Kavanaugh [Opens in a new window] ,
Alexa Fryc  and
Linda L. Carpenter
Brian C. Kavanaugh*
Affiliation:
Department of Psychiatry & Human Behavior, E. P. Bradley Hospital, Riverside, RI 02915, USA Department of Psychiatry & Human Behavior, Alpert Medical School of Brown University, Providence, RI 02903, USA
Alexa Fryc
Affiliation:
Department of Psychology, University of Rhode Island, Kingston, RI 02881, USA
Linda L. Carpenter
Affiliation:
Department of Psychiatry & Human Behavior, Alpert Medical School of Brown University, Providence, RI 02903, USA Department of Psychiatry & Human Behavior, Butler Hospital, Providence, RI 02906, USA
*
Correspondence and reprint requests to: Brian C. Kavanaugh, E. P. Bradley Hospital/Alpert, Medical School of Brown University, 1011 Veterans Memorial Parkway, East Providence, RI 02915, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite the critical role of working memory (WM) in neuropsychiatric conditions, there remains a dearth of available WM-targeted interventions. Gamma and theta oscillations as measured with electroencephalography (EEG) or magnetoencephalography (MEG) reflect the neural underpinnings of WM. The WM processes that fluctuate in conjunction with WM demands are closely correlated with WM test performance, and their EEG signatures are abnormal in several clinical populations. Novel interventions such as transcranial magnetic stimulation (TMS) have been shown to modulate these oscillations and subsequently improve WM performance and clinical symptoms. Systematically identifying pathological WM-related gamma/theta oscillatory patterns with EEG/MEG and developing ways to target them with interventions such as TMS is an active area of clinical research. Results hold promise for enhancing the outcomes of our patients with WM deficits and for moving the field of clinical neuropsychology towards a mechanism-based approach.

Keywords

OscillationsWorking memoryEEGrTMSGammaTheta
Type
Short Review
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 10 , November 2019 , pp. 1076 - 1081
Copyright
Copyright © INS. Published by Cambridge University Press, 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albouy, P., Weiss, A., Baillet, S., & Zatorre, R.J. (2017). Selective entrainment of theta oscillations in the dorsal stream causally enhances auditory working memory performance. Neuron, 94(1), 193–206.e5. doi:10.1016/j.neuron.2017.03.015 CrossRefGoogle ScholarPubMed
Bai, W., Xia, M., Liu, T., & Tian, X. (2016). Aβ1-42-induced dysfunction in synchronized gamma oscillation during working memory. Behavioural Brain Research, 307, 112–119. doi:10.1016/j.bbr.2016.04.003 CrossRefGoogle ScholarPubMed
Barker, A.T., Jalinous, R., & Freeston, I.L. (1985). Non-invasive magnetic stimulation of human motor cortex. The Lancet, 325, 1106–1107.CrossRefGoogle Scholar
Barr, M.S., Farzan, F., Arenovich, T., Chen, R., Fitzgerald, P.B., & Daskalakis, Z.J. (2011). The effect of repetitive transcranial magnetic stimulation on gamma oscillatory activity in schizophrenia. PLoS One, 6(7), e22627. doi:10.1371/journal.pone.0022627 CrossRefGoogle Scholar
Barr, M.S., Farzan, F., Rusjan, P.M., Chen, R., Fitzgerald, P.B., & Daskalakis, Z.J. (2009). Potentiation of gamma oscillatory activity through repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex. Neuropsychopharmacology, 34(11), 2359–2367. doi:10.1038/npp.2009.79 CrossRefGoogle ScholarPubMed
Barr, M.S., Farzan, F., Tran, L.C., Chen, R., Fitzgerald, P.B., & Daskalakis, Z.J. (2010). Evidence for excessive frontal evoked gamma oscillatory activity in schizophrenia during working memory. Schizophrenia Research, 121(1–3), 146–152. doi:10.1016/j.schres.2010.05.023 CrossRefGoogle ScholarPubMed
