nach oben

European Archives of Psychiatry and Clinical Neuroscience

Erschienen in:

15.06.2023 | Original Paper

Brain–heart interaction disruption in major depressive disorder: disturbed rhythm modulation of the cardiac cycle on brain transient theta bursts

verfasst von: Hongliang Zhou, Tingting Xiong, Zhongpeng Dai, Haowen Zou, Xvmiao Wang, Hao Tang, Yinghong Huang, Hao Sun, Wei You, Zhijian Yao, Qing Lu

Erschienen in: European Archives of Psychiatry and Clinical Neuroscience | Ausgabe 3/2024

Einloggen, um Zugang zu erhalten

Abstract

Brain neurons support arousal and cognitive activity in the form of spectral transient bursts and cooperate with the peripheral nervous system to adapt to the surrounding environment. However, the temporal dynamics of brain–heart interactions have not been confirmed, and the mechanism of brain–heart interactions in major depressive disorder (MDD) remains unclear. This study aimed to provide direct evidence for brain–heart synchronization in temporal dynamics and clarify the mechanism of brain–heart interaction disruption in MDD. Eight-minute resting-state (closed eyes) electroencephalograph and electrocardiogram signals were acquired simultaneously. The Jaccard index (JI) was used to measure the temporal synchronization between cortical theta transient bursts and cardiac cycle activity (diastole and systole) in 90 MDD patients and 44 healthy controls (HCs) at rest. The deviation JI was used to reflect the equilibrium of brain activity between diastole and systole. The results showed that the diastole JI was higher than the systole JI in both the HC and MDD groups; compared to HCs, the deviation JI attenuated at F4, F6, FC2, and FC4 in the MDD patients. The eccentric deviation JI was negatively correlated with the despair factor scores of the HAMD, and after 4 weeks of antidepressant treatment, the eccentric deviation JI was positively correlated with the despair factor scores of the HAMD. It was concluded that brain–heart synchronization existed in the theta band in healthy individuals and that disturbed rhythm modulation of the cardiac cycle on brain transient theta bursts at right frontoparietal sites led to brain–heart interaction disruption in MDD.

Nur mit Berechtigung zugänglich

Otte C, Gold SM, Penninx BW, Pariante CM, Etkin A, Fava M, Mohr DC, Schatzberg AF (2016) Major depressive disorder. Nat Rev Dis Primers 2:16065. https://doi.org/10.1038/nrdp.2016.65CrossRefPubMed

Hare DL, Toukhsati SR, Johansson P, Jaarsma T (2014) Depression and cardiovascular disease: a clinical review. Eur Heart J 35:1365–1372. https://doi.org/10.1093/eurheartj/eht462CrossRefPubMed

Rajan S, McKee M, Rangarajan S, Bangdiwala S, Rosengren A, Gupta R, Kutty VR, Wielgosz A, Lear S, AlHabib KF, Co HU, Lopez-Jaramillo P, Avezum A, Seron P, Oguz A, Kruger IM, Diaz R, Nafiza MN, Chifamba J, Yeates K, Kelishadi R, Sharief WM, Szuba A, Khatib R, Rahman O, Iqbal R, Bo H, Yibing Z, Wei L, Yusuf S, Prospective Urban Rural Epidemiology (PURE) Study Investigators (2020) Association of symptoms of depression with cardiovascular disease and mortality in low-, middle-, and high-income countries. JAMA Psychiatry 77:1052–1063. https://doi.org/10.1001/jamapsychiatry.2020.1351CrossRefPubMedPubMedCentral

Huimahn AC (2017) Listening with your heart. Sci Transl Med 9(414):1224. https://doi.org/10.1126/scitranslmed.aaq1224CrossRef

John PC (2021) The head and the heart of fear. Sience 374(6570):937–938. https://doi.org/10.1126/science.abm6790CrossRef

Andrea Z, Mauro GP, Eleonora P, Costantini M, Ferri F (2022) Brain–heart interactions are modulated across the respiratory cycle via interoceptive attention. NeuroImage 262:119548. https://doi.org/10.1016/j.neuroimage.2022.119548CrossRef

