An update on the enigma of Mayer waves

(1)

HAL Id: hal-03031473

https://hal.archives-ouvertes.fr/hal-03031473

Submitted on 1 Dec 2020

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

An update on the enigma of Mayer waves

Claude Julien

To cite this version:

Claude Julien. An update on the enigma of Mayer waves. Cardiovascular Research, Oxford University

Press (OUP), 2020, 116 (14), pp.e210-e211. �10.1093/cvr/cvz327�. �hal-03031473�

(2)

.. ..

.. .

An update on the enigma of Mayer waves

Claude Julien*

EA 7426: Pathophysiology of Injury- Induced Immunosuppression (PI³), Institut des Sciences Pharmaceutiques et Biologiques, Faculte de Pharmacie de Lyon, Universite´ Claude Bernard - Lyon 1, Lyon, France

Keywords Mayer wave

•

Blood pressure

•

Sympathetic

•

Circulation

•

Haemodynamics

More than a decade on from having published my 2006 review paper on Mayer waves, I noted from a cursory Google Scholar search that it con- tinued to garner attention and interest.¹For this reason, I deemed it use- ful, and perhaps timely, to write a brief update suggesting some pointers for future research in this fascinating areaTable 1.

1. Definition of Mayer waves

For a start, it is interesting to examine the ‘career’ of the term Mayer waves. In 2006, I proposed, for the sake of convenience, that this term be reserved to blood pressure (BP) oscillations slower than respiration and correlating (i.e. coherent) with synchronous oscillations of a periph- eral sympathetic nervous activity (SNA). However, the term has often been used ever since to qualify almost every cardiovascular or autonomic oscillation slower than respiration. Even when it was reserved to BP, it could be read that Mayer waves can be observed ‘at frequencies as low as 0.03 Hz [. . .]’,²while, to the best of my knowledge, coherent oscillations of SNA and BP have never been recorded at such low frequencies in humans. In order to avoid confusion and misinterpretations, I reiterate my initial suggestion of defining Mayer waves as sympathetically mediated oscillations of BP slower than respiration. It is also important to recall that we are talking aboutoscillations, i.e. rhythmic fluctuations of BP with a fairly regular frequency. These oscillations must, therefore, appear as a peak in the spectra. The absence of such a peak, even in the presence of measurable spectral power in the band, points to the absence of Mayer waves. For example, after sinoaortic baroreceptor de- nervation (SAD) in rats, there is no longer a peak in the frequency band containing Mayer waves, but there is still spectral power (about one-half that measured in control rats). Power then appears as a continuation of the 1/f trend present at lower frequencies.¹There is also significant power in the renal SNA spectra of SAD rats and this power is coherent with that of BP. Furthermore, the residual variability of BP disappears after ganglionic blockade.¹It is thus quite likely that it originates from desynchronized discharges of sympathetic neurons.

Considering that the frequency of Mayer waves is species-specific, and that this frequency varies little among individuals of a given species, I suggest reconsidering the estimate of 0.4 Hz that was initially proposed for the central frequency of Mayer waves in mice.¹Although recordings of SNA have now been performed in conscious mice,³oscillatory compo-

nents of the signal have still not been described. It is, therefore, difficult to firmly assign anything else than a frequency band to Mayer waves in mice, on the basis of indirect, pharmacological evidence. However, it is interesting to note that long-term recordings of telemetric electrocar- diogram have been performed in conscious mice.⁴By carefully selecting 3-min stationary periods over 12 h during 2 months, the authors reported the presence in their RR interval spectra of a well-defined peak reproducibly centred near 0.7 Hz. This peak was not visible when analy- sing the entirety of the recordings. Assuming a baroreflex origin of RR interval oscillations in this band, it seems, therefore, reasonable to suggest that Mayer waves do not appear frequently in mice and that, when present, have a characteristic frequency of0.7 Hz.

2. What determines the frequency of Mayer waves?

I went through several papers dealing, at least in part, with the ‘pace- maker theory’, i.e. the hypothesis of an autonomous central oscillator

...

Table 1What is similar and what has changed about Mayer waves since 2006

What is similar What has changed

Mayer waves are sympathetically mediated oscillations of blood pressure slower than respiration.

Haemodynamic oscillations related to Mayer waves have been dem- onstrated in the human cerebral circulation.

Frequency of Mayer waves is fairly constant within a given animal species.

Frequency of Mayer waves in mice is probably closer to 0.7 than 0.4 Hz.

Frequency of Mayer waves depends on the ratio of noradrenaline to ATP released by sympathetic nerves.

Amplitude of Mayer waves is highly variable both between and within subjects.

Variability of Mayer wave amplitude can be predicted by using a simple model of baroreceptor discharge.

* Corresponding author. Tel:þ33 478 77 70 50, E-mail: julien@univ-lyon1.fr

Cardiovascular Research

doi:10.1093/cvr/cvz327 INVITED ONLIFE COMMENTARY

Downloaded from https://academic.oup.com/cardiovascres/article-abstract/doi/10.1093/cvr/cvz327/5684835 by guest on 25 June 2020

(3)

.. ..

generating slow oscillations of SNA, hence Mayer waves. I did not find

.

any convincing new study supporting this hypothesis. While the study by Morriset al.⁵basically confirmed previous studies, other studies were ex- tremely speculative. We are, therefore, still awaiting studies reporting slow rhythms in the spontaneous discharge of sympathetic premotor neurons recorded in conscious baroreceptor denervated animals.⁶

In 2006, I briefly mentioned the possible role of the cotransmitter of noradrenaline, ATP, in the determinism of the central frequency of Mayer waves. Very shortly after,⁷we had confirmation in conscious rats that the maximum coherence between BP and renal SNA was shifted from 0.4 to 0.2 Hz after P2 receptor blockade, thus confirming that ATP plays an important role in determining the frequency of Mayer waves.

