Respiration aligns perception with neural excitability

Abstract

Recent studies from the field of interoception have highlighted the link between bodily and neural rhythms during action, perception, and cognition. The mechanisms underlying functional body-brain coupling, however, are poorly understood, as are the ways in which they modulate behavior. We acquired respiration and human magnetoencephalography data from a near-threshold spatial detection task to investigate the trivariate relationship between respiration, neural excitability, and performance. Respiration was found to significantly modulate perceptual sensitivity as well as posterior alpha power (8–13 Hz), a well-established proxy of cortical excitability. In turn, alpha suppression prior to detected versus undetected targets underscored the behavioral benefits of heightened excitability. Notably, respiration-locked excitability changes were maximized at a respiration phase lag of around –30° and thus temporally preceded performance changes. In line with interoceptive inference accounts, these results suggest that respiration actively aligns sampling of sensory information with transient cycles of heightened excitability to facilitate performance.

References 75

1. 1.

   Allen M, Levy A, Parr T, Friston KJ. In the Body’s Eye: The Computational Anatomy of Interoceptive Inference. bioRxiv. 2019a.

   Not in our library10.1101/603928

2. 2.

   Allen M, Poggiali D, Whitaker K, Marshall TR, Kievit RA. Raincloud plots: a multi-platform tool for robust data visualization. Wellcome Open Research. 2019b;4:63.

   Not in our library10.12688/wellcomeopenres.15191.1

3. 3.

   Arnal LH, Giraud AL. Cortical oscillations and sensory predictions. Trends in Cognitive Sciences. 2012;16:390-398.

   Not in our library10.1016/j.tics.2012.05.003

4. 4.

   Bareither I, Chaumon M, Bernasconi F, Villringer A, Busch NA. Invisible visual stimuli elicit increases in alpha-band power. Journal of Neurophysiology. 2014;112:1082-1090.

   Not in our library10.1152/jn.00550.2013

5. 5.

   Becker R, Reinacher M, Freyer F, Villringer A, Ritter P. How ongoing neuronal oscillations account for evoked fMRI variability. The Journal of Neuroscience. 2011;31:11016-11027.

   Not in our library10.1523/jneurosci.0210-11.2011

6. 6.
   Organization of prefrontal network activity by respiration-related oscillations · 2017

   No notice
7. 7.

   Bollimunta A, Chen Y, Schroeder CE, Ding M. Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques. The Journal of Neuroscience. 2008;28:9976-9988.

   Not in our library10.1523/jneurosci.2699-08.2008

8. 8.

   Busch NA, VanRullen R. Spontaneous EEG oscillations reveal periodic sampling of visual attention. PNAS. 2010;107:16048-16053.

   Not in our library10.1073/pnas.1004801107

9. 9.

   Canolty RT, Knight RT. The functional role of cross-frequency coupling. Trends in Cognitive Sciences. 2010;14:506-515.

   Not in our library10.1016/j.tics.2010.09.001

10. 10.

    Carmichael ST, Clugnet MC, Price JL. Central olfactory connections in the macaque monkey. The Journal of Comparative Neurology. 1994;346:403-434.

    Not in our library10.1002/cne.903460306

11. 11.

    Chapeton JI, Haque R, Wittig JH, Inati SK, Zaghloul KA. Large-Scale Communication in the Human Brain Is Rhythmically Modulated through Alpha Coherence. Current Biology. 2019;29:2801-2811.

    Not in our library10.1016/j.cub.2019.07.014

12. 12.

    Chaumon M, Busch NA. Prestimulus neural oscillations inhibit visual perception via modulation of response gain. Journal of Cognitive Neuroscience. 2014;26:2514-2529.

    Not in our library10.1162/jocn_a_00653

13. 13.

    Corcoran AW, Pezzulo G, Hohwy J. Commentary: Respiration-Entrained Brain Rhythms Are Global but Often Overlooked. Frontiers in Systems Neuroscience. 2018;12:25.

    Not in our library10.3389/fnsys.2018.00025

14. 14.

    da Silva FH, van Lierop TH, Schrijer CF, van Leeuwen WS. Organization of thalamic and cortical alpha rhythms: spectra and coherences. Electroencephalography and Clinical Neurophysiology. 1973;35:627-639.

    Not in our library10.1016/0013-4694(73)90216-2

15. 15.

    Dougherty K, Cox MA, Ninomiya T, Leopold DA, Maier A. Ongoing Alpha Activity in V1 Regulates Visually Driven Spiking Responses. Cerebral Cortex. 2017;27:1113-1124.

    Not in our library10.1093/cercor/bhv304

16. 16.