Northoff G (2016) Spatiotemporal psychopathology I: no rest for the brain’s resting state activity in depression? Spatiotemporal psychopathology of depressive symptoms. J Affect Disord 190:854–866. https://doi.org/10.1016/j.jad.2015.05.007CrossRefPubMed

Skora LI, Livermore JJA, Roelofs K (2022) The functional role of cardiac activity in perception and action. Neurosci Biobehav Rev 137:104655. https://doi.org/10.1016/j.neubiorev.2022.104655CrossRefPubMed

Mann DL, Zipes DP, Libby P, Bonow RO (2015) Braunwald’s heart disease: a textbook of cardiovascular medicine. Elsevier, Amsterdam

10.

Young A, Hunt T, Ericson M (2021) The slowest shared resonance: a review of electromagnetic field oscillations between central and peripheral nervous systems. Front Hum Neurosci 15:796455. https://doi.org/10.3389/fnhum.2021.796455CrossRefPubMed

11.

Schmidt-Hieber C, Nolan MF (2017) Synaptic integrative mechanisms for spatial cognition. Nat Neurosci 20(11):1483–1492. https://doi.org/10.1038/nn.4652CrossRefPubMed

12.

Park HD, Bernasconi F, Bello-Ruiz J, Pfeiffer C, Salomon R, Blanke O (2016) Transient modulations of neural responses to heartbeats covary with bodily self-consciousness. J Neurosci 36(32):8453–8460. https://doi.org/10.1523/JNEUROSCI.0311-16.2016CrossRefPubMedPubMedCentral

13.

Park HD, Bernasconi F, Salomon R, Tallon-Baudry C, Spinelli L, Seeck M, Schaller K, Blanke O (2018) Neural Sources and underlying mechanisms of neural responses to heartbeats, and their role in bodily self-consciousness: an intracranial EEG study. Cereb Cortex 28(7):2351–2364. https://doi.org/10.1093/cercor/bhx136CrossRefPubMed

14.

Kato Y, Takei Y, Umeda S, Mimura M, Fukuda M (2020) Alterations of heartbeat evoked magnetic fields induced by sounds of disgust. Front Psychiatry 11:683. https://doi.org/10.3389/fpsyt.2020.00683CrossRefPubMedPubMedCentral

15.

Hsueh B, Chen R, Jo Y, Tang D, Raffiee M, Kim YS, Inoue M, Randles S, Ramakrishnan C, Patel S, Kim DK, Liu TX, Kim SH, Tan L, Mortazavi L, Cordero A, Shi J, Zhao M, Ho TT, Crow A, Yoo AW, Raja C, Evans K, Bernstein D, Zeineh M, Goubran M, Deisseroth K (2023) Cardiogenic control of affective behavioural state. Nature 615(7951):292–299. https://doi.org/10.1038/s41586-023-05748-8CrossRefPubMedPubMedCentral

16.

Machetanz K, Berelidze L, Guggenberger R, Alireza G (2021) Brain–heart interaction during transcutaneous auricular vagus nerve stimulation. Front Neurosci 15:632697. https://doi.org/10.3389/fnins.2021.632697CrossRefPubMedPubMedCentral

17.

Shokri-Kojori E, Tomasi D, Volkow ND (2018) An autonomic network: synchrony between slow rhythms of pulse and brain resting state is associated with personality and emotions. Cereb Cortex 28:3356–3371. https://doi.org/10.1093/cercor/bhy144CrossRefPubMedPubMedCentral

18.

Vorkapić M, Savić A, Janković M, Useinović N, Isaković M, Puškaš N, Stanojlović O, Hrnčić D (2020) Alterations of medial prefrontal cortex bioelectrical activity in experimental model of isoprenaline-induced myocardial infarction. PLoS ONE 15:e0232530. https://doi.org/10.1371/journal.pone.0232530CrossRefPubMedPubMedCentral

19.

