Evidence of language-related left hypofrontality in Major Depression: An EEG Beta band study.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
18 05 2020
18 05 2020
Historique:
received:
15
11
2019
accepted:
23
04
2020
entrez:
20
5
2020
pubmed:
20
5
2020
medline:
17
12
2020
Statut:
epublish
Résumé
Major depression (MDD) has been associated with an altered EEG frontal asymmetry measured in resting state; nevertheless, this association has showed a weak consistency across studies. In the present study, which starts from an evolutionistic view of psychiatric disorders, we investigated frontal asymmetry in MDD, using language as a probe to test the integrity of large inter- and intra-hemispheric networks and processes. Thirty MDD patients (22 women) and 32 matched controls (HC) were recruited for an EEG recording in resting state and during two linguistic tasks, phonological and semantic. Normalized alpha and beta EEG spectral bands were measured across all three conditions in the two groups. EEG alpha amplitude showed no hemispheric asymmetry, regardless of group, both at rest and during linguistic tasks. During resting state, analysis of EEG beta revealed a lack of hemispheric asymmetry in both groups, but during linguistic tasks, HC exhibited the typical greater left frontal beta activation, whereas MDD patients showed a lack of frontal asymmetry and a significantly lower activation of left frontal sites. In depressed patients, positive affect was negatively correlated with depression levels and positively correlated with left frontal EEG beta amplitude. Language represents the human process that requires the largest level of integration between and within the hemispheres; thus, language asymmetry was a valid probe to test the left frontal alteration encompassing highly impairing psychiatric disorders, such as schizophrenia and MDD. Indeed, these severe diseases are marked by delusions, ruminations, thought disorders, and hallucinations, all of which have a clear linguistic or metalinguistic basis.
Identifiants
pubmed: 32424130
doi: 10.1038/s41598-020-65168-w
pii: 10.1038/s41598-020-65168-w
pmc: PMC7235005
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8166Références
Elliott, R. The neuropsychological profile in unipolar depression. Trends in Cognitive Sciences 2, 447–454 (1998).
pubmed: 21227276
doi: 10.1016/S1364-6613(98)01235-2
Drevets, W. C. Neuroimaging studies of Mood Disorders. Biological Psychiatry 48, 813–829 (2000).
pubmed: 11063977
doi: 10.1016/S0006-3223(00)01020-9
Davidson, R. J., Pizzagalli, D., Nitschke, J. B. & Putnam, K. Depression: Perspectives from Affective Neuroscience. Annual Review of Psychology 53, 545–574 (2002).
pubmed: 11752496
doi: 10.1146/annurev.psych.53.100901.135148
Siddiqui, S. V., Chatterjee, U., Kumar, D., Siddiqui, A. & Goyal, N. Neuropsychology of prefrontal cortex. Indian Journal of Psychiatry 50, 202–208 (2008).
pubmed: 19742233
pmcid: 2738354
doi: 10.4103/0019-5545.43634
Miller, E. K. The prefrontal cortex and cognitive control. Nature Reviews Neuroscience 1, 59–65 (2000).
pubmed: 11252769
doi: 10.1038/35036228
pmcid: 11252769
Allen, J. J. B., Urry, H. L., Hitt, S. K. & Coan, J. A. The stability of resting frontal electroencephalographic asymmetry in depression. Psychophysiology 41, 269–280 (2004).
pubmed: 15032992
doi: 10.1111/j.1469-8986.2003.00149.x
Coan, J. A. & Allen, J. J. B. The state and trait nature of frontal EEG asymmetry in emotion. In K., Hugdahl & R.J., Davidson (Eds.), The asymmetrical brain (2nd ed., pp. 565-615). Cambridge, MA: MIT press (2003).
