Characterization of Mayer wave oscillations in functional near-infrared spectroscopy using a physiologically informed model of the neural power spectra

Significance: Mayer waves are spontaneous oscillations in arterial blood pressure that can mask cortical hemodynamic responses associated with neural activity of interest. Aim: To characterize the properties of oscillations in the fNIRS signal generated by Mayer waves in a large sample of fNIRS recordings. Further, we aim to determine the impact of short-channel correction for the attenuation of these unwanted signal components. Approach: Mayer wave oscillation parameters were extracted from 310 fNIRS measurements using the Fitting Oscillations & One-Over-F (FOOOF) method to compute normative values. The effect of short-channel correction on Mayer wave oscillation power was quantified on 222 measurements. The practical benefit of the short-channel correction approach for reducing Mayer waves and improving response detection was also evaluated on a subgroup of 17 fNIRS measurements collected during a passive auditory speech detection experiment. Results: Mayer wave oscillations had a mean frequency of 0.108 Hz, bandwidth of 0.075 Hz, and power of 3.5 μM2/Hz. The distribution of oscillation signal power was positively skewed, with some measurements containing large Mayer waves. Short-channel correction significantly reduced the amplitude of these undesired signals; greater attenuation was observed for measurements containing larger Mayer wave oscillations. Conclusions: A robust method for quantifying Mayer wave oscillations in the fNIRS signal spectrum was presented and used to provide normative parameterization. Short-channel correction is recommended as an approach for attenuating Mayer waves, particularly in participants with large oscillations.

Blood pressure variability from intra-arterial recordings in humans

Systolic and diastolic blood pressures are reported as single point values by the non-invasive techniques used in clinical practice, while, in fact, they are highly varying signals. The objective of this study was to document the magnitude of variation of systolic and diastolic pressures over a few minutes by analysing intra-arterial pressure recordings made in 51 haemodynamically stable patients in an intensive care unit. Intra-arterial pressure data were acquired by a validated data acquisition system. Fast-Flush test was performed and the dynamic characteristics of the catheter transducer system namely natural frequency and damping co-efficient were calculated. Only those recordings with acceptable dynamic characteristics were included in the analysis. Power spectral calculation using the Discrete Fourier transform (DFT) of the pressure recording revealed two frequency peaks below the peak at heart rate. The lower and higher frequency peaks below the heart rate peak are referred to as Mayer and Traube waves in this study. Mayer wave peaks were observed in DFT spectra of 49 out of 51 patients. The Mayer wave frequency peaks ranged between 0.045 Hz to 0.065 Hz in 41 out of 51 patients. The frequency of Traube waves or the respiratory variations was more than 0.14 Hz. Three categories of systolic and diastolic pressure variabilities namely beat-to-beat variability, Respiratory variability (Traube wave amplitude) and Total magnitude of variation are reported for all 51 patients. The mean systolic and diastolic pressure variations (in a period of about 10 minutes) in the study sample were 21 ± 9 mm Hg and 14 ± 5 mm Hg respectively. Given the magnitude of systolic and diastolic pressure variations over a few minutes, the validity of reporting single point values for these pressures and using single point cut-offs for diagnosis and treatment of hypertension must be re-evaluated.

Causal Coupling Between Electrophysiological Signals, Cerebral Hemodynamics and Systemic Blood Supply Oscillations in Mayer Wave Frequency Range

The aim of the study was to assess causal coupling between neuronal activity, microvascular hemodynamics and blood supply oscillations in the Mayer wave frequency range. An electroencephalogram, cerebral blood oxygenation changes, an electrocardiogram and blood pressure were recorded during rest and during a movement task. Causal coupling between them was evaluated using directed transfer function, a measure based on the Granger causality principle. The multivariate autoregressive model was fitted to all the signals simultaneously, which made it possible to construct a complete scheme of interactions between the considered signals. The obtained pattern of interactions in the resting state estimated in the 0.05–0.15 Hz band revealed a predominant influence of blood pressure oscillations on all the other variables. Reciprocal connections between blood pressure and heart rate variability time series indicated the presence of feedback loops between these signals. During movement, the pattern of connections did not change dramatically. The number of connections decreased, but the couplings between blood pressure and heart rate variability signal were not significantly changed, and the strong influence of the decreased blood hemoglobin concentration on the oxygenated hemoglobin concentration persisted. For the first time our results provided a comprehensive scheme of interactions between electrical and hemodynamic brain signals, heart rate and blood pressure oscillations. Persistent reciprocal connections between blood pressure and heart rate variability time series suggest possible feedforward and feedback coupling of cardiovascular variables which may lead to the observed oscillations in Mayer wave range.

