Heartbeat-related EEG amplitude and phase modulations from wakefulness to deep sleep: Interactions with sleep spindles and slow oscillations

Psychophysiology

Volumn 52, Issue 11, 2015, Pages 1441-1450

  Lechinger, Julia ^a   Heib, Dominik Philip Johannes ^a   Gruber, Walter ^a   Schabus, Manuel ^a   Klimesch, Wolfgang ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

Author keywords

EEG oscillations; Heart rate; Heartbeat evoked potential; Sleep spindles; Slow oscillations

Indexed keywords

BRAIN; ELECTROENCEPHALOGRAPHY; FEMALE; HEART RATE; HUMAN; MALE; PHYSIOLOGY; POLYSOMNOGRAPHY; SLEEP; SLEEP STAGE; WAKEFULNESS;

BRAIN; ELECTROENCEPHALOGRAPHY; FEMALE; HEART RATE; HUMANS; MALE; POLYSOMNOGRAPHY; SLEEP; SLEEP STAGES; WAKEFULNESS;

EID: 84942982144     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/psyp.12508     Document Type: Article

References (60)

1. Achermann, P., & Borbely, A. A. (1997). Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience, 81, 213-222. doi: 10.1016/S0306-4522(97)00186-3
2. Anderer, P., Gruber, G., Parapatics, S., Woertz, M., Miazhynskaia, T., Klösch, G., ... Danker-Hopfe, H. (2005). An E-health solution for automatic sleep classification according to Rechtschaffen and Kales: Validation study of the Somnolyzer 24 × 7 utilizing the Siesta database. Neuropsychobiology, 51, 115-133. doi: 10.1159/000085205
3. Bastien, C. H., Crowley, K. E., & Colrain, I. M. (2002). Evoked potential components unique to non-REM sleep: Relationship to evoked K-complexes and vertex sharp waves. International Journal of Psychophysiology, 46, 257-274. doi: 10.1016/S0167-8760(02)00117-4
4. Becker, C., Gramann, K., Müller, H. J., & Elliott, M. A. (2009). Electrophysiological correlates of flicker-induced color hallucinations. Consciousness and Cognition, 18, 266-276. doi: 10.1016/j.concog.2008.05.001
5. Benjamini, Y., & Hochberg, Y. (2000). On the adaptive control of the false discovery rate in multiple testing with independent statistics. Journal of Educational and Behavioral Statistics, 25, 60-83. doi: 10.2307/1165312
6. Blanke, O. (2012). Multisensory brain mechanisms of bodily self-consciousness. Nature Reviews Neuroscience, 13, 556-571. doi: 10.1038/nrn3292
7. Burkitt, G. R, Silberstein, R. B., Cadusch, P. J., & Wood, A. W. (2000). Steady-state visual evoked potentials and travelling waves. Clinical Neurophysiology, 111, 246-258. doi: 10.1016/S1388-2457(99)00194-7
8. Busch, N. A., Debener, S., Kranczioch, C., Engel, A. K., & Herrmann, C. S. (2004). Size matters: Effects of stimulus size, duration and eccentricity on the visual gamma-band response. Clinical Neurophysiology, 115, 1810-1820. doi: 10.1016/j.clinph.2004.03.015
9. Censi, F., Calcagnini, G., & Cerutti, S. (2002). Coupling patterns between spontaneous rhythms and respiration in cardiovascular variability signals. Computer Methods and Programs in Biomedicine, 68, 37-47. doi: 10.1016/S0169-2607(01)00158-4
10. Critchley, H. D., & Harrison, N. A. (2013). Visceral influences on brain and behavior. Neuron, 77, 624-638. doi: 10.1016/j.neuron.2013.02.008
11. Csercsa, R., Dombovári, B., Fabó, D., Wittner, L., Eross, L. Entz, L., ... Kelemen, A. (2010). Laminar analysis of slow wave activity in humans. Brain, 133, 2814-2829. doi: 10.1093/brain/awq169