Davidson, R. J. Anterior electrophysiological asymmetries, emotion, and depression: Conceptual and methodological conundrums. Psychophysiology 35, 607–614 (1998).
pubmed: 9715104
doi: 10.1017/S0048577298000134
Cantero, J. L., Atienza, M. & Salas, R. M. Human alpha oscillations in wakefulness, drowsiness period, and REM sleep: different electroencephalographic phenomena within the alpha band. Clinical Neurophysiology 32, 54–71 (2002).
pubmed: 11915486
doi: 10.1016/S0987-7053(01)00289-1
pmcid: 11915486
Laufs, H. et al. EEG-correlated fMRI of human alpha activity. NeuroImage 19, 1463–1476 (2003).
pubmed: 12948703
doi: 10.1016/S1053-8119(03)00286-6
Allen, J. J. B., Iacono, W. G., Depue, R. A. & Arbisi, P. Regional electroencephalographic asymmetries in bipolar seasonal affective disorder before and after exposure to bright light. Biological Psychiatry 33, 642–646 (1993).
pubmed: 8329494
doi: 10.1016/0006-3223(93)90104-L
Allen, J. J. B., Coan, J. A. & Nazarian, M. What’s the difference? Issue and assumptions in the use of difference scores and other metrics of anterior brain asymmetry in emotion. Biological Psychology 67, 183–218 (2004).
pubmed: 15130531
doi: 10.1016/j.biopsycho.2004.03.007
pmcid: 15130531
Stewart, J. L., Coan, J. A., Towers, D. N. & Allen, J. J. B. Resting and task-elicited prefrontal EEG alpha asymmetry in depression: Support for the capability model. Psychophysiology 51, 446–455 (2014).
pubmed: 24611480
pmcid: 3984363
doi: 10.1111/psyp.12191
Bruder, G. E. et al. Regional brain asymmetries in major depression with or without anxiety disorder: A quantitative electroencephalographic study. Biological Psychiatry 41, 939–948 (1997).
pubmed: 9110099
doi: 10.1016/S0006-3223(96)00260-0
pmcid: 9110099
Pizzagalli, D. A. et al. Brain electrical tomography in depression: the importance of symptom severity, anxiety, and melancholic feature. Biological Psychiatry 52, 73–85 (2002).
pubmed: 12113998
doi: 10.1016/S0006-3223(02)01313-6
pmcid: 12113998
Reid, S. A., Duke, L. M. & Allen, J. J. B. Resting frontal electroencephalographic asymmetry in depression: inconsistencies suggest the need to identify mediating factors. Psychophysiology 35, 389–404 (1998).
pubmed: 9643053
doi: 10.1111/1469-8986.3540389
pmcid: 9643053
Van der Vinne, N., Vollebregt, M. A., van Putten, M. J. A. M. & Arns, M. Frontal alpha asymmetry as a diagnostic marker in depression: Fact or fiction? A meta-analysis. NeuroImage: Clinical 16, 79–87 (2017).
doi: 10.1016/j.nicl.2017.07.006
Coan, J. A., Allen, J. J. B. & McKnight, P. E. A capability model of individual differences in frontal EEG asymmetry. Biological Psychology 72, 198–207 (2006).
pubmed: 16316717
doi: 10.1016/j.biopsycho.2005.10.003
pmcid: 16316717
Coan, J. A., Allen, J. J. B. & Harmon-Jones, E. Voluntary facial expression and hemispheric asymmetry over the frontal cortex. Psychophysiology 38, 912–925 (2001).
pubmed: 12240668
doi: 10.1111/1469-8986.3860912
pmcid: 12240668
Ekman, P. & Davidson, J. R. Voluntary smiling changes regional brain activity. Psychological Science 4, 342–345 (1993).
doi: 10.1111/j.1467-9280.1993.tb00576.x
Stewart, J. L., Coan, J. A., Towers, D. N. & Allen, J. J. B. Frontal EEG asymmetry during emotional challenge differentiates individuals with and without lifetime major depressive disorder. Journal of Affective Disorders 129, 167–174 (2011).
pubmed: 20870293
doi: 10.1016/j.jad.2010.08.029
Potter, G. G., Kittinger, J. D., Wagner, H. R., Steffens, D. C. & Krishnan, K. R. R. Prefrontal neuropsychological predictors of treatment remission in late-life depression. Neuropsychopharmacology 29, 2266–2271 (2004).
pubmed: 15340392
doi: 10.1038/sj.npp.1300551
Story, T. J., Potter, G. G., Attix, D. K., Welsh-Bohmer, K. A. & Steffens, D. C. Neurocognitive correlates of response to treatment in late-life depression. American Journal of Geriatric Psychiatry 16, 752–759 (2008).