Kim J, Jeong B (2019) heartbeat induces a cortical theta-synchronized network in the resting state. eNeuro 6:ENEURO.0200-19.2019. https://doi.org/10.1523/ENEURO.0200-19.2019CrossRefPubMedPubMedCentral

20.

Jones SR (2016) When brain rhythms aren’t ‘rhythmic’: implication for their mechanisms and meaning. Curr Opin Neurobiol 40:72–80. https://doi.org/10.1016/j.conb.2016.06.010CrossRefPubMedPubMedCentral

21.

Sherman MA, Lee S, Law R, Thorn CA, Hämäläinen MS, Moore CI, Jones SR (2016) Neural mechanisms of transient neocortical beta rhythms: converging evidence from humans, computational modeling, monkeys, and mice. Proc Natl Acad Sci USA 113:E4885-4894. https://doi.org/10.1073/pnas.1604135113CrossRefPubMedPubMedCentral

22.

van Ede F, Quinn AJ, Woolrich MW, Nobre AC (2018) Neural oscillations: sustained rhythms or transient burst-events? Trends Neurosci 41:415–417. https://doi.org/10.1016/j.tins.2018.04.004CrossRefPubMedPubMedCentral

23.

Liu Y, Nour MM, Schuck NW, Behrens TEJ, Dolan RJ (2022) Decoding cognition from spontaneous neural activity. Nat Rev Neurosci 23(4):204–214. https://doi.org/10.1038/s41583-022-00570-zCrossRefPubMed

24.

Zich C, Quinn AJ, Mardell LC, Ward NS, Bestmann S (2020) Dissecting transient burst events. Trends Cogn Sci 24:784–788. https://doi.org/10.1016/j.tics.2020.07.004CrossRefPubMedPubMedCentral

25.

Stringer C, Pachitariu M, Steinmetz N, Reddy CB, Carandini M, Harris KD (2019) Spontaneous behaviors drive multidimensional, brain wide activity. Science 364:255. https://doi.org/10.1126/science.aav7893CrossRefPubMedPubMedCentral

26.

Tal I, Neymotin S, Bickel S, Lakatos P, Schroeder CE (2020) Oscillatory bursting as a mechanism for temporal coupling and information coding. Front Comput Neurosci 14:82. https://doi.org/10.3389/fncom.2020.00082CrossRefPubMedPubMedCentral

27.

Kircanski K, Williams LM, Gotlib IH (2019) Heart rate variability as a biomarker of anxious depression response to antidepressant medication. Depress Anxiety 36:63–71. https://doi.org/10.1002/da.22843CrossRefPubMed

28.

Patron E, Messerotti Benvenuti S, Favretto G, Gasparotto R, Palomba D (2015) Depression is associated with increased vagal withdrawal during unpleasant emotional imagery after cardiac surgery. Auton Neurosci 189:75–82. https://doi.org/10.1016/j.autneu.2015.02.002CrossRefPubMed

29.

Tonhajzerova I, Visnovcova Z, Mestanikova A, Jurko A, Mestanik M (2016) Cardiac vagal control and depressive symptoms in response to negative emotional stress. Adv Exp Med Biol 934:23–30. https://doi.org/10.1007/5584_2016_17CrossRefPubMed

30.

Zhou H, Zou H, Dai Z, Zhao S, Hua L, Xia Y, Han Y, Yan R, Tang H, Huang Y, Du Y, Wang X, Yao Z, Lu Q (2022) Interoception dysfunction contributes to the negative emotional bias in major depressive disorder. Front Psychiatry 13:874859. https://doi.org/10.3389/fpsyt.2022.874859CrossRefPubMedPubMedCentral

31.

Bair A, Marksteiner J, Falch R, Ettinger U, Reyes Del Paso GA, Duschek S (2021) Features of autonomic cardiovascular control during cognition in major depressive disorder. Psychophysiology 58:e13628. https://doi.org/10.1111/psyp.13628CrossRefPubMed

32.