12. Cysarz, D., von Bonin, D., Lackner, H., Heusser, P., Moser, M., & Bettermann, H. (2004). Oscillations of heart rate and respiration synchronize during poetry recitation. American Journal of Physiology-Heart and Circulatory Physiology, 287, H579-H587. doi: 10.1152/ajpheart.01131.2003
13. Dirlich, G., Vogl, L., Plaschke, M., & Strian, F. (1997). Cardiac field effects on the EEG. Electroencephalography and Clinical Neurophysiology, 102, 307-315. doi: 10.1016/S0013-4694(96)96506-2
14. Engel, A. K., & Singer, W. (2001). Temporal binding and the neural correlates of sensory awareness. Trends in Cognitive Sciences, 5, 16-25. doi: 10.1016/S1364-6613(00)01568-0
15. Fowles, D. C., Fisher, A. E., & Tranel, D. T. (1982). The heart beats to reward: The effect of monetary incentive on heart rate. Psychophysiology, 19, 506-513. doi: 10.1111/j.1469-8986.1982.tb02577.x
16. Fukushima, H., Terasawa, Y., & Umeda, S. (2011). Association between interoception and empathy: Evidence from heartbeat-evoked brain potential. International Journal of Psychophysiology, 79, 259-265. doi: 10.1016/j.ijpsycho.2010.10.015
17. Gray, M. A., Taggart, P., Sutton, P. M., Groves, D., Holdright, D. R., Bradbury, D., ... Critchley, H. D. (2007). A cortical potential reflecting cardiac function. Proceedings of the National Academy of Sciences, 104, 6818-6823. doi: 10.1073/pnas.0609509104
18. Herrmann, C. S. (2001). Human EEG responses to 1-100 Hz flicker: Resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Experimental Brain Research, 137, 346-353. doi: 10.1007/s002210100682
19. Herrmann, C. S., Mecklinger, A., & Pfeifer, E. (1999). Gamma responses and ERPs in a visual classification task. Clinical Neurophysiology, 110, 636-642. doi: 10.1016/S1388-2457(99)00002-4
20. Jänig, W. (1996). Neurobiology of visceral afferent neurons: Neuroanatomy, functions, organ regulations and sensations. Biological Psychology, 42, 29-51. doi: 10.1016/0301-0511(95)05145-7
21. Jensen, O., & Colgin, L. L. (2007). Cross-frequency coupling between neuronal oscillations. Trends in Cognitive Sciences, 11, 267-269. doi: 10.1016/j.tics.2007.05.003
22. Jensen, O., Gelfand, J., Kounios, J., & Lisman, J. E. (2002). Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. Cerebral Cortex, 12, 877-882. doi: 10.1093/cercor/12.8.877
23. Jensen, O., & Mazaheri, A. (2010). Shaping functional architecture by oscillatory alpha activity: Gating by inhibition. Frontiers in Human Neuroscience, 4. doi: 10.3389/fnhum.2010.00186
24. 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, 3244-3251. doi: 10.1523/JNEUROSCI.5399-06.2007
25. Klimesch, W. (2012). Alpha-band oscillations, attention, and controlled access to stored information. Trends in Cognitive Sciences, 16, 606-617. doi: 10.1016/j.tics.2012.10.007
26. Klimesch, W. (2013). An algorithm for the EEG frequency architecture of consciousness and brain body coupling. Frontiers in Human Neuroscience, 7. doi: 10.3389/fnhum.2013.00766
27. Klimesch, W., Fellinger, R., & Freunberger, R. (2011). Alpha oscillations and early stages of visual encoding. Frontiers in Psychology, 2, 118. doi: 10.3389/fpsyg.2011.00118
28. Klimesch, W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53, 63-88. doi: 10.1016/j.brainresrev.2006.06.003
29. Lachaux, J. P., Rodriguez, E., Martinerie, J., & Varela, F. J. (1999). Measuring phase synchrony in brain signals. Human Brain Mapping, 8, 194-208. doi: 10.1002/(SICI)1097-0193(1999)8:4%3C194::AID-HBM4%3E3.0.CO;2-C
