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Brain response during controlled whole-body exposure

PeopleDutch adventurer Wim Hof is known as "The Iceman" after establishing several world records for prolonged resistance to cold exposure, an ability he attributes to a self-developed set of techniques of breathing and meditation, known as the Wim Hof Method. The first experimental study on how his brain responds to whole-body cold exposure has now been conducted.

Wayne State University School of Medicine professors Dr Otto Muzik and Dr Vaibhav Diwadkar changed that. They are the first to study how The Iceman's brain responds during experimentally controlled whole-body cold exposure. These investigations are part of the scientists' series of seminal studies launched in 2014 on how the human brain responds to thermo-regulatory challenges.

The results document compelling brain processes in The Iceman and present intriguing possibilities for how his techniques might exert positive effects related to disorders of the immune system and even psychiatry.

Over three days, Muzik and Diwadkar studied Hof's brain and body functions using two distinct imaging techniques – including functional magnetic resonance imaging (fMRI) to study his brain and positron emission tomography (PET) to study his body. During the studies, Hof wore a specifically designed whole-body suit the researchers could infuse with temperature-controlled water while the imaging data were acquired in order to relate changes in his biology to cold exposure.

The Iceman's results when compared to a group of healthy comparison participants were startling.

Practice of the Wim Hof Method made Hof's skin temperature relatively invariant to cold exposure, a finding the researchers attributed to his increased sympathetic innervation and glucose consumption in intercostal muscle revealed by PET imaging. The method appeared to allow him to generate heat that dissipates to lung tissue and warms circulating blood in the pulmonary capillaries.

"The wilful regulation of skin temperature – and, by implication, core body temperature, even when the body is being stressed with cold – is an unusual occurrence and may explain his resistance to frostbite," said Muzik, professor of paediatrics, of neurology and of radiology.

"From our previous studies, we expected The Iceman to show significant brain activations in a region known as the anterior insula, where the brain's higher thermoregulatory centres are located. However, we observed more substantial differences in an area called periaqueductal grey matter, located in the upper brainstem. This area is associated with brain mechanisms for the control of sensory pain and is thought to implement this control through the release of opioids and cannabinoids," Muzik added.

These last set of results are striking – not only for what they reveal about The Iceman, but even more so for the implications of the relevance of the Wim Hof Method for behavioural and physical health. The researchers hypothesise that by generating a stress-induced analgesic response in periaqueductal grey matter, the Wim Hof Method may promote the spontaneous release of opioids and cannabinoids in the brain. This effect has the potential to create a feeling of well-being, mood control and reduced anxiety.

"The practice of the Wim Hof Method may lead to tonic changes in autonomous brain mechanisms, a speculation that has implications for managing medical conditions ranging from diseases of the immune system to more intriguingly psychiatric conditions such as mood and anxiety disorders," said Diwadkar, professor of psychiatry and behavioural neurosciences. "We are in the process of implementing interventional studies that will evaluate these questions using behavioural and biological assessments. These possibilities are too intriguing to ignore."

"It is not mysterious to imagine that what we practice can change our physiology. The goal of our research is to ascertain the mechanisms underlying these changes using objective and scientific analyses, and to evaluate their relevance for medicine," Muzik added.

The defense of body temperature against environmental thermal challenges is a core objective of homeostatic regulation governed by the autonomic nervous system. Autonomous mechanisms of thermoregulation are only weakly affected by top-down modulation, allowing only transient tolerance for extreme cold. There is however, anecdotal evidence of a unique set of individuals known for extreme cold tolerance. Here we present a case study of a 57-year old Dutch national, Wim Hof, the so-called “Iceman”, with the ability to withstand frequent prolonged periods of extreme cold exposure based on the practice of a self-developed technique involving a combination of forced breathing, cold exposure and meditation (collectively referred to as the Wim Hof Method, henceforth “WHM”). The relative contributions of the brain and the periphery that endow the Iceman with these capabilities is unknown. To investigate this, we conducted multi-modal imaging assessments of the brain and the periphery using a combination of fMRI and PET/CT imaging. Thermoregulatory defense was evoked by subjecting the Iceman (and a cohort of typical controls) to a fMRI paradigm designed to generate periods of mild hypothermia interspersed by periods of return to basal core body temperature. fMRI was acquired in two separate sessions: in a typical (passive) state and following the practice of WHM. In addition, the Iceman also underwent a whole body PET/CT imaging session using the tracers C11-hydroxyephedrine (HED) and 18F-fluorodeoxyglucose (FDG) during both thermoneutral and prolonged mild cold conditions. This acquisition allowed us to determine changes in sympathetic innervation (HED) and glucose consumption (FDG) in muscle and fat tissues in the absence of the WHM. fMRI analyses indicated that the WHM activates primary control centers for descending pain/cold stimuli modulation in the periaqueductal gray (PAG), possibly initiating a stress-induced analgesic response. In addition, the WHM also engages higher-order cortical areas (left anterior and right middle insula) that are uniquely associated with self-reflection, and which facilitate both internal focus and sustained attention in the presence of averse (e.g. cold) external stimuli. However, the activation of brown adipose tissue (BAT) was unremarkable. Finally, forceful respiration results in increased sympathetic innervation and glucose consumption in intercostal muscle, generating heat that dissipates to lung tissue and warms circulating blood in the pulmonary capillaries. Our results provide compelling evidence for the primacy of the brain (CNS) rather than the body (peripheral mechanisms) in mediating the Iceman's responses to cold exposure. They also suggest the compelling possibility that the WHM might allow practitioners to develop higher level of control over key components of the autonomous system, with implications for lifestyle interventions that might ameliorate multiple clinical syndromes.

Otto Muzik, Kaice T Reilly, Vaibhav A Diwadkar

[link url="https://www.sciencedaily.com/releases/2018/02/180228164934.htm"]Wayne State University material[/link]
[link url="https://www.sciencedirect.com/science/article/pii/S1053811918300673?via%3Dihub"]Neurolmage abstract[/link]

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