Hoffmann A, Ettinger U, Reyes Del Paso GA, Duschek S (2017) Executive function and cardiac autonomic regulation in depressive disorders. Brain Cogn 118:108–117. https://doi.org/10.1016/j.bandc.2017.08.003CrossRefPubMed

33.

Gatus A, Jamieson G, Stevenson B (2022) Past and future explanations for depersonalization and derealization disorder: a role for predictive coding. Front Hum Neurosci 16:744487. https://doi.org/10.3389/fnhum.2022.744487CrossRefPubMedPubMedCentral

34.

Terhaar J, Viola FC, Bär KJ, Debener S (2012) Heartbeat evoked potentials mirror altered body perception in depressed patients. Clin Neurophysiol 123:1950–1957. https://doi.org/10.1016/j.clinph.2012.02.086CrossRefPubMed

35.

Koch C, Wilhelm M, Salzmann S, Rief W, Euteneuer F (2019) A meta-analysis of heart rate variability in major depression. Psychol Med 49:1948–1957. https://doi.org/10.1017/S0033291719001351CrossRefPubMed

36.

Northoff G, Wiebking C, Feinberg T, Panksepp J (2011) The ‘resting-state hypothesis’ of major depressive disorder-a translational subcortical-cortical framework for a system disorder. Neurosci Biobehav Rev 35(9):1929–1945. https://doi.org/10.1016/j.neubiorev.2010.12.007CrossRefPubMed

37.

Tumati S, Paulus MP, Northoff G (2021) Out-of-step: brain–heart desynchronization in anxiety disorders. Mol Psychiatry 26:1726–1737. https://doi.org/10.1038/s41380-021-01029-wCrossRefPubMed

38.

Pollatos O, Traut-Mattausch E, Schandry R (2009) Differential effects of anxiety and depression on interoceptive accuracy. Depress Anxiety 26(2):167–173. https://doi.org/10.1002/da.20504CrossRefPubMed

39.

Müller LE, Schulz A, Andermann M, Gäbel A, Gescher DM, Spohn A, Herpertz SC, Bertsch K (2015) Cortical representation of afferent bodily signals in borderline personality disorder: neural correlates and relationship to emotional dysregulation. JAMA Psychiatry 72:1077–1086. https://doi.org/10.1001/jamapsychiatryCrossRefPubMed

40.

Borchardt V, Fan Y, Dietz M, Melendez ALH, Bajbouj M, Gärtner M, Li M, Walter M, Grimm S (2018) Echoes of affective stimulation in brain connectivity networks. Cereb Cortex 28:4365–4378. https://doi.org/10.1093/cercor/bhx290CrossRefPubMed

41.

Pizzagalli DA, Webb CA, Dillon DG, Tenke CE, Kayser J, Goer F, Fava M, McGrath P, Weissman M, Parsey R, Adams P, Trombello J, Cooper C, Deldin P, Oquendo MA, McInnis MG, Carmody T, Bruder G, Trivedi MH (2018) Pretreatment rostral anterior cingulate cortex theta activity in relation to symptom improvement in depression: a randomized clinical trial. JAMA Psychiatry 75(6):547–554. https://doi.org/10.1001/jamapsychiatry.2018.0252CrossRefPubMedPubMedCentral

42.

Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62. https://doi.org/10.1136/jnnp.23.1.56CrossRefPubMedPubMedCentral

43.

Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32:50–55. https://doi.org/10.1111/j.2044-8341.1959.tb00467.xCrossRefPubMed

44.

Chenguang J, Hongliang Z, Limin C, Zhou Z (2021) Problem solving therapy improves effortful cognition in major depression front. Psychiatry 12:607718. https://doi.org/10.3389/fpsyt.2021.607718CrossRef

45.

Chaumon M, Bishop DV, Busch NA (2015) A practical guide to the selection of independent components of the electroencephalogram for artifact correction. J Neurosci Methods 250:47–63. https://doi.org/10.1016/j.jneumeth.2015.02.025CrossRefPubMed

46.