30. 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, 1904-1911. doi: 10.1152/jn.00263.2005
31. Lawrence, C. A, & Barry, R. J. (2010). Cognitive processing effects on auditory event-related potentials and the evoked cardiac response. International Journal of Psychophysiology, 78, 100-106. doi: 10.1016/j.ijpsycho.2010.06.027
32. Lyskov, E., Ponomarev, V., Sandström, M., Hansson Mild, K., & Medvedev, S. (1998). Steady-state visual evoked potentials to computer monitor flicker. International Journal of Psychophysiology, 28, 285-290. doi: 10.1016/S0167-8760(97)00074-3
33. Massimini, M., Boly, M., Casali, A., Rosanova, M., & Tononi, G. (2009). A perturbational approach for evaluating the brain's capacity for consciousness. Progress in Brain Research, 177, 201-214. doi: 10.1016/S0079-6123(09)17714-2
34. Massimini, M., Ferrarelli, F., Esser, S. K., Riedner, B. A., Huber, R., Murphy, M., ... Tononi, G. (2007). Triggering sleep slow waves by transcranial magnetic stimulation. Proceedings of the National Academy of Sciences of the United States of America, 104, 8496-8501. doi: 10.1073/pnas.0702495104
35. Massimini, M., Ferrarelli, F., Murphy, M. J., Huber, R., Riedner, B. A., Casarotto, S., & Tononi, G. (2010). Cortical reactivity and effective connectivity during REM sleep in humans. Cognitive Neuroscience, 1, 176-183. doi: 10.1080/17588921003731578
36. Massimini, M., Huber, R., Ferrarelli, F., Hill, S., & Tononi, G. (2004). The sleep slow oscillation as a traveling wave. Journal of Neuroscience, 24, 6862-6870. doi: 10.1523/JNEUROSCI.1318-04.2004
37. Mies, G. W., van der Veen, F. M., Tulen, J. H. M., Hengeveld, M. W., & van der Molen, M. W. (2011). Cardiac and electrophysiological responses to valid and invalid feedback in a time-estimation task. Journal of Psychophysiology, 25, 131-142. doi: 10.1027/0269-8803/a000049
38. Mölle, M., Eschenko, O., Gais, S., Sara, S. J., & Born, J. (2009). The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. European Journal of Neuroscience, 29, 1071-1081. doi: 10.1111/j.1460-9568.2009.06654.x
39. Mölle, M., Marshall, L., Gais, S., & Born, J. (2002). Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. Journal of Neuroscience, 22, 10941-10947.
40. Montoya, P., Schandry, R., & Müller, A. (1993). Heartbeat evoked potentials (HEP): Topography and influence of cardiac awareness and focus of attention. Electroencephalography and Clinical Neurophysiology, 88, 163-172. doi: 10.1016/0168-5597(93)90001-6
41. Novak, V., Novak, P., De Champlain, J., Le Blanc, A. R., Martin, R., & Nadeau, R. (1993). Influence of respiration on heart rate and blood pressure fluctuations. Journal of Applied Physiology, 74, 617-617.
42. Palva, J. M., Palva, S., & Kaila, K. (2005). Phase synchrony among neuronal oscillations in the human cortex. Journal of Neuroscience, 25, 3962-3972. doi: 10.1523/JNEUROSCI.4250-04.2005
43. Panitz, C., Wacker, J., Stemmler, G., & Mueller, E. M. (2013). Brain-heart coupling at the P300 latency is linked to anterior cingulate cortex and insula-A cardio-electroencephalographic covariance tracing study. Biological Psychology, 94, 185-191. doi: 10.1016/j.biopsycho.2013.05.017
44. Park, H.-D., Correia, S., Ducorps, A., & Tallon-Baudry, C. (2014). Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nature Neuroscience, 17, 612-618. doi: 10.1038/nn.3671