    Dulla CG, Dobelis P, Pearson T, Frenguelli BG, Staley KJ, Masino SA. Adenosine and ATP link PCO2 to cortical excitability via pH. Neuron. 2005;48:1011-1023.

    Not in our library10.1016/j.neuron.2005.11.009

17. 17.

    Ergenoglu T, Demiralp T, Bayraktaroglu Z, Ergen M, Beydagi H, Uresin Y. Alpha rhythm of the EEG modulates visual detection performance in humans. Brain Research. Cognitive Brain Research. 2004;20:376-383.

    Not in our library10.1016/j.cogbrainres.2004.03.009

18. 18.

    Fleming S, Thompson M, Stevens R, Heneghan C, Plüddemann A, Maconochie I, Tarassenko L, Mant D. Normal ranges of heart rate and respiratory rate in children from birth to 18 years of age: a systematic review of observational studies. Lancet. 2011;377:1011-1018.

    Not in our library10.1016/s0140-6736(10)62226-x

19. 19.

    Florez CM, McGinn RJ, Lukankin V, Marwa I, Sugumar S, Dian J, Hazrati LN, Carlen PL, Zhang L, Valiante TA. In vitro recordings of human neocortical oscillations. Cerebral Cortex. 2015;25:578-597.

    Not in our library10.1093/cercor/bht235

20. 20.

    Fontanini A, Bower JM. Slow-waves in the olfactory system: an olfactory perspective on cortical rhythms. Trends in Neurosciences. 2006;29:429-437.

    Not in our library10.1016/j.tins.2006.06.013

21. 21.

    Galvez-Pol A, McConnell R, Kilner JM. Active sampling in visual search is coupled to the cardiac cycle. Cognition. 2020;196:104149.

    Not in our library10.1016/j.cognition.2019.104149

22. 22.

    Goldman RI, Stern JM, Engel J, Cohen MS. Simultaneous EEG and fMRI of the alpha rhythm. Neuroreport. 2002;13:2487-2492.

    Not in our library10.1097/01.wnr.0000047685.08940.d0

23. 23.

    Haegens S, Barczak A, Musacchia G, Lipton ML, Mehta AD, Lakatos P, Schroeder CE. Laminar Profile and Physiology of the α Rhythm in Primary Visual, Auditory, and Somatosensory Regions of Neocortex. The Journal of Neuroscience. 2015;35:14341-14352.

    Not in our library10.1523/jneurosci.0600-15.2015

24. 24.
    Breathing as a Fundamental Rhythm of Brain Function · 2017

    No notice
25. 25.

    Heck D.H., Kozma R, Kay LM. The rhythm of memory: how breathing shapes memory function. Journal of Neurophysiology. 2019;122:563-571.

    Not in our library10.1152/jn.00200.2019

26. 26.

    Herrero JL, Khuvis S, Yeagle E, Cerf M, Mehta AD. Breathing above the brain stem: volitional control and attentional modulation in humans. Journal of Neurophysiology. 2018;119:145-159.

    Not in our library10.1152/jn.00551.2017

27. 27.

    Iemi L, Chaumon M, Crouzet SM, Busch NA. Spontaneous Neural Oscillations Bias Perception by Modulating Baseline Excitability. The Journal of Neuroscience. 2017;37:807-819.

    Not in our library10.1523/jneurosci.1432-16.2016

28. 28.

    Iemi L, Busch NA. Moment-to-Moment Fluctuations in Neuronal Excitability Bias Subjective Perception Rather than Strategic Decision-Making. ENeuro. 2018;5:ENEURO.0430-17.2018.

    Not in our library10.1523/eneuro.0430-17.2018

29. 29.
    Multiple mechanisms link prestimulus neural oscillations to sensory responses · 2019

    No notice
30. 30.

    Iemi L, Gwilliams L, Samaha J, Auksztulewicz R, Cycowicz YM, King JR, Nikulin VV, Thesen T, Doyle W, Devinsky O. Spontaneous Neural Oscillations Influence Behavior and Sensory Representations by Suppressing Neuronal Excitability. bioRxiv. 2021.

    Not in our library10.1101/2021.03.01.433450

31. 31.
    A statistical framework for neuroimaging data analysis based on mutual information estimated via a gaussian copula · 2016

    No notice
32. 32.

    Ito J, Roy S, Liu Y, Cao Y, Fletcher M, Lu L, Boughter JD, Grün S, Heck DH. Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration. Nature Communications. 2014;5:3572.

    Not in our library10.1038/ncomms4572

33. 33.

    Jensen O, Colgin LL. Cross-frequency coupling between neuronal oscillations. Trends in Cognitive Sciences. 2007;11:267-269.

    Not in our library10.1016/j.tics.2007.05.003

34. 34.

    Jensen O, Mazaheri A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Frontiers in Human Neuroscience. 2010;4:186.