Seedat ZA, Quinn AJ, Vidaurre D, Liuzzi L, Gascoyne LE, Hunt BAE, O’Neill GC, Pakenham DO, Mullinger KJ, Morris PG, Woolrich MW, Brookes MJ (2020) The role of transient spectral ‘bursts’ in functional connectivity: a magnetoencephalography study. Neuroimage 209:116537. https://doi.org/10.1016/j.neuroimage.2020.116537CrossRefPubMed

47.

Mainali KP, Slud E, Singer MC, Fagan WF (2022) A Better index for analysis of co-occurrence and similarity. Sci Adv 28:eabj9204. https://doi.org/10.1126/sciadv.abj9204CrossRef

48.

Furukawa TA, Cipriani A, Cowen PJ, Leucht S, Egger M, Salanti G (2019) Optimal dose of selective serotonin reuptake inhibitors, venlafaxine, and mirtazapine in major depression: a systematic review and dose–response meta-analysis. Lancet Psychiatry 6:6019. https://doi.org/10.1016/S2215-0366(19)30217-2CrossRef

49.

McCraty R, Shaffer F (2015) Heart rate variability: new perspectives on physiological mechanisms, assessment of self-regulatory capacity, and health risk. Glob Adv Health Med 4:46–61. https://doi.org/10.7453/gahmj.2014.073CrossRefPubMedPubMedCentral

50.

Galvez-Pol A, McConnell R, Kilner JM (2020) Active sampling in visual search is coupled to the cardiac cycle. Cognition 196:104149. https://doi.org/10.1016/j.cognition.2019.104149CrossRefPubMed

51.

Grund M, Pabst M, Dabbagh A, Stephani T, Nierhaus T, Gaebler M, Villringer A (2022) Respiration, heartbeat, and conscious tactile perception. J Neurosci 42:643–656. https://doi.org/10.1523/JNEUROSCI.0592-21.2021CrossRefPubMedPubMedCentral

52.

Dworkin BR, Elbert T, Rau H, Birbaumer N, Pauli P, Droste C, Brunia CH (1994) Central effects of baroreceptor activation in humans: attenuation of skeletal reflexes and pain perception. Proc Natl Acad Sci USA 91:6329–6333. https://doi.org/10.1073/pnas.91.14.6329CrossRefPubMedPubMedCentral

53.

Martins AQ, Ring C, McIntyre D, Edwards L, Martin U (2009) Effects of unpredictable stimulation on pain and nociception across the cardiac cycle. Pain 147:84–90. https://doi.org/10.1016/j.pain.2009.08.016CrossRefPubMed

54.

Nyklícek I, Wijnen V, Rau H (2005) Effects of baroreceptor stimulation and opioids on the auditory startle reflex. Psychophysiology 42:213–222. https://doi.org/10.1111/j.1469-8986.2005.00273.xCrossRefPubMed

55.

Richter S, Schulz A, Port J, Blumenthal TD, Schächinger H (2009) Cardiopulmonary baroreceptors affect reflexive startle eye blink. Physiol Behav 98:587–593. https://doi.org/10.1016/j.physbeh.2009.09.010CrossRefPubMed

56.

Young CB, Raz G, Everaerd D, Beckmann CF, Tendolkar I, Hendler T, Fernández G, Hermans EJ (2017) Dynamic shifts in large-scale brain network balance as a function of arousal. J Neurosci 37:281–290. https://doi.org/10.1523/JNEUROSCI.1759-16.2016CrossRefPubMedPubMedCentral

57.

Esterman M, Rothlein D (2019) Models of sustained attention. Curr Opin Psychol 29:174–180. https://doi.org/10.1016/j.copsyc.2019.03.005CrossRefPubMed

58.

Bogdány T, Perakakis P, Bódizs R, Simor P (2022) The heartbeat evoked potential is a questionable biomarker in nightmare disorder: a replication study. Neuroimage Clin 33:102933. https://doi.org/10.1016/j.nicl.2021.102933CrossRefPubMed

59.