pubmed: 18697883
doi: 10.1097/JGP.0b013e31817e739a
Roiser, J. P., Elliott, R. & Sahakian, B. J. Cognitive mechanisms of treatment in depression. Neuropsychopharmacology 37, 117–136 (2012).
pubmed: 21976044
doi: 10.1038/npp.2011.183
Harvey, P. O. et al. Executive functions and updating of the contents of working memory in unipolar depression. Journal of Psychiatric Research 38, 567–576 (2004).
pubmed: 15458852
doi: 10.1016/j.jpsychires.2004.03.003
Fossati, P., Amar, G., Raoux, N., Ergis, A. M. & Allilaire, J. F. Executive functioning and verbal memory in young patients with unipolar depression and schizophrenia. Psychiatry Research 89, 171–187 (1999).
pubmed: 10708264
doi: 10.1016/S0165-1781(99)00110-9
Nebes, R. D. et al. Decreased working memory and processing speed mediate cognitive impairment in geriatric depression. Psychological Medicine 30, 679–691 (2000).
pubmed: 10883722
doi: 10.1017/S0033291799001968
Majer, M. et al. Impaired divided attention predicts delayed response and risk to relapse in subjects with depressive disorders. Psychological Medicine 34, 1453–1463 (2004).
pubmed: 15724876
doi: 10.1017/S0033291704002697
Lee, R. S., Hermens, D. F., Porter, M. A. & Redoblado-Hodge, M. A. A meta-analysis of cognitive deficits in first-episode major depressive disorder. Journal of Affective Disorders 140, 113–124 (2012).
pubmed: 22088608
doi: 10.1016/j.jad.2011.10.023
Rock, P. L., Roiser, J. P., Riedel, W. J. & Blackwell, A. D. Cognitive impairment in depression: A systematic review and meta-analysis. Psychological Medicine 44, 2029–2040 (2014).
pubmed: 24168753
doi: 10.1017/S0033291713002535
pmcid: 24168753
Levin, R. L., Heller, W., Mohanty, A., Herringhton, J. D. & Miller, G. A. Cognitive Deficits in Depression and Functional Specificity of Regional Brain Activity. Cognitive Therapy and Research 31, 211–233 (2007).
doi: 10.1007/s10608-007-9128-z
Craddock, N., O’Donovan, M. C. & Owen, M. J. Psychosis genetics: Modeling the relationship between schizophrenia, bipolar disorder and mixed (or “schizoaffective”) psychoses. Schizophrenia Bulletin 35, 482–490 (2010).
doi: 10.1093/schbul/sbp020
Heckers, S. et al. Structure of the psychotic disorders classification in DSM-5. Schizophrenia Research 150, 11–14 (2013).
pubmed: 23707641
doi: 10.1016/j.schres.2013.04.039
pmcid: 23707641
Cuthbert, B. N. & Insel, T. R. Toward new approaches to psychotic disorders: The NIMH research domain criteria project. Schizophrenia Bulletin 36, 1061–1062 (2010).
pubmed: 20929969
pmcid: 2963043
doi: 10.1093/schbul/sbq108
Spironelli, C., Penolazzi, B., Vio, C. & Angrilli, A. Cortical reorganization in dyslexic children after a phonological training: evidence from early evoked potentials. Brain 133, 3385–3395 (2010).
pubmed: 20688811
doi: 10.1093/brain/awq199
pmcid: 20688811
Spironelli, C. & Angrilli, A. Brain plasticity in aphasic patients: Intra- and inter-hemispheric reorganisation of the whole linguistic network probed by N150 and N350 components. Scientific Reports 5, 12541, https://doi.org/10.1038/srep12541 (2015).
doi: 10.1038/srep12541
pubmed: 26217919
pmcid: 4649892
Angrilli, A. et al. Schizophrenia as failure of left hemispheric dominance for the phonological component of language. Plos ONE 4(2), e4507, https://doi.org/10.1371/journal.pone.0004507 (2009).
doi: 10.1371/journal.pone.0004507
pubmed: 19223971
pmcid: 2637431
Spironelli, C. & Angrilli, A. Language-related gamma EEG frontal reduction is associated with positive symptoms in schizophrenia patients. Schizophrenia Research 165, 22–29 (2015).