    Not in our library10.3389/fnhum.2010.00186

35. 35.

    Kelly SP, O’Connell RG. Internal and external influences on the rate of sensory evidence accumulation in the human brain. The Journal of Neuroscience. 2013;33:19434-19441.

    Not in our library10.1523/jneurosci.3355-13.2013

36. 36.

    Kluger DS, Gross J. Depth and phase of respiration modulate cortico-muscular communication. NeuroImage. 2020;222:117272.

    Not in our library10.1016/j.neuroimage.2020.117272

37. 37.
    Respiration modulates oscillatory neural network activity at rest · 2021

    No notice
38. 38.

    Kurnikova A, Moore JD, Liao SM, Deschênes M, Kleinfeld D. Coordination of Orofacial Motor Actions into Exploratory Behavior by Rat. Current Biology. 2017;27:688-696.

    Not in our library10.1016/j.cub.2017.01.013

39. 39.

    Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. Journal of Neurophysiology. 2005;94:1904-1911.

    Not in our library10.1152/jn.00263.2005

40. 40.

    Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science. 2008;320:110-113.

    Not in our library10.1126/science.1154735

41. 41.

    Lundqvist M, Bastos AM, Miller EK. Preservation and Changes in Oscillatory Dynamics across the Cortical Hierarchy. Journal of Cognitive Neuroscience. 2020;32:2024-2035.

    Not in our library10.1162/jocn_a_01600

42. 42.

    Mather M, Thayer J. How heart rate variability affects emotion regulation brain networks. Current Opinion in Behavioral Sciences. 2018;19:98-104.

    Not in our library10.1016/j.cobeha.2017.12.017

43. 43.

    McKay LC, Evans KC, Frackowiak RSJ, Corfield DR. Neural correlates of voluntary breathing in humans. Journal of Applied Physiology. 2003;95:1170-1178.

    Not in our library10.1152/japplphysiol.00641.2002

44. 44.

    Michalareas G, Vezoli J, van Pelt S, Schoffelen J-M, Kennedy H, Fries P. Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas. Neuron. 2016;89:384-397.

    Not in our library10.1016/j.neuron.2015.12.018

45. 45.

    Moore JD, Deschênes M, Furuta T, Huber D, Smear MC, Demers M, Kleinfeld D. Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature. 2013;497:205-210.

    Not in our library10.1038/nature12076

46. 46.

    Morillon B, Hackett TA, Kajikawa Y, Schroeder CE. Predictive motor control of sensory dynamics in auditory active sensing. Current Opinion in Neurobiology. 2015;31:230-238.

    Not in our library10.1016/j.conb.2014.12.005

47. 47.

    Mumford D. On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biological Cybernetics. 1992;66:241-251.

    Not in our library10.1007/bf00198477

48. 48.
    FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data · 2011

    No notice
49. 49.

    Owens AP, Allen M, Ondobaka S, Friston KJ. Interoceptive inference: From computational neuroscience to clinic. Neuroscience and Biobehavioral Reviews. 2018;90:174-183.

    Not in our library10.1016/j.neubiorev.2018.04.017

50. 50.

    Perl O, Ravia A, Rubinson M, Eisen A, Soroka T, Mor N, Secundo L, Sobel N. Human non-olfactory cognition phase-locked with inhalation. Nature Human Behaviour. 2019;3:501-512.

    Not in our library10.1038/s41562-019-0556-z

51. 51.

    Pollatos O, Schandry R. Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. Psychophysiology. 2004;41:476-482.

    Not in our library10.1111/1469-8986.2004.00170.x

52. 52.

    Potes C, Brunner P, Gunduz A, Knight RT, Schalk G. Spatial and temporal relationships of electrocorticographic alpha and gamma activity during auditory processing. NeuroImage. 2014;97:188-195.

    Not in our library10.1016/j.neuroimage.2014.04.045

53. 53.

    R Development Core Team. 2014.

    Not in our library

54. 54.

    Rassler B, Raabe J. Co-ordination of breathing with rhythmic head and eye movements and with passive turnings of the body. European Journal of Applied Physiology. 2003;90:125-130.

    Not in our library10.1007/s00421-003-0876-5

55. 55.
    Stomach-brain synchrony reveals a novel, delayed-connectivity resting-state network in humans · 2018

    No notice
56. 56.

    Romei V, Gross J, Thut G. On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? The Journal of Neuroscience. 2010;30:8692-8697.

    Not in our library10.1523/jneurosci.0160-10.2010

57. 57.

    Samaha J, Iemi L, Postle BR. Prestimulus alpha-band power biases visual discrimination confidence, but not accuracy. Consciousness and Cognition. 2017;54:47-55.