Barr, M.S., Rajji, T.K., Zomorrodi, R., Radhu, N., George, T.P., Blumberger, D.M., & Daskalakis, Z.J. (2017). Impaired theta-gamma coupling during working memory performance in schizophrenia. Schizophrenia Research, 189, 104–110. doi:10.1016/j.schres.2017.01.044 CrossRefGoogle Scholar
Basar-Eroglu, C., Brand, A., Hildebrandt, H., Karolina Kedzior, K., Mathes, B., & Schmiedt, C. (2007). Working memory related gamma oscillations in schizophrenia patients. International Journal of Psychophysiology, 64(1), 39–45. doi:10.1016/j.ijpsycho.2006.07.007 CrossRefGoogle ScholarPubMed
Basar, E. (2013). A review of gamma oscillations in healthy subjects and in cognitive impairment. International Journal of Psychophysiology, 90(2), 99–117. doi:10.1016/j.ijpsycho.2013.07.005 CrossRefGoogle ScholarPubMed
Boudewyn, M.A. & Carter, C.S. (2018). Evolving concepts in brain oscillations and cognitive control in schizophrenia. Biological Psychiatry, 84, 632–633. doi:10.1016/j.biopsych.2018.08.017 CrossRefGoogle Scholar
Buzsaki, G. & Watson, B.O. (2012). Brain rhythms and neural syntax: Implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues in Clinical Neuroscience, 14, 345–367.Google ScholarPubMed
Cavanagh, J.F. & Frank, M.J. (2014). Frontal theta as a mechanism for cognitive control. Trends in Cognitive Sciences, 18(8), 414–421. doi:10.1016/j.tics.2014.04.012 CrossRefGoogle ScholarPubMed
Chaieb, L., Leszczynski, M., Axmacher, N., Hohne, M., Elger, C.E., & Fell, J. (2015). Theta-gamma phase-phase coupling during working memory maintenance in the human hippocampus. Cognitive Neuroscience, 6(4), 149–157. doi:10.1080/17588928.2015.1058254 CrossRefGoogle ScholarPubMed
Chen, C.M., Stanford, A.D., Mao, X., Abi-Dargham, A., Shungu, D.C., Lisanby, S.H., Schroeder, C.E., & Kegeles, L.S. (2014). GABA level, gamma oscillation, and working memory performance in schizophrenia. NeuroImage: Clinical, 4, 531–539. doi:10.1016/j.nicl.2014.03.007 CrossRefGoogle Scholar
Cole, M.W. & Schneider, W. (2007). The cognitive control network: Integrated cortical regions with dissociable functions. Neuroimage, 37(1), 343–360. doi:10.1016/j.neuroimage.2007.03.071 CrossRefGoogle ScholarPubMed
Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64, 135–168. doi:10.1146/annurev-psych-113011-143750 CrossRefGoogle ScholarPubMed
George, M.S., Lisanby, S.H., & Sackeim, H.A. (1999). Transcranial magnetic stimulation: Applications in neuropsychiatry. Archives of General Psychiatry, 56, 300–311.CrossRefGoogle ScholarPubMed
Gonzalez-Ortega, I., de Los Mozos, V., Echeburua, E., Mezo, M., Besga, A., Ruiz de Azua, S., Gonzalez-Pinto, A., Gutierrez, M., Zorrilla, I., & Gonzalez-Pinto, A. (2013). Working memory as a predictor of negative symptoms and functional outcome in first episode psychosis. Psychiatry Research, 206(1), 8–16. doi:10.1016/j.psychres.2012.08.025 CrossRefGoogle ScholarPubMed
Goodman, M.S., Kumar, S., Zomorrodi, R., Ghazala, Z., Cheam, A.S.M., Barr, M.S., Daskalakis, Z.J., Blumberger, D.M., Fischer, C., Flint, A., Mah, L., Herrmann, N., Bowie, C.R., Mulsant, B.H., & Rajji, T.K. (2018). Theta-gamma coupling and working memory in Alzheimer’s dementia and mild cognitive impairment. Frontiers in Aging Neuroscience, 10, 101. doi:10.3389/fnagi.2018.00101 CrossRefGoogle ScholarPubMed
Holz, E.M., Glennon, M., Prendergast, K., & Sauseng, P. (2010). Theta-gamma phase synchronization during memory matching in visual working memory. Neuroimage, 52(1), 326–335. doi:10.1016/j.neuroimage.2010.04.003 CrossRefGoogle ScholarPubMed
