Does heart rate variability reflect brain plasticity as a likely mechanism of adaptation to space mission?
V. B. Rusanov
E. V. Fomina - State Scientific Center of the Russian Federation Institute of Biomedical Problems of Russian Academy of Sciences, Moscow, Russia
In space medicine, the definition of “health” is considered as the ability of a crew member to carry out a high-quality space mission program and at the same time retain enough functional reserves for readaptation to earth conditions after it is completed (Baevsky et al., 2013).
Professional space crews are formed from specially selected, practically healthy people trained to work in changed conditions and under constant stress (Kovacs and Shadden, 2017). Monitoring of their functional state is based on the assessment of changes within the physiological norm, where the main ones are shifts (reorganizations) occurring in the mechanisms of regulation and developing at the information-temporal or information-energy levels of the body (Baevsky et al., 2011). In this sense, the individual approach of space medicine to health assessment can be seen as a prerequisite for modern personalized medicine (Dietrich et al., 2018; Pavez Loriè et al., 2021).
On the one hand, the structural elements of the human body are a system of independent components, on the other hand, they are characterized by complex interactions (Burggren and Monticino, 2005; Grenfell et al., 2006), therefore, the creation of a unified concept of health in space medicine is an integrative task that can be solved from the standpoint of systems biology.
The totality of space flight factors requires the human body to exert constant tension on its regulatory systems to maintain homeostasis (Baevsky et al., 2014). The complex impact of stress factors leads to the fact that ever-higher levels of control over the physiological functions of the body are involved in the adaptation process (Baevsky et al., 2007; Baevsky et al., 2009). This ensures the necessary coordination of various systems and processes within the framework of a single goal—balancing the body with the environment (Baevsky and Chernikova, 2016).
One of the characteristics of a system that ensures the quality of its functioning is plasticity, which allows it to quickly cope with the challenges of a changing environment (Goldberger, 1991; Beckers et al., 2006; McCraty et al., 2009; Smith et al., 2017). First of all, this is due to the ability of neurons, neural structures, and neural networks of the brain to dynamically change structural and functional characteristics and modify response patterns in response to changes in external conditions and afferent stimuli (Slenzka, 2003; Pearson-Fuhrhop and Crame, 2006).
In this regard, neuroimaging is an important tool for studying the plasticity of the brain in space flight, as well as the dynamic structural and functional networks that connect the body and brain in the process of adaptive changes.
Studies of structural changes in the brain after spaceflight appear compression of the gyri, narrowing of the calcarine and central sulcus, supravermian cistern, expansion of the cerebral ventricles with extensive redistribution of cerebrospinal fluid, and, in general, an upward displacement of the brain inside the skull. These changes were directly related to the duration of the mission and persisted for some time after the end of the mission (Roberts et al., 2017; Van Ombergen et al., 2018; Van Ombergen et al., 2019; Kramer et al., 2020).
In addition, microstructural changes occurring during a space mission in sensorimotor pathways, including tracts connecting the cerebellum, as well as within the corpus callosum, inferior fronto-occipital, and arcuate fascicles, may reflect various sources of space flight effects on the brain, including fluid displacement effects, structural brain changes and neuroplasticity (Doroshin et al., 2022).
In a study by Barisano et al. (2019) an increase in the lateral ventricles and a decrease in the subarachnoid space in the vertex region were found, which correlated with an increase in the volume of the perivascular space of the basal ganglia and the perivascular space of the white matter after space flight.
It seems to us that the plasticity of nervous structures underlies successful adaptive reactions that maintain homeostasis at an adequate level. In addition, it provides a transition between the functional states associated with autonomous control. Neuroplasticity induces adaptive changes or predisposes functional systems to adaptive plasticity.
Weightlessness, as a condition of existence atypical for an organism, models the specific relationship between the brain and the heart. This process is based on structural and functional networks dynamically changing in time and space, which provide multilevel interactions in the whole organism (Ivanov et al., 2016). The dynamic network approach to defining states has revealed new aspects of the connections between the heart and brain (Valenza et al., 2016). CAN include structures that modulate autonomic balance brain stem nuclei that directly regulate the functioning of the heart, solitary tract, hypothalamus, and amygdala, as well as areas of the prefrontal cortex (Benarroch, 1993; Beissner et al., 2013; Dampney, 2015; Shoemaker and Goswami, 2015). Piper et al. (2014) to study the dynamics of the central autonomic network (CAN), which controls the cardiovascular and cardiorespiratory systems, used time-varying coherence analysis to quantify the role of neural networks in the sympathetic control of the heart.
According to the “neurovisceral integration” model (Thayer and Lane, 2000; Thayer and Lane, 2009), CAN neural structures interact with each other as a “supersystem” that provides adaptive regulation. An integrative characteristic that reflects the level of functioning of this system is heart rate variability (HRV) since it reflects the degree of functional integration between areas of the prefrontal cortex, the brain stem, and the peripheral nervous system. The hypothesis is that HRV is not only an indicator of cardiac function but also an indicator of adaptive regulation and brain plasticity (Thayer et al., 2012). This is consistent with the concept of functional state analysis used to evaluate adaptation processes in space flight (Baevsky et al., 2011; Baevsky and Chernikova, 2016).