    Not in our library10.1016/j.concog.2017.02.005

58. 58.

    Samaha J, Iemi L, Haegens S, Busch NA. Spontaneous Brain Oscillations and Perceptual Decision-Making. Trends in Cognitive Sciences. 2020a;24:639-653.

    Not in our library10.1016/j.tics.2020.05.004

59. 59.

    Samaha J, LaRocque JJ, Postle BR. Spontaneous Alpha-Band Amplitude Predicts Subjective Visibility but Not Discrimination Accuracy during High-Level Perception. bioRxiv. 2020b.

    Not in our library10.1101/2020.07.13.201178

60. 60.

    Schroeder CE, Wilson DA, Radman T, Scharfman H, Lakatos P. Dynamics of Active Sensing and perceptual selection. Current Opinion in Neurobiology. 2010;20:172-176.

    Not in our library10.1016/j.conb.2010.02.010

61. 61.

    Schütt HH, Harmeling S, Macke JH, Wichmann FA. Painfree and accurate Bayesian estimation of psychometric functions for (potentially) overdispersed data. Vision Research. 2016;122:105-123.

    Not in our library10.1016/j.visres.2016.02.002

62. 62.

    Spaak E, Bonnefond M, Maier A, Leopold DA, Jensen O. Layer-specific entrainment of γ-band neural activity by the α rhythm in monkey visual cortex. Current Biology. 2012;22:2313-2318.

    Not in our library10.1016/j.cub.2012.10.020

63. 63.

    Stolk A, Todorovic A, Schoffelen JM, Oostenveld R. Online and offline tools for head movement compensation in MEG. NeuroImage. 2013;68:39-48.

    Not in our library10.1016/j.neuroimage.2012.11.047

64. 64.

    Thut G, Nietzel A, Brandt SA, Pascual-Leone A. Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. The Journal of Neuroscience. 2006;26:9494-9502.

    Not in our library10.1523/jneurosci.0875-06.2006

65. 65.

    Thut G, Miniussi C, Gross J. The functional importance of rhythmic activity in the brain. Current Biology. 2012;22:R658-R663.

    Not in our library10.1016/j.cub.2012.06.061

66. 66.

    Tort ABL, Kramer MA, Thorn C, Gibson DJ, Kubota Y, Graybiel AM, Kopell NJ. Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. PNAS. 2008;105:20517-20522.

    Not in our library10.1073/pnas.0810524105

67. 67.

    Veniero D, Gross J, Morand S, Duecker F, Sack AT, Thut G. Top-down control of visual cortex by the frontal eye fields through oscillatory realignment. Nature Communications. 2021;12:1-13.

    Not in our library10.1038/s41467-021-21979-7

68. 68.

    Wachowiak M. All in a sniff: olfaction as a model for active sensing. Neuron. 2011;71:962-973.

    Not in our library10.1016/j.neuron.2011.08.030

69. 69.

    Watson AB, Pelli DG. QUEST: a Bayesian adaptive psychometric method. Perception & Psychophysics. 1983;33:113-120.

    Not in our library10.3758/bf03202828

70. 70.

    Welker WI. Analysis of Sniffing of the Albino Rat 1). Behaviour. 1964;22:223-244.

    Not in our library10.1163/156853964x00030

71. 71.

    Wyart V, Tallon-Baudry C. How ongoing fluctuations in human visual cortex predict perceptual awareness: baseline shift versus decision bias. The Journal of Neuroscience. 2009;29:8715-8725.

    Not in our library10.1523/jneurosci.0962-09.2009

72. 72.

    Yang CF, Feldman JL. Efferent projections of excitatory and inhibitory preBötzinger Complex neurons. Journal of Comparative Neurology. 2018;526:1389-1402.

    Not in our library10.1002/cne.24415

73. 73.

    Yanovsky Y, Ciatipis M, Draguhn A, Tort ABL, Branka k J. Slow Oscillations in the Mouse Hippocampus Entrained by Nasal Respiration. Journal of Neuroscience. 2014;34:5949-5964.

    Not in our library10.1523/jneurosci.5287-13.2014

74. 74.

    Zelano C, Jiang H, Zhou G, Arora N, Schuele S, Rosenow J, Gottfried JA. Nasal Respiration Entrains Human Limbic Oscillations and Modulates Cognitive Function. The Journal of Neuroscience. 2016;36:12448-12467.

    Not in our library10.1523/jneurosci.2586-16.2016

75. 75.

    Zhang Y, Wang X, Bressler SL, Chen Y, Ding M. Prestimulus Cortical Activity is Correlated with Speed of Visuomotor Processing. Journal of Cognitive Neuroscience. 2008;20:1915-1925.

    Not in our library10.1162/jocn.2008.20132

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.