Honkanen, R., Rouhinen, S., Wang, S.H., Palva, J.M., & Palva, S. (2015). Gamma oscillations underlie the maintenance of feature-specific information and the contents of visual working memory. Cerebral Cortex, 25(10), 3788–3801. doi:10.1093/cercor/bhu263 CrossRefGoogle ScholarPubMed
Hoy, K.E., Bailey, N., Michael, M., Fitzgibbon, B., Rogasch, N.C., Saeki, T., & Fitzgerald, P.B. (2016). Enhancement of working memory and task-related oscillatory activity following intermittent theta burst stimulation in healthy controls. Cerebral Cortex, 26(12), 4563–4573. doi:10.1093/cercor/bhv193 CrossRefGoogle ScholarPubMed
Hsieh, L.T. & Ranganath, C. (2014). Frontal midline theta oscillations during working memory maintenance and episodic encoding and retrieval. Neuroimage, 85 Pt 2, 721–729. doi:10.1016/j.neuroimage.2013.08.003 CrossRefGoogle ScholarPubMed
Huang-Pollock, C., Shapiro, Z., Galloway-Long, H., & Weigard, A. (2017). Is poor working memory a transdiagnostic risk factor for psychopathology? Journal of Abnormal Child Psychology, 45(8), 1477–1490. doi:10.1007/s10802-016-0219-8 CrossRefGoogle ScholarPubMed
Itthipuripat, S., Wessel, J.R., & Aron, A.R. (2013). Frontal theta is a signature of successful working memory manipulation. Experimental Brain Research, 224(2), 255–262. doi:10.1007/s00221-012-3305-3 CrossRefGoogle ScholarPubMed
Jasper, H.H. & Carmichael, L. (1935). Electrical potentials from the intact human brain. Science, 81, 51–53.CrossRefGoogle ScholarPubMed
Jensen, O., Kaiser, J., & Lachaux, J.P. (2007). Human gamma-frequency oscillations associated with attention and memory. Trends in Neurosciences, 30(7), 317–324. doi:10.1016/j.tins.2007.05.001 CrossRefGoogle ScholarPubMed
Jokisch, D. & Jensen, O. (2007). Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. Journal of Neuroscience, 27(12), 3244–3251. doi:10.1523/JNEUROSCI.5399-06.2007 CrossRefGoogle ScholarPubMed
Kahana, M.J. (2006). The cognitive correlates of human brain oscillations. Journal of Neuroscience, 26(6), 1669–1672. doi:10.1523/JNEUROSCI.3737-05c.2006 CrossRefGoogle ScholarPubMed
Kaiser, J., Rieder, M., Abel, C., Peters, B., & Bledowski, C. (2017). Pre-encoding gamma-band activity during auditory working memory. Scientific Reports, 7, 42599. doi:10.1038/srep42599 CrossRefGoogle ScholarPubMed
Kaiser, J., Ripper, B., Birbaumer, N., & Werner, L. (2003). Dynamics of gamma-band activity in human magnetoencephalogram during auditory pattern working memory. Neuroimage, 20, 816–827. doi:10.1016/S1053-8119(03)00350-1 CrossRefGoogle ScholarPubMed
Kavanaugh, B.C., Cancilliere, M.K., & Spirito, A. (2019). Neurocognitive heterogeneity across the spectrum of psychopathology: Need for improved approaches to deficit detection and intervention. CNS Spectrums. doi:10.1017/S1092852919001081. [Epub ahead of print].CrossRefGoogle Scholar
Khurana, A., Romer, D., Betancourt, L.M., & Hurt, H. (2017). Working memory ability and early drug use progression as predictors of adolescent substance use disorders. Addiction, 112(7), 1220–1228. doi:10.1111/add.13792 CrossRefGoogle ScholarPubMed
Kim, J.W., Kim, B.N., Lee, J., Na, C., Kee, B.S., Min, K.J., Han, D.H., Kim, J.I., & Lee, Y.S. (2016). Desynchronization of theta-phase gamma-amplitude coupling during a mental arithmetic task in children with attention deficit/hyperactivity disorder. PLoS One, 11(3), e0145288. doi:10.1371/journal.pone.0145288 CrossRefGoogle ScholarPubMed
Kumar, S., Zomorrodi, R., Ghazala, Z., Goodman, M.S., Blumberger, D.M., Cheam, A., Fischer, C., Daskalakis, Z.J., Mulsant, B.H., Pollock, B.G., & Rajji, T.K. (2017). Extent of dorsolateral prefrontal cortex plasticity and its association with working memory in patients with Alzheimer disease. JAMA Psychiatry, 74(12), 1266–1274. doi:10.1001/jamapsychiatry.2017.3292 CrossRefGoogle ScholarPubMed