Neuroimaging studies have demonstrated links between HRV and specific brain regions (Thayer et al., 2012). Evidence suggests that the medial prefrontal cortex and adjacent anterior cingulate cortex are associated with HRV modulation (Sakaki et al., 2016). The dynamics of these associations are related to sex and age (Koenig and Thayer, 2016; Kumral et al., 2019).
External conditions model the dynamic relationship between the brain and the heart. In a situation of high stress, the degree of synchronization between the prefrontal cortex and the heart can change (Chand et al., 2020). This flexibility determines the transition between functional states mediated by the autonomic nervous system (Baevsky and Chernikova, 2017).
HRV may be one of the complex markers of stress, as it is associated not only with dynamic modulation of vagal control of heart rate (Author Anonymous, 1996) but also through putative connections with neural structures involved in threat and safety assessment (Sakaki et al., 2016), can characterize the level of functional state, as well as individual signs associated with physical and mental health (Holzman and Bridgett, 2017). The current theoretical foundations of HRV suggest that it reflects the ability to self-regulate (the ability to regulate behavioral, cognitive, and emotional processes) and, therefore, can be used as a biomarker of the circulatory system and complex mental and behavioral processes (Porges and Furman, 2011; Oken et al., 2015; Crestani 2016; Walker et al., 2017).
HRV gives an idea of the adaptation processes to the conditions of the space environment due to the integration of the brain and vegetative processes and the activation of higher vegetative centers, which ultimately determines the health level of a space mission participant (Baevsky et al., 2014).
To maintain cardiovascular homeostasis at an optimal level, active restructuring of regulatory mechanisms is necessary. At different stages of adaptation of the body to microgravity conditions, the degree of tension of regulatory systems and their functional reserves change, and the adaptation process itself is associated with a gradual increase in the influence of higher levels of regulation (Baevsky et al., 1998, 2013). At the same time, the reaction of regulatory mechanisms depends on individual characteristics that persist during repeated flights after several years (Baevsky et al., 2014).
Links between brain functional networks and HRV have been analyzed in studies by Otsuka et al. In one of them, the authors report that space missions lasting 6 months improve HRV (Otsuka et al., 2019). Another study documented an increase in the circadian periodicity of HRV, an improvement in sleep quality, and an increase in parasympathetic modulating influences at night (Otsuka et al., 2021). According to the authors, these data indicate an unconscious activation of the functional network of the brain during long-term space travel and contribute to slowing down the aging of regulatory mechanisms.
Changes in brain function reflected in HRV may explain the fact that the process of neural adaptation improves with the increase in the number of missions since neuroplasticity refers to the ability of the nervous system to change its activity in response to internal or external stimuli by reorganizing its structure, functions or connections (Demertzi et al., 2016; Pechenkova et al., 2019).
Perhaps the reorganization of the brain in repeated space missions is associated with countermeasures implemented on board the International Space Station (ISS). In the previously mentioned study and Barisano et al. (2019) differences in the reorganization of the brain of NASA astronauts, the European Space Agency, and Roscosmos cosmonauts were revealed. The authors have suggested that this is due to differences in the use of countermeasures and high-resistance exercise regimens, which may affect the redistribution of cerebral fluid, since age, mission duration, and environmental conditions on the ISS were identical.
Physical exercise has a positive effect on the functional connectivity of the brain and can act as neuroenhancers. In a study by Schneider et al. (2013), in a 520-day isolation experiment simulating a flight to Mars, it was shown that post-exercise cortical activity was most pronounced after endurance-oriented protocols using an active treadmill. In another analog space mission with 120-days of isolation, simulating a flight to the Moon and a stay in lunar orbit, it was demonstrated that individual aerobic running training induces responses that maintain brain plasticity (Abeln et al., 2022).
In our opinion, the study of the structural and functional effects that occur in the central nervous system in weightlessness will open up possibilities for understanding the body functions associated with the adaptation and health of space travelers. The theoretical assumption is that due to the interaction of neural networks consisting of nerve centers dynamically located at all levels of the brain and controlling HRV, it is this integral characteristic that reflects brain plasticity as a possible mechanism for adaptation to microgravity conditions. Undoubtedly, this thesis requires experimental confirmation and, nowadays has serious limitations associated with the insufficiency of repeated long-term space missions. In addition, the complexity of the mechanisms of neuronal cardiovascular integration requires their clearer differentiation, which is the subject of further research. However, understanding the impact of weightlessness on the processes of reorganization of the human brain and identifying possible markers of this process is important for developing an adequate strategy of countermeasures to maintain the health and performance of space crews, which will ultimately determine the success and safety of future long-term space missions to distant planets.
Author contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Funding
The work was carried out within the framework of the basic theme of RAS 63.1 and 64.1 for 2013–2023.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Keywords: heart rate variability, brain plasticity, adaptation, space mission, system biology
Citation: Rusanov VB, Fomina EV and Orlov OI (2022) Does heart rate variability reflect brain plasticity as a likely mechanism of adaptation to space mission?. Front. Space Technol. 3:998610. doi: 10.3389/frspt.2022.998610
Received: 20 July 2022; Accepted: 05 September 2022;
Published: 16 September 2022.
Edited by:
Mark Sephton, Imperial College London, United KingdomReviewed by:
Gabriel G. De La Torre, University of Cádiz, SpainCopyright © 2022 Rusanov, Fomina and Orlov. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: V. B. Rusanov, vasilyrusanov@gmail.com