Eur J Appl Physiol DOI 10.1007/s00421-014-2927-5

Original Article

Psychophysiological responses of artificial gravity exposure to humans Sebastian Dern · Tobias Vogt · Vera Abeln · Heiko K. Strüder · Stefan Schneider 

Received: 17 February 2014 / Accepted: 30 May 2014 © Springer-Verlag Berlin Heidelberg 2014

Abstract  Aim The aim of this study was to determine psychophysiological responses and cognitive performance after a single bout of artificial gravity, in order to investigate its use as a potential holistic countermeasure for long-duration human space flight, considering mental health. Methods  Sixteen male participants were exposed to two different hypergravity protocols in a randomized order, one providing a constant +2 Gz environment for 30 min, the other providing participants for five times with repeated 3-min intervals of +2 Gz and rest, respectively. EEG was recorded prior, during and after AG. In addition, selfreported mood and cognitive performance was assessed before and after AG exposure. EEG data were analyzed using standardized brain electromagnetic tomography (sLORETA). Results  Beta-1 EEG activity (12–18 Hz) was decreased in the left middle frontal gyrus after the continuous profile. Participants’ motivation decreased after continuous artificial gravity, while perceived physical state was increased. The intermittent profile did not induce any changes in Communicated by Dick F. Stegeman. S. Dern · T. Vogt · V. Abeln · H. K. Strüder · S. Schneider (*)  Department of Exercise Neuroscience, Institute of Movement and Neurosciences, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933 Cologne, Germany e-mail: schneider@dshs‑koeln.de S. Dern · T. Vogt · V. Abeln · S. Schneider  Centre for Health and Integrative Physiology in Space (CHIPS), German Sport University Cologne, Cologne, Germany S. Schneider  Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Maroochydore, QLD, Australia

the observed parameters. Cognitive performance was not affected by either of both profiles. Conclusion The continuous profile induced neurophysiological changes, which are considered with negative affect and withdrawal related motivation, according to the model of frontal asymmetry. This notion was further confirmed by decreases in self-reported mood after continuous AG. Therefore, the continuous profile would not be appropriate for the human space flight program. Intermittent AG did not induce any psychophysiological changes and might therefore provide a more appropriate approach as a countermeasure for further investigations. Keywords Countermeasure · EEG · Frontal asymmetry · Neuroaffective response · sLORETA Abbreviations AG Artificial gravity ANOVA Analysis of Variance EEG Electroencephalography PFC Prefrontal cortex PSPs Synchronized postsynaptic potentials SAHC Short-arm human centrifuge sLORETA  Standardized low-resolution brain electromagnetic tomography

Introduction Maintaining psychological health and crew performance during long-term space missions is still one of the biggest issues in the human space flight program. Artificial gravity (AG), achieved through centrifugation, has been proposed as a promising tool to counteract negative physiological effects of exposure to weightlessness (Clément and

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Pavy-Le Traon 2004; Hargens et al. 2012), since current exercise protocols are not sufficient to fully prevent physiological deconditioning during long-term missions (Trappe et al. 2009; Gopalakrishnan et al. 2010). Besides the wellknown positive impact of AG on the musculoskeletal system and cardiovascular system (Iwase 2005; Caiozzo et al. 2009), which is currently under intense investigation as a possible replacement for exercise, yet very little is known about the effects on human neuroaffective and neurocognitive responses and mental health. Using the most advanced neuroimaging techniques such as functional magnetic resonance imaging (fMRI) or positron emission tomography (PET) is not possible due to technical and logistical limitations in changed gravity conditions (Genik et al. 2005). However, using imaging methods providing source localization have been proposed to be crucial in order to precisely describe the source of scalprecorded signals (Davidson 2004). Recording of electroencephalography (EEG) combined with standardized lowresolution brain electromagnetic tomography (sLORETA) has been shown to be a valid research tool to investigate the function of the central nervous system during changed gravity conditions (Schneider et al. 2008a, c). sLORETA is a reliable and well-established technique which has been validated against fMRI and PET (Mulert et al. 2004; Gamma et al. 2