pubmed: 25913900
doi: 10.1016/j.schres.2015.04.003
pmcid: 25913900
Spironelli, C., Angrilli, A. & Stegagno, L. Failure of language lateralization in schizophrenia patients: an ERP study on early linguistic components. Journal of Psychiatry and Neuroscience 33, 235–243 (2008).
pubmed: 18592042
pmcid: 18592042
Spironelli, C., Angrilli, A., Calogero, A. & Stegagno, L. Delta EEG band as a marker of left hypofrontality for language in schizophrenia patients. Schizophrenia Bulletin 37, 757–767 (2011).
pubmed: 19933713
doi: 10.1093/schbul/sbp145
pmcid: 19933713
Crow, T. J. Schizophrenia as failure of hemispheric dominance for language. Trends in Neurosciences 20, 339–343 (1997).
pubmed: 9246721
doi: 10.1016/S0166-2236(97)01071-0
pmcid: 9246721
Crow, T. J. Schizophrenia as the price that Homo sapiens pays for language: a resolution of the central paradox in the origin of the species. Brain Research Reviews 31, 118–129 (2000).
pubmed: 10719140
doi: 10.1016/S0165-0173(99)00029-6
pmcid: 10719140
Spironelli, C. & Angrilli, A. Language lateralization in Phonological, Semantic and Orthographic tasks: a slow evoked potential study. Behavioral Brain Research 175, 296–304 (2006).
doi: 10.1016/j.bbr.2006.08.038
Angrilli, A., Elbert, T., Cusumano, S., Stegagno, L. & Rockstroh, B. Temporal dynamics of linguistic processes are reorganized in aphasics’ cortex: an EEG mapping study. Neuroimage 20, 657–666 (2003).
pubmed: 14568442
doi: 10.1016/S1053-8119(03)00395-1
pmcid: 14568442
Kelley, N. J., Hortensius, R. & Harmon-Jones, E. When anger leads to rumination: Induction of relative right Frontal cortical activity with transcranial Direct Current Stimulation increases anger-related rumination. Psychological Science 24, 475–481 (2013).
pubmed: 23449843
doi: 10.1177/0956797612457384
pmcid: 23449843
Ahern, G. L. & Schwartz, G. E. Differential lateralization for positive and negative emotion in the human brain: EEG spectral analysis. Neuropsychologia 23, 745–755 (1985).
pubmed: 4080136
doi: 10.1016/0028-3932(85)90081-8
pmcid: 4080136
Zhao, G. et al. Asymmetric hemisphere activation in tenderness: evidence from EEG signals. Scientific Reports 8, 8029, https://doi.org/10.1038/s41598-018-26133-w (2018).
doi: 10.1038/s41598-018-26133-w
pubmed: 29795119
pmcid: 5966511
Wyczesany, M., Capotosto, P., Zappasodi, F. & Prete, G. Hemispheric asymmetries and emotions: Evidence from effective connectivity. Neuropsychologia 121, 98–105 (2018).
pubmed: 30352221
doi: 10.1016/j.neuropsychologia.2018.10.007
Demaree, H. A., Everhart, D. E., Youngstrom, E. A. & Harrison, D. W. Brain Lateralization of Emotional Processing: Historical Roots and a Future Incorporating “Dominance”. Behavioral and Cognitive Neuroscience Reviews 4, 3–20 (2005).
pubmed: 15886400
doi: 10.1177/1534582305276837
Beer, M. D. Psychosis: A history of the concept. Comprehensive Psychiatry 37, 273–291 (1996).
pubmed: 8826692
doi: 10.1016/S0010-440X(96)90007-3
Andreasen, N. C. et al. Hypofrontality in neuroleptic-naïve patients and in patients with chronic schizophrenia: assessment with xenon 133 single-photon emission computed tomography and the Tower of London. Archives of General Psychiatry 49, 943–958 (1992).
pubmed: 1360199
doi: 10.1001/archpsyc.1992.01820120031006
Insel, T. R. Faulty Circuits. Scientific American, 44–51 (2010).