Lee, R.S., Hermens, D.F., Redoblado-Hodge, M.A., Naismith, S.L., Porter, M.A., Kaur, M., White, D., Scott, E.M., & Hickie, I.B. (2013). Neuropsychological and socio-occupational functioning in young psychiatric outpatients: A longitudinal investigation. PLoS One, 8(3), e58176. doi:10.1371/journal.pone.0058176 CrossRefGoogle ScholarPubMed
Li, S., Bai, W., Liu, T., Yi, H., & Tian, X. (2012). Increases of theta-low gamma coupling in rat medial prefrontal cortex during working memory task. Brain Research Bulletin, 89(3–4), 115–123. doi:10.1016/j.brainresbull.2012.07.012 CrossRefGoogle ScholarPubMed
Lisanby, S.H., Luber, B., Perera, T., & Sackeim, H.A. (2000). Transcranial magnetic stimulation: Applications in basic neuroscience and neuropsychopharmacology. International Journal of Neuropsychopharmacology, 3, 259–273.CrossRefGoogle ScholarPubMed
Lisman, J. (2010). Working memory: The importance of theta and gamma oscillations. Current Biology, 20(11), R490–R492. doi:10.1016/j.cub.2010.04.011 CrossRefGoogle ScholarPubMed
Luck, S.J. (2005). An introduction to the event-related potential technique. Cambridge, MA: MIT Press.Google Scholar
Lundqvist, M., Herman, P., Warden, M.R., Brincat, S.L., & Miller, E.K. (2018). Gamma and beta bursts during working memory readout suggest roles in its volitional control. Nature Communications, 9(1), 394. doi:10.1038/s41467-017-02791-8 CrossRefGoogle ScholarPubMed
Lundqvist, M., Rose, J., Herman, P., Brincat, S.L., Buschman, T.J., & Miller, E.K. (2016). Gamma and beta bursts underlie working memory. Neuron, 90(1), 152–164. doi:10.1016/j.neuron.2016.02.028 CrossRefGoogle ScholarPubMed
Lutzenberger, W., Ripper, B., Busse, L., Birbaumer, N., & Kaiser, J. (2002). Dynamics of gamma-band activity during an audiospatial working memory task in humans. The Journal of Neuroscience, 22, 5630–5638.CrossRefGoogle ScholarPubMed
Mably, A.J. & Colgin, L.L. (2018). Gamma oscillations in cognitive disorders. Current Opinion in Neurobiology, 52, 182–187. doi:10.1016/j.conb.2018.07.009 CrossRefGoogle ScholarPubMed
Martino, D.J., Marengo, E., Igoa, A., Scapola, M., Ais, E.D., Perinot, L., & Strejilevich, S.A. (2009). Neurocognitive and symptomatic predictors of functional outcome in bipolar disorders: A prospective 1 year follow-up study. Journal of Affective Disorders, 116(1–2), 37–42. doi:10.1016/j.jad.2008.10.023 CrossRefGoogle ScholarPubMed
Mathalon, D.H. & Sohal, V.S. (2015). Neural oscillations and synchrony in brain dysfunction and neuropsychiatric disorders: It’s about time. JAMA Psychiatry, 72(8), 840–844. doi:10.1001/jamapsychiatry.2015.0483 CrossRefGoogle ScholarPubMed
Miller, E.K., Lundqvist, M., & Bastos, A.M. (2018). Working memory 2.0. Neuron, 100(2), 463–475. doi:10.1016/j.neuron.2018.09.023 CrossRefGoogle ScholarPubMed
Missonnier, P., Curtis, L., Ventura, J., Herrmann, F.R., & Merlo, M.C.G. (2017). Differences of temporal dynamics and signal complexity of gamma band oscillations in first-episode psychosis during a working memory task. Journal of Neural Transmission (Vienna), 124(7), 853–862. doi:10.1007/s00702-017-1728-5 CrossRefGoogle ScholarPubMed
Murray, J.D., Jaramillo, J., & Wang, X.J. (2017). Working memory and decision-making in a frontoparietal circuit model. Journal of Neuroscience, 37(50), 12167–12186. doi:10.1523/JNEUROSCI.0343-17.2017 CrossRefGoogle Scholar
Niendam, T.A., Laird, A.R., Ray, K.L., Dean, Y.M., Glahn, D.C., & Carter, C.S. (2012). Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cognitive, Affective, & Behavioral Neuroscience, 12(2), 241–268. doi:10.3758/s13415-011-0083-5 CrossRefGoogle ScholarPubMed