Increased cerebral blood volume pulsatility during head-down tilt with elevated carbon dioxide: the SPACECOT Study

Astronauts aboard the International Space Station (ISS) have exhibited hyperopic shifts, posterior eye globe flattening, dilated optic nerve sheaths, and even optic disk swelling from spaceflight. Elevated intracranial pressure (ICP) consequent to cephalad fluid shifts is commonly hypothesized as contributing to these ocular changes. Head-down tilt (HDT) is frequently utilized as an Earth-based analog to study similar fluid shifts. Sealed environments like the ISS also exhibit elevated CO2, a potent arteriolar vasodilator that could further affect cerebral blood volume (CBV) and cerebral blood flow, intracranial compliance, and ICP. A collaborative pilot study between the National Space Biomedical Research Institute and the German Aerospace Center tested the hypotheses that 1) HDT and elevated CO2 physiologically interact and 2) cerebrovascular pulsatility is related to HDT and/or elevated CO2. In a double-blind crossover study ( n = 6), we measured CBV pulsatility via near-infrared spectroscopy, alongside noninvasive ICP and intraocular pressure (IOP) during 28-h −12° HDT at both nominal (0.04%) and elevated (0.5%) ambient CO2. In our cohort, CBV pulsatility increased significantly over time at cardiac frequencies (0.031 ± 0.009 μM/h increase in total hemoglobin concentration pulsatility amplitude) and Mayer wave frequencies (0.019 ± 0.005 μM/h increase). The HDT-CO2 interaction on pulsatility was not robust but rather driven by one individual. Significant differences between atmospheres were not detected in ICP or IOP. Further work is needed to determine whether individual differences in pulsatility responses to CO2 relate to visual changes in space. NEW & NOTEWORTHY Cerebral blood volume (CBV) pulsatility—as measured by near-infrared spectroscopy—increases over time during −12° head-down tilt at both cardiac and Mayer wave frequencies. CBV pulsatility appeared to increase more under elevated (0.5%) CO2 at Mayer wave frequencies in some individuals. If similar dynamic pulsatility increases occur in astronauts, there is the potential to initiate vascular and possibly other remodeling processes that lead to symptoms associated with sustained increases in intracranial pressure.

Arousal dynamics drive vocal production in marmoset monkeys

Vocal production is the result of interacting cognitive and autonomic processes. Despite claims that changes in one interoceptive state (arousal) govern primate vocalizations, we know very little about how it influences their likelihood and timing. In this study we investigated the role of arousal during naturally occurring vocal production in marmoset monkeys. Throughout each session, naturally occurring contact calls are produced more quickly, and with greater probability, during higher levels of arousal, as measured by heart rate. On average, we observed a steady increase in heart rate 23 s before the production of a call. Following call production, there is a sharp and steep cardiac deceleration lasting ∼8 s. The dynamics of cardiac fluctuations around a vocalization cannot be completely predicted by the animal's respiration or movement. Moreover, the timing of vocal production was tightly correlated to the phase of a 0.1-Hz autonomic nervous system rhythm known as the Mayer wave. Finally, a compilation of the state space of arousal dynamics during vocalization illustrated that perturbations to the resting state space increase the likelihood of a call occurring. Together, these data suggest that arousal dynamics are critical for spontaneous primate vocal production, not only as a robust predictor of the likelihood of vocal onset but also as scaffolding on which behavior can unfold.

Functional connectivity in raphé-pontomedullary circuits supports active suppression of breathing during hypocapnic apnea

Hyperventilation is a common feature of disordered breathing. Apnea ensues if CO2drive is sufficiently reduced. We tested the hypothesis that medullary raphé, ventral respiratory column (VRC), and pontine neurons have functional connectivity and persistent or evoked activities appropriate for roles in the suppression of drive and rhythm during hyperventilation and apnea. Phrenic nerve activity, arterial blood pressure, end-tidal CO2, and other parameters were monitored in 10 decerebrate, vagotomized, neuromuscularly-blocked, and artificially ventilated cats. Multielectrode arrays recorded spiking activity of 649 neurons. Loss and return of rhythmic activity during passive hyperventilation to apnea were identified with the S-transform. Diverse fluctuating activity patterns were recorded in the raphé-pontomedullary respiratory network during the transition to hypocapnic apnea. The firing rates of 160 neurons increased during apnea; the rates of 241 others decreased or stopped. VRC inspiratory neurons were usually the last to cease firing or lose rhythmic activity during the transition to apnea. Mayer wave-related oscillations (0.04–0.1 Hz) in firing rate were also disrupted during apnea. Four-hundred neurons (62%) were elements of pairs with at least one hyperventilation-responsive neuron and a correlational signature of interaction identified by cross-correlation or gravitational clustering. Our results support a model with distinct groups of chemoresponsive raphé neurons contributing to hypocapnic apnea through parallel processes that incorporate disfacilitation and active inhibition of inspiratory motor drive by expiratory neurons. During apnea, carotid chemoreceptors can evoke rhythm reemergence and an inspiratory shift in the balance of reciprocal inhibition via suppression of ongoing tonic expiratory neuron activity.