Price, C. J. The anatomy of language: A review of 100 fMRI studies published in 2009. Annals of the New York Academy of Sciences 1191, 62–88 (2010).
pubmed: 20392276
doi: 10.1111/j.1749-6632.2010.05444.x
Huth, A. G., de Heer, W. A., Griffiths, T. L., Theunissen, F. E. & Gallant, J. L. Natural speech reveals the semantic maps that tile human cerebral cortex. Nature 532, 453–458 (2016).
pubmed: 27121839
pmcid: 4852309
doi: 10.1038/nature17637
Mesholam-Gately, R. I., Giuliano, A. J., Goff, K. P., Faraone, S. V. & Seidman, L. J. Neurocognition in First-Episode Schizophrenia: A Meta-Analytic Review. Neuropsychology 23, 315–336 (2009).
pubmed: 19413446
doi: 10.1037/a0014708
Spironelli, C. & Angrilli, A. Brain plasticity in aphasic patients: intra- and inter-hemispheric reorganisation of the whole linguistic network probed by N150 and N350 components. Scientific Reports 5, 1254, https://doi.org/10.1038/srep12541 (2015).
doi: 10.1038/srep12541
Grajny, K. et al. Depression Symptoms in Chronic Left Hemisphere Stroke Are Related to Dorsolateral Prefrontal Cortex Damage. Journal of Neuropsychiatry and Clinical Neuroscience 28, 292–298 (2016).
doi: 10.1176/appi.neuropsych.16010004
Indefrey, P. & Levelt, W. J. M. The spatial and temporal signatures of word production components. Cognition 92, 101–144 (2004).
doi: 10.1016/j.cognition.2002.06.001
Paulesu, E., Frith, C. D. & Frackowiak, R. S. J. The neural correlates of the verbal component of working memory. Nature 362, 342–345 (1993).
pubmed: 8455719
doi: 10.1038/362342a0
pmcid: 8455719
Bookheimer, S. Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annual Review of Neuroscience 25, 151–188 (2002).
pubmed: 12052907
doi: 10.1146/annurev.neuro.25.112701.142946
Hagoort, P. On Broca, brain, and binding: a new framework. TRENDS in Cognitive Sciences 9, 416–423 (2005).
pubmed: 16054419
doi: 10.1016/j.tics.2005.07.004
Koechlin, E. & Jubault, T. Broca’s area and the hierarchical organization of human behavior. Neuron 50, 963–974 (2006).
pubmed: 16772176
doi: 10.1016/j.neuron.2006.05.017
Oldfield, R. C. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9, 97–113 (1971).
doi: 10.1016/0028-3932(71)90067-4
Hamilton, M. Rating depressive patients. Journal of Clinical Psychiatry 41, 21–24 (1980).
pubmed: 7440521
Beck, A. T., Steer, R. A. & Brown, G. K. Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation (1996).
Spielberger, C. D., Gorssuch, R. L., Lushene, P. R., Vagg, P. R. & Jacobs, G. A. Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press (1983).
Mroczek, D. K. & Kolarz, C. M. The effect of age on positive and negative affect: a developmental perspective on happiness. Journal of personality and social psychology 75, 1333–1349 (1998).
pubmed: 9866191
doi: 10.1037/0022-3514.75.5.1333
Bortolini, V., Tagliavini, C. & Zampolli, A. Lessico di frequenza della lingua italiana contemporanea [Lexical frequency in current Italian]. Milano, Italy: Aldo Garzanti Editore (1972).
Oostenveld, R. & Praamstra, P. The five percent electrode system for high-resolution EEG and ERP measurements. Clinical Neurophysiology 112, 713–719 (2001).
pubmed: 11275545
doi: 10.1016/S1388-2457(00)00527-7
Ille, N., Berg, P. & Scherg, M. Artifact correction of the ongoing EEG using spatial filters based on artifact and brain signal topographies. Journal of Clinical Neurophysiology 19, 113–124 (2002).
pubmed: 11997722
doi: 10.1097/00004691-200203000-00002
pmcid: 11997722
Spironelli, C., Manfredi, M. & Angrilli, A. Beta EEG band: a measure of functional brain damage and language reorganization in aphasic patients after recovery. Cortex 49, 2650–2660 (2013).
pubmed: 23810123
doi: 10.1016/j.cortex.2013.05.003
pmcid: 23810123