Noda, Y., Nakamura, M., Saeki, T., Inoue, M., Iwanari, H., & Kasai, K. (2013). Potentiation of quantitative electroencephalograms following prefrontal repetitive transcranial magnetic stimulation in patients with major depression. Neuroscience Research, 77(1–2), 70–77. doi:10.1016/j.neures.2013.06.002 CrossRefGoogle ScholarPubMed
Noda, Y., Zomorrodi, R., Saeki, T., Rajji, T.K., Blumberger, D.M., Daskalakis, Z.J., & Nakamura, M. (2017). Resting-state EEG gamma power and theta-gamma coupling enhancement following high-frequency left dorsolateral prefrontal rTMS in patients with depression. Clinical Neurophysiology, 128(3), 424–432. doi:10.1016/j.clinph.2016.12.023 CrossRefGoogle ScholarPubMed
Park, J.Y., Jhung, K., Lee, J., & An, S.K. (2013). Theta-gamma coupling during a working memory task as compared to a simple vigilance task. Neuroscience Letters, 532, 39–43. doi:10.1016/j.neulet.2012.10.061 CrossRefGoogle ScholarPubMed
Pathak, Y., Salami, O., Baillet, S., Li, Z., & Butson, C.R. (2016). Longitudinal changes in depressive circuitry in response to neuromodulation therapy. Frontiers in Neural Circuits, 10, 50. doi:10.3389/fncir.2016.00050 CrossRefGoogle ScholarPubMed
Prehn-Kristensen, A., Wiesner, C.D., & Baving, L. (2015). Early gamma-band activity during interference predicts working memory distractibility in ADHD. Journal of Attention Disorders, 19(11), 971–976. doi:10.1177/1087054712459887 CrossRefGoogle ScholarPubMed
Rajji, T.K., Zomorrodi, R., Barr, M.S., Blumberger, D.M., Mulsant, B.H., & Daskalakis, Z.J. (2017). Ordering information in working memory and modulation of gamma by theta oscillations in humans. Cerebral Cortex, 27(2), 1482–1490. doi:10.1093/cercor/bhv326 Google ScholarPubMed
Roux, F. & Uhlhaas, P.J. (2014). Working memory and neural oscillations: Alpha-gamma versus theta-gamma codes for distinct WM information? Trends in Cognitive Sciences, 18(1), 16–25. doi:10.1016/j.tics.2013.10.010 CrossRefGoogle ScholarPubMed
Roux, F., Wibral, M., Mohr, H.M., Singer, W., & Uhlhaas, P.J. (2012). Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory. Journal of Neuroscience, 32(36), 12411–12420. doi:10.1523/JNEUROSCI.0421-12.2012 CrossRefGoogle ScholarPubMed
Senkowski, D. & Gallinat, J. (2015). Dysfunctional prefrontal gamma-band oscillations reflect working memory and other cognitive deficits in schizophrenia. Biological Psychiatry, 77(12), 1010–1019. doi:10.1016/j.biopsych.2015.02.034 CrossRefGoogle Scholar
Senkowski, D., Schneider, T.R., Tandler, F., & Engel, A.K. (2009). Gamma-band activity reflects multisensory matching in working memory. Experimental Brain Research, 198(2–3), 363–372. doi:10.1007/s00221-009-1835-0 CrossRefGoogle ScholarPubMed
Tamura, M., Spellman, T.J., Rosen, A.M., Gogos, J.A., & Gordon, J.A. (2017). Hippocampal-prefrontal theta-gamma coupling during performance of a spatial working memory task. Nature Communications, 8(1), 2182. doi:10.1038/s41467-017-02108-9 CrossRefGoogle ScholarPubMed
von Lautz, A.H., Herding, J., Ludwig, S., Nierhaus, T., Maess, B., Villringer, A., & Blankenburg, F. (2017). Gamma and beta oscillations in human MEG encode the contents of vibrotactile working memory. Frontiers in Human Neuroscience, 11, 576. doi:10.3389/fnhum.2017.00576 CrossRefGoogle ScholarPubMed
Yamamoto, J., Suh, J., Takeuchi, D., & Tonegawa, S. (2014). Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell, 157(4), 845–857. doi:10.1016/j.cell.2014.04.009 CrossRefGoogle ScholarPubMed
Zhang, Y., Zhang, Y., Yu, H., Yang, Y., Li, W., & Qian, Z. (2017). Theta-gamma coupling in hippocampus during working memory deficits induced by low frequency electromagnetic field exposure. Physiology & Behavior, 179, 135–142. doi:10.1016/j.physbeh.2017.05.033 CrossRefGoogle ScholarPubMed