Impact of acute partial-body cryostimulation on cognitive performance, cerebral oxygenation, and cardiac autonomic activity

www.nature.com/scientificreports OPEN Impact of acute partial‑body cryostimulation on cognitive performance, cerebral oxygenation, and cardiac autonomic activity Dimitri Theurot1, Benoit Dugué1, Wafa Douzi1, Paul Guitet1, Julien Louis2 & Olivier Dupuy 1,3* We assessed the effects of a 3-min partial-body cryostimulation (PBC) exposure—where the whole body is exposed to extreme cold, except the head—on cognitive inhibition performance and the possible implications of parasympathetic cardiac control and cerebral oxygenation. In a randomized controlled counterbalanced cross-over design, eighteen healthy young adults (nine males and nine females) completed a cognitive Stroop task before and after one single session of PBC (3-min exposure at − 150 °C cold air) and a control condition (3 min at room temperature, 20 °C). During the cognitive task, heart rate variability (HRV) and cerebral oxygenation of the prefrontal cortex were measured using heart rate monitoring and near-infrared spectroscopy methods. We also recorded the cerebral oxygenation during the PBC session. Stroop performance after PBC exposure was enhanced (562.0 ± 40.2 ms) compared to pre-PBC (602.0 ± 56.4 ms; P < 0.042) in males only, accompanied by an increase (P < 0.05) in HRV indices of parasympathetic tone, in greater proportion in males compared to females. During PBC, cerebral oxygenation decreased in a similar proportion in males and females but the cerebral extraction (deoxyhemoglobin: ΔHHb) remained higher after exposure in males, only. These data demonstrate that a single PBC session enhances the cognitive inhibition performance on a Stroop task in males, partly mediated by a greater parasympathetic cardiac control and greater cerebral oxygenation. The effects of PBC on cognitive function seem different in females, possibly explained by a different sensitivity to cold stimulation. The therapeutic effects of cold have been known for a very long time. Hippocrates (460–370 BC) already recommended the use of local cold application through ice and snow to relieve pain. In contemporary times, winter swimming regularly takes place in the form of bath in ice-cold water in certain countries1. Nowadays, local and systemic cold applications using various cryostimulation techniques (e.g. cold water immersion, ice application, partial- and whole-body cryostimulation) are widely used for therapeutic purposes, including the control of inflammation, pain, and swelling associated with certain p athologies2–4. In sports medicine, the use of whole- or partial-body cryostimulation (WBC or PBC, exposition of the whole body or the whole body except the head, respectively, to a very cold air) has gained popularity for its systemic effects on the organism, in particular to accelerate the post-exercise recovery process. For example, WBC and PBC were shown to reduce muscle pain sensations5,6, reduce inflammation7–9, improve s leep10,11, and possibly enhance recovery through an increased activation of the parasympathetic tone of the autonomic nervous system10,12–15 and muscle tissue oxygenation16. However, despite the plethora of studies conducted in the last decade, the physiological underpinning of PBC and WBC is not well known, and in particular its effects on the central nervous system and most particularly on cognitive function. 1 Laboratory MOVE (EA 6314), Faculty of Sport Sciences, University of Poitiers, 8 allée Jean Monnet, 86000 Poitiers, France. 2Research Institute for Sport and Exercise Sciences (RISES), Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK. 3Ecole de Kinésiologie et des Sciences de l’Actvivité Physique (EKSAP), Faculté de Medecine, Université de Montreal, Montreal, Canada. *email: Scientific Reports | (2021) 11:7793 | https://doi.org/10.1038/s41598-021-87089-y 1 Vol.:(0123456789) www.nature.com/scientificreports/ Age Height Weight BMI Fat mass % Male 22.3 ± 1.8 177.3 ± 4.9 77.7 ± 9.7 24.6 ± 2.5 15.2 ± 5.5 Female 22.8 ± 1.4 162.0 ± 6.0* 57.5 ± 9.4* 21.8 ± 2.3* 25.3 ± 5.0* Table 1.  Characteristics of participants. Data are presented mean ± SD. *Significant difference between male and female P < 0.05. Cognitive function refers to mental processes taking part in the acquisition and treatment of external information17. These mental processes are various and include functions such as memory, attention, and executive functions18. Good cognitive functioning is essential in daily life activities and processes such as executive function, which classically refers to inhibition, working memory, and cognitive flexibility allowing the realization of complex cognitive t asks19. Cognitive processes also play a major role in physical performance. Indeed, many sporting disciplines require strong executive functions, such as cognitive flexibility and inhibition, in order to make timely decisions and perform at one’s best. Executive functions, mainly under the control of the prefrontal cortex, are affected by several physiological mechanisms such as neuroendocrine responses and oxygen availability. Based on the neurovisceral integration model, heart rate variability (HRV) and executive functions are linked through the prefrontal neural function20,21, while the vagal related control of the myocardium is related to the prefrontal cortex a ctivity22. Previous studies evaluating the link between cardiac parasympathetic activation (measured through HRV indices), and performance of executive functions, revealed that a higher vagal tone was associated with better executive functioning23,24. On the contrary, decreased HRV indices of parasympathetic activation and increased sympathetic activation were linked to reduced performances of executive functions25. Moreover, increases in HRV indices of cardiac vagal control following aerobic exercise training were associated with enhanced performances of inhibition26. Brain oxygen availability also plays a major role in cognitive performance and increased cerebral oxygenation seems to be related to better executive function27–30. On the contrary, decreased cerebral oxygen availability as shown in different experimental conditions (i.e., exercise or hypoxia) negatively altered cognitive performance31. The influence of short-term cold exposure on human brain functioning and cognitive functions has not received much attention. Amongst the few studies conducted so far, a decrease in core body temperature following body exposure to cold would have a detrimental effect on cognitive p erformance18,32–34 including executive functions32. This detrimental effect would be explained by the distraction theory according to which the cold stimuli may interfere with the focus that should be put to the completion of a given cognitive task6. However, most of these studies evaluated cognitive performance during or following long-duration exposures to cold, such as two hours in 10 °C cold air32 or after cold water immersion34,35. The shorter exposure times (...truncated)