Authors: Giovanna Grenno (1), Andrea Piarulli (1), Angelo Gemignani (1,2)
1) Department of Surgical, Medical, Molecular Pathology and Critical Area, University of Pisa
2) Department of Neuroscience, Pisa University Hospital
1. Breath and Consciousness: from age-old practices to neuroscientific discoveries
"Breathing is much more than taking air into the body. It is the most intimate connection with what surrounds us"
(Nestor, 2020)
From a physiological standpoint, unlike other vegetative functions solely under the control of the autonomic nervous system, breathing has the peculiarity of being modulated voluntarily and consciously (Betka et al., 2022). Conscious awareness and regulation of breathing constitute fundamental aspects of Indo-Tibetan Yoga and, in general, meditative practices; both approaches assert a bidirectional relationship between the mind and breath, suggesting that higher levels of consciousness can be achieved through breath modulation (Balaji et al., 2012; Brown & Gerbarg, 2009). Specifically, the slower the breath, the greater the potential to alter the level of consciousness: literature studies propose that meditative techniques based on slow breathing may be an effective tool to attain states of consciousness defined as "non-ordinary" (Zaccaro et al., 2022).
Breath thus becomes an integral part of mind-body practices; in Yoga, for instance, one of the fundamental techniques is represented by slow breathing known as Pranayama (from the Sanskrit "prana", meaning life breath/vital energy, and "ayama", meaning expansion/regulation/control). Pranayama involves voluntary modifications of breath, usually performed in a seated position and typically characterized by three phases: Puraka (inhalation), Kumbhaka (breath retention), and Rechaka (exhalation) (Jayawardena et al., 2020).
While various techniques of pranayama exist, most of them share a significant slowing of the respiratory rate (down to 2-3 breaths per minute), and they often emphasize nasal breathing. Yogic breathing exercises can be considered a form of meditation in themselves, as well as a preparation for deep meditation (Campanelli et al., 2020). The effects of such practices are believed to enhance physical well-being and self-awareness, improve lung and cognitive capacities, and contribute to the reduction of blood pressure and anxiety levels (Brown & Gerbarg, 2009; Rocha et al., 2012; Sharma et al., 2014; Novaes et al., 2020).
Studies on the psychophysiological effects of various Pranayama techniques have yielded results that seem to confirm what ancient traditions have asserted, emphasizing the close relationships between breathing and the central nervous system (Sengupta, 2012).
However, for breathing to lead to an "altered state of consciousness," it is not enough for it to be slow. It is crucial that it occurs through the nasal passages. Ancient yogic texts already emphasized the importance of the nostrils for prana control, but it is only through the third-person approach typical of neuroscience that we have been able to begin understanding the neurophysiological and neurophenomenological mechanisms underlying the interrelation between nasal breathing and consciousness.
Today, we know that nasal breathing not only allows the entry of air through the nose but also enables the synchronization of neural activity in cortical and subcortical structures (Tort et al., 2018; Biskamp et al., 2017; Zelano et al., 2016; Ito et al., 2014). Olfactory sensory neurons, located in the nasal vault epithelium, exhibit sensitivity to both chemical stimuli (the molecules underlying odors) and mechanical stimuli resulting from the impact of inhaled air flow on the nasal vault mucosa (Grosmaitre et al., 2007).
Fontanini & Bower (2006) hypothesized that the activation of mechanoreceptors in the nasal vault induced by inhaled air could generate a wave of neural synchronization starting from the olfactory bulb, involving the entire cortical mantle, with effects on behavior, emotional regulation, and states of consciousness.
Delving more deeply into the mechanisms linking breath to "altered states of consciousness," it is crucial to reference the seminal work of Nobel laureate Sir Edgar Douglas Adrian. Adrian's study (1942) marks the first observation in animal models of modulatory effects on the rhythmic activity of the piriform cortex through mechanical stimulation of the olfactory epithelium by air, highlighting for the first time the mechanoreceptive component of the nasal vault.