45. Park, H.-D., & Tallon-Baudry, C. (2014). The neural subjective frame: From bodily signals to perceptual consciousness. Philosophical Transactions of the Royal Society B: Biological Sciences, 369, 20130208. doi: 10.1098/rstb.2013.0208
46. Pollatos, O., & Schandry, R. (2004). Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. Psychophysiology, 41, 476-482. doi: 10.1111/1469-8986.2004.00170.x
47. Rechtschaffen, A., & Kales, A. A. (1968). A manual of standardized terminology, techniques and scoring system for sleep stages of human sujects. Bethesda, MD: U. S. Department of Health, Education, and Welfare Public Health Service-NIH/NIND.
48. Saul, J. P., Kaplan, D. T., & Kitney, R. I. (1988). Nonlinear interactions between respiration and heart rate: Classical physiology or entrained nonlinear oscillators. Computers in Cardiology, 1988, 299-302. doi: 10.1109/CIC.1988.72621
49. Schabus, M., Dang-Vu, T. T., Albouy, G., Balteau, E., Boly, M., Carrier, J., ... Maquet, P. (2007). Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proceedings of the National Academy of Sciences of the United States of America, 104, 13164-13169. doi: 10.1073/pnas.0703084104
50. Schabus, M., Gruber, G., Parapatics, S., Sauter, C., Klosch, G., Anderer, P., ... Zeitlhofer, J. (2004). Sleep spindles and their significance for declarative memory consolidation. SLEEP, 27, 1479-1485.
51. Schandry, R., & Weitkunat, R. (1990). Enhancement of heartbeat-related brain potentials through cardiac awareness training. International Journal of Neuroscience, 53, 243-253. doi: 10.3109/00207459008986611
52. Schimicek, P., Zeitlhofer, J., Anderer, P., & Saletu, B. (1994). Automatic sleep-spindle detection procedure-Aspects of reliability and validity. Clinical EEG and Neuroscience, 25, 26-29. doi: 10.1177/155005949402500108
53. Steriade, M., Contreras, D., Curro Dossi, R., & Nunez, A. (1993). The slow (<1 Hz) oscillation in reticular thalamic and thalamocortical neurons: Scenario of sleep rhythm generation in interacting thalamic and cortical networks. Journal of Neuroscience, 13, 3284-3299.
54. Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science, 262, 679-685. doi: 10.1126/science.8235588
55. Tallon-Baudry, C. (2009). The roles of gamma-band oscillatory synchrony in human visual cognition. Frontiers in Bioscience, 14, 321-332. doi: 10.2741/3246
56. Tallon-Baudry, C., & Bertrand, O. (1999). Oscillatory gamma activity in humans and its role in object representation. Trends in Cognitive Science, 3, 151-162. doi: 10.1016/S1364-6613(99)01299-1
57. Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 33, 81-88. doi: 10.1016/j.neubiorev.2008.08.004
58. Thut, G., Veniero, D., Romei, V., Miniussi, C., Schyns, P., & Gross, J (2011). Rhythmic TMS causes local entrainment of natural oscillatory signatures. Current Biology, 21, 1176-1185. doi: 10.1016/j.cub.2011.05.049
59. van der Veen, F. M., van der Molen, M. W., Crone, E. A., & Jennings, J. R. (2004). Phasic heart rate responses to performance feedback in a time production task: Effects of information versus valence. Biological Psychology, 65, 147-161. doi: 10.1016/j.biopsycho.2003.07.003
60. Zauner, A., Gruber, W., Himmelstoß, N. A., Lechinger, J., & Klimesch, W. (2014). Lexical access and evoked traveling alpha waves. NeuroImage, 91, 252-261. doi: 10.1016/j.neuroimage.2014.01.041