Whether ATP is important in between-species differences in Mayer wave frequency remains to be investigated. Studies in P2X receptor knockout animals would help answer the question.

3. What determines the amplitude of Mayer waves?

I can only deplore the lack of significant advance in this area of research.

I will just have a quick look back to a result previously obtained in my lab- oratory,⁸which I did not value enough in 2006. In this study, baroreflex increases and decreases in renal SNA were obtained by infusing vasoac- tive drugs in conscious rats. It was observed that the amplitude of the low-frequency (LF) oscillation of renal SNA coherent with Mayer waves showed a biphasic response to sympathetic activation, namely, amplifica- tion during moderate activation and an almost complete reversal at the strongest activation levels. Very similar responses were observed for the pulse synchronous oscillation of SNA. A simple model of baroreceptor discharge incorporating a threshold nicely accounted for the behaviour of the pulse synchronous rhythm of renal SNA (open-loop operation), but was disregarded for explaining LF oscillations (closed-loop operation). I now think that it should be reconsidered because it works very well within the frame of the baroreflex theory, insofar as amplitude of LF oscillations partly depends on the sensitivity of the sympathetic vascular component of the baroreflex. The model would provide a simple expla- nation for the attenuation of Mayer waves during, e.g. strenuous exercise in healthy subjects, and in patients with congestive heart failure, both sit- uations being characterized by strong sympathetic activation. Moreover, this theory would also be valid in case of moderate sympathetic activa-

tion combined with baroreflex resetting and sensitization, e.g. during mental stress in rats,⁹a situation during which Mayer waves and accom- panying renal SNA oscillations are amplified.¹

4. Mayer waves in the cerebral circulation

To conclude, I must mention the recent studies accumulating about LF oscillations of cerebral haemodynamics, examined with the aid of functional imaging techniques. When this point is examined, it appears that these cerebral haemodynamic oscillations correlate with Mayer waves.

Mayer waves are then sometimes viewed as a biological source of

‘noise’,¹⁰or are expected to serve a physiological, yet unknown, function.¹¹Obviously, further studies are required to examine the important question of the function of Mayer waves in the cerebral circulation.

Conflict of interest:none declared.

References

1. Julien C. The enigma of Mayer waves: facts and models.Cardiovasc Res 2006;70:

12–21.

2. Draghici AE, Taylor JA. The physiological basis and measurement of heart rate variability in humans.J Physiol Anthropol2016;35:22.

3. Hamza SM, Hall JE. Direct recording of renal sympathetic nerve activity in unre- strained, conscious mice.Hypertension2012;60:856–864.

4. Thireau J, Zhang BL, Poisson D, Babuty D. Heart rate variability in mice: a theoretical and practical guide.Exp Physiol2008;93:83–94.

5. Morris KF, Nuding SC, Segers LS, Baekey DM, Shannon R, Lindsey BG, Dick TE.

Respiratory and Mayer wave-related discharge patterns of raphe´ and pontine neurons change with vagotomy.J Appl Physiol (1985)2010;109:189–202.

6. Barman SM, Yates BJ. Deciphering the neural control of sympathetic nerve activity:

status report and directions for future research.Front Neurosci2017;11:730.

7. Emonnot L, Bakhos C, Chapuis B, Ore´a V, Barre`s C, Julien C. Role of purinergic cotransmission in the sympathetic control of arterial pressure variability in conscious rats.Am J Physiol Regul Integr Comp Physiol2006;291:R736–R741.

8. Bertram D, Ore´a V, Chapuis B, Barre`s C, Julien C. Differential responses of frequency components of renal sympathetic nerve activity to arterial pressure changes in conscious rats.Am J Physiol Regul Integr Comp Physiol2005;289:R1074–R1082.

9. Kanbar R, Ore´a V, Barre`s C, Julien C. Baroreflex control of renal sympathetic nerve activity during air-jet stress in rats.Am J Physiol Regul Integr Comp Physiol2007;292:

R362–R367.

10. Yu¨cel MA, Selb J, Aasted CM, Lin PY, Borsook D, Becerra L, Boas DA. Mayer waves reduce the accuracy of estimated hemodynamic response functions in functional near-infrared spectroscopy.Biomed Opt Express2016;7:3078–3088.

11. Whittaker JR, Driver ID, Venzi M, Bright MG, Murphy K. Cerebral autoregulation evi- denced by synchronized low frequency oscillations in blood pressure and resting- state fMRI.Front Neurosci2019;13:433.

Author

Biography:Claude Julien received his PharmD degree in 1983 and his PhD degree in 1988, at Claude Bernard University of Lyon. He is presently Director of Research at the National Centre of Scientific Research (CNRS) in Lyon. His main scientific interests are in the field of the autonomic control of the circulation under normal and pathological conditions (arterial hypertension, cardiac arrhythmias, and sepsis). He is a founding member of the Working Group on Blood pressure and Heart Rate Variability of the European Society of Hypertension, which later enlarged to become the Working Group on Blood Pressure Monitoring and Cardiovascular Variability.

e2 C. Julien

Downloaded from https://academic.oup.com/cardiovascres/article-abstract/doi/10.1093/cvr/cvz327/5684835 by guest on 25 June 2020