Subsequently, Arduini and Moruzzi, by blowing puffs of air into the cat's nostrils, recorded corresponding electrical activities in the olfactory bulb (Arduini & Moruzzi, 1953), and these results were replicated by Hobson (1967) in frogs, highlighting how the airflow through the nostrils had a synchronizing effect on brain electrical activity dependent on the stimulation frequency.
An extremely intriguing aspect arises from the observation that the global neural synchronization induced by nasal stimulation is almost completely abolished following: a) tracheotomy (Fontanini et al., 2003; Ito et al., 2014; Yanovsky et al., 2014; Lockmann et al., 2016; Zhong et al., 2017); b) surgical lesions of the olfactory epithelium (Moberly et al., 2018); and; d) pharmacological inhibition and surgical removal of the olfactory bulb (Liu et al., 2017; Ito et al., 2014; Biskamp et al., 2017). These data strongly underscore the role of air passing through the nostrils in synchronizing brain rhythms, configuring a kind of crucial electrophysiological carrier to modulate large-scale information integration phenomena at both cortical and subcortical levels.
Adrian's discovery ultimately paved the way for studies, both in animal models and humans, aimed at determining the neurophysiological and psychobiological effects of the coupling between brain activity and nasal breathing (Fontanini & Bower, 2003; Biskamp et al., 2017; Ito et al., 2014, Yanovsky et al., 2014; Zelano et al., 2016; Piarulli et al., 2018).
In humans, an innovative contribution on the subject has been provided by Zelano and colleagues, who, using intracranial electroencephalography (iEEG), observed synchronized electro-physiological oscillations with nasal breathing in epileptic patients in brain structures such as the cerebellum, amygdala, and hippocampus. As evidence of the crucial role of nasal breathing in neural activity synchronization, the authors noted that this synchronization disappeared when subjects breathed through their mouths (Zelano et al., 2016).
In summary, during nasal breathing, the airflow activates olfactory mechanoreceptors, inducing rhythmic neural activity in the olfactory bulb (Fontanini & Bower, 2006). Subsequently, the activity of the olfactory bulb influences oscillations in brain areas not directly associated with odor processing, making the olfactory system, similar to the thalamus, a structure capable of generating patterns of discharge complexity from billions of neural cells.
Although the function of respiration-dependent brain oscillations has not been fully elucidated, the underlying hypothesis is that the generation of such oscillatory rhythms may synchronize the activity of cell groups distributed in different areas of the brain, potentially leading to the reorganization of spatiotemporal dynamics in the central nervous system underlying the state of consciousness (González et al., 2022; Zaccaro et al., 2022; Piarulli et al., 2018).
Just as described in the work of Fontanini & Bower (2006), the influence of the olfactory system, especially the respiratory aspect, on cortical oscillatory dynamics can offer fascinating insights into how various meditative techniques based on nasal breathing may modulate levels of consciousness.
2. Breath and Meditation: Studies conducted at the University of Pisa
"The influence of the olfactory system in general and of breathing on brain oscillatory states provides a potentially intriguing new perspective on meditation"
(Fontanini & Bower, 2006)
Taking into consideration the modulatory effect of breathing on brain activity and its connections with meditative states, the research group at the University of Pisa, led by Prof. Angelo Gemignani, has been conducting a line of research for years aimed at investigating the role of nasal breathing on brain dynamics and consciousness (Piarulli et al., 2018; Zaccaro et al., 2022).
Specifically, in the 2018 study by Piarulli and colleagues, the authors explored the possibility of studying the psychobiological effects of mechanical stimulation of the olfactory epithelium through odorless air on cortical electrical activity in humans.
The experiment was based on the use of a cannula, positioned at the nasal vault, connected to an engineering system for delivering odorless air. The system aimed to artificially replicate respiratory dynamics. Healthy subjects recruited for the experiment, with no prior experience in meditative practices throughout their lives (which could have constituted a methodological and experiential bias), underwent stimulation with odorless air in the nasal vault, following the timing of pranayama breathing (8 seconds of airflow and 12 seconds of pause). This passive stimulation method in individuals completely naive to any meditative technique or experience allowed the elimination of typical cognitive biases associated with meditation, such as attention levels, awareness, etc. The electrical cortical activity of all experimental subjects was recorded using high-density electroencephalography. Subsequently, their level of consciousness was assessed using the Phenomenology of Consciousness Inventory (Pekala, 1982). As a control condition, the same subjects underwent sham stimulation, during which no air was delivered into the nasal vault. In all experimental conditions, subjects breathed through their mouths.
The main results from the study highlighted:
a) An increase in the power of slow rhythms (delta and theta), typical of NREM sleep, across the entire cortical mantle, with a certain topological preference for structures belonging to the Default Mode Network (DMN).
b) Reversal of the flow of theta activity, similar to what occurs during NREM sleep, i.e., from anterior to posterior regions (Kaminski et al., 1995).
c) From a phenomenological perspective, all subjects reported that stimulation of the nasal vault, with dynamics similar to Pranayama breathing, induced perceptual modifications attributable to a "non-ordinary state of consciousness." This state was characterized by a directed attention towards oneself, a different perception of the body and the passage of time, a reduction in volitional control, and a decrease in rational thinking (Piarulli et al., 2018).
In general, this study has highlighted that the increase in slow activity in the medio-central prefrontal cortices and areas of the Default Mode Network (DMN), associated with a sleep-like reversal of information flow, could characterize a state of consciousness where the internal world takes precedence over the external one, thereby altering the sense of reality and increasing introspection and self-awareness (Brewer et al., 2011; Panda et al., 2016; Lou et al., 2017).
Subsequently, the same authors addressed the effects of olfactory epithelium stimulation in a more purely meditative context, namely by studying expert Pranayama meditators. Using the same approach to record psychobiological parameters as employed in Piarulli et al., 2018, the authors compared the effects of Pranayama breathing performed through the nose (mouth closed) with that done through the mouth (nose blocked). This experimental model allowed for a more ecologically valid assessment of the psychobiological modulation of neural activity and induced behavior of nasal breathing compared to oral breathing, while maintaining equal vagal activation related, for example, to chest expansion (Zaccaro et al., 2022). The results of this study align with those reported in "naive" subjects by Piarulli et al., 2018. In summary, compared to oral breathing, nasal breathing induced:
a) an increase in the power of low frequencies (delta and theta) in the medial prefrontal areas;
b) a widespread increase in connectivity both at low and high frequencies;
c) a non-ordinary state of consciousness characterized by a positive mood, an altered experience of consciousness as well as awareness, and ultimately a significant reduction in perceived stress.
These results, in addition to aligning with the neurophysiological hypotheses derived from animal models, suggest that, similar to the thalamus, the olfactory bulb in humans plays a role as a modulator of cortical integrations and therefore the non-ordinary state of consciousness experienced by individuals, regardless of their experiences with meditative practices (Piarulli et al., 2018; Zaccaro et al., 2022).
An additional contribution comes from studies conducted by Professor Bruno Neri at the Monastic University of Sera Jey (India), where the effects of different meditative practices on cortical electrical activity were compared in experienced monks. In this case as well, the findings indicate that breath-focused meditation induces an increase in slow rhythms, especially in the theta band (Neri et al., submitted).
All the studies mentioned so far scientifically link breath and consciousness, an integrated dyad that has always characterized the approach of Eastern cultures to the concept of the mind.
3. How Voluntary Control of Breathing Can Improve Our Health
"The nose is a silent warrior: the guardian of our bodies, the pharmacist of our minds, and the weather vane of our emotions."
(Nestor, 2020)
In Western culture, breathing practices have taken shape and gained ground entirely independently of religious or spiritual influences, predominantly employed for therapeutic purposes (Zaccaro et al., 2018). For this reason, they have garnered significant attention, especially since scientific studies have described biological substrate modifications correlating with an enhancement of the sense of well-being (Jayawardena et al., 2020; Kuppusami et al., 2017; Jerath et al., 2006).
In addition to neurophysiological models related to the stimulation of the nasal vault, various experimental models have been proposed, employing top-down or bottom-up approaches to describe the psychophysiological mechanisms underlying the positive effects induced by such techniques.
Certainly, among the most observed effects are changes in the output of the autonomic nervous system, detected through the study of Heart Rate Variability (HRV). This non-invasive approach has highlighted that, in general, respiratory control techniques are primarily characterized by a shift in autonomic nervous system activity toward parasympathetic predominance. In other words, higher HRV associated with increased parasympathetic activity would be advantageous in dealing with stress-related responses, making our biological system significantly more resilient. On the contrary, a dysfunctional response to stress, commonly found in situations of chronic stress, anxiety, and depression, is characterized by autonomic nervous system activity dominated by sympathetic prevalence and low HRV (Fincham et al., 2023).
Chronic stress has a significant impact on individuals' health, being associated with numerous somatic pathologies such as hypertension, cardiovascular diseases, and making people more vulnerable to the development of mental disorders such as anxiety and depression, or the worsening of pre-existing morbid conditions (Birdee et al., 2023).
As observed from the analysis of scientific literature, it undoubtedly emerges that slow nasal breathing can induce, in addition to the synchronization of brain rhythms, an improvement in psychological well-being, characterized by increased relaxation and reduction of anxious and depressive symptoms. These effects seem to be expressions of parasympathetic dominance (Zaccaro et al., 2018), as well as modifications in brain complexity (Piarulli et al., 2018; Zaccaro et al., 2022).
It is not coincidental that the connection between respiratory activity and neural activity appears to have particularly intense effects on emotions: it has been observed that slow breathing protocols can have a relaxing and calming effect, while faster breathing tends to induce anxious states (Goheen et al., 2023). This dual mode of psychological response to respiratory frequency seems to find an explanation in the relationships between breathing and the activity of the locus coeruleus, a fundamental structure for arousal, attention and emotional expression. Sheikhbahaei & Smith, 2017; Yackle et al., 2017.
Going beyond the direct effect of breathing, its voluntary control during meditative techniques represents one of the main ways to maintain focused attention and, above all, serves as the primary channel for consciously activating the interoceptive network (Lutz et al., 2008; Fox et al., 2016). This network includes various brain regions, such as the insular cortex, the cingulate cortex, the inferior frontal gyrus, and the somatosensory cortex (Garcia-Cordero et al., 2017); moreover, this network has connections with the amygdala, the hypothalamus, and the hippocampus (Kleint et al., 2015; Khalsa et al., 2018). All types of meditation, besides inducing an improvement in interoceptive awareness, seem to modulate both the activity and thickness of the insula, which in turn correlate with breath control (Gibson, 2019). The perception and processing of visceral stimuli promote a conscious perception of bodily processes, playing a role in emotional experience and self-regulation processes. All of this assumes a pivotal dimension, meaning that a lack of awareness of internal physical processes has the potential to amplify stress, while a correct perception can enhance resilience (Schulz & Vögele, 2015).
In conclusion, slow breathing techniques appear to enhance autonomic, cerebral, emotional, and behavioral flexibility, leading to a series of benefits for individuals who practice them. On one hand, the psychophysiological changes induced by voluntary control of slow breathing seem to be linked to interoception and, therefore, to the voluntary regulation of internal states of the body. On the other hand, the role of the mechanoreceptors of the nasal vault, through the modulation of the olfactory bulb activity, appears to influence the activity of the entire cerebral cortex (Zaccaro et al., 2018).