Bylsma LM (2021) Emotion context insensitivity in depression: toward an integrated and contextualized approach. Psychophysiology 58:e13715. https://doi.org/10.1111/psyp.13715CrossRefPubMed

60.

Garfinkel SN, Critchley HD (2016) Threat and the body: how the heart supports fear processing. Trends Cogn Sci 20:34–46. https://doi.org/10.1016/j.tics.2015.10.005CrossRefPubMed

61.

Garfinkel SN, Minati L, Gray MA, Seth AK, Dolan RJ, Critchley HD (2014) Fear from the heart: sensitivity to fear stimuli depends on individual heartbeats. J Neurosci 34:6573–6582. https://doi.org/10.1523/JNEUROSCI.3507-13.2014CrossRefPubMedPubMedCentral

62.

Schiweck C, Piette D, Berckmans D, Claes S, Vrieze E (2019) Heart rate and high frequency heart rate variability during stress as biomarker for clinical depression. A systematic review. Psychol Med 49(2):200–211. https://doi.org/10.1017/S0033291718001988CrossRefPubMed

63.

Ribeiro MJ, Castelo-Branco M (2019) Neural correlates of anticipatory cardiac deceleration and its association with the speed of perceptual decision-making, in young and older adults. Neuroimage 199:521–533. https://doi.org/10.1016/j.neuroimage.2019.06.004CrossRefPubMed

64.

Schneider TR, Hipp JF, Domnick C, Carl C, Büchel C, Engel AK (2018) Modulation of neuronal oscillatory activity in the beta- and gamma-band is associated with current individual anxiety levels. Neuroimage 178:423–434. https://doi.org/10.1016/j.neuroimage.2018.05.059CrossRefPubMed

Titel: Brain–heart interaction disruption in major depressive disorder: disturbed rhythm modulation of the cardiac cycle on brain transient theta bursts
verfasst von: Hongliang Zhou
Tingting Xiong
Zhongpeng Dai
Haowen Zou
Xvmiao Wang
Hao Tang
Yinghong Huang
Hao Sun
Wei You
Zhijian Yao
Qing Lu
Publikationsdatum: 15.06.2023
Verlag: Springer Berlin Heidelberg
Erschienen in: European Archives of Psychiatry and Clinical Neuroscience / Ausgabe 3/2024
Print ISSN: 0940-1334
Elektronische ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-023-01628-4

Update Psychiatrie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Die Highlights vom Kongress des American College of Cardiology 2024

Springer Medizin

Brain–heart interaction disruption in major depressive disorder: disturbed rhythm modulation of the cardiac cycle on brain transient theta bursts

Abstract

Neu im Fachgebiet Psychiatrie

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

ADHS-Medikation erhöht das kardiovaskuläre Risiko

Klinikreform soll zehntausende Menschenleben retten

Typ-2-Diabetes und Depression folgen oft aufeinander

Update Psychiatrie

Die Highlights vom Kongress des American College of Cardiology 2024

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2024

Multilayer depressive symptom networks in adults with bodily pain living in precarious housing or homelessness

Association of subclinical hypothyroidism with metabolic syndrome and its components among outpatients with first-episode drug-naïve major depressive disorder: a large-scale cross-sectional study

From pathogenesis of stress-related mental disorders to treatment: beyond the brain

Linking connectivity of deep brain stimulation of nucleus accumbens area with clinical depression improvements: a retrospective longitudinal case series

Decreased serum allopregnanolone and progesterone levels in male patients with bipolar disorder and their effects on cognitive functions

Risk of autoimmune diseases after post-traumatic stress disorder: a nationwide cohort study

Neu im Fachgebiet Psychiatrie

„Übersichtlicher Wegweiser“: Lauterbachs umstrittener Klinik-Atlas ist online

ADHS-Medikation erhöht das kardiovaskuläre Risiko

Klinikreform soll zehntausende Menschenleben retten

Typ-2-Diabetes und Depression folgen oft aufeinander

Update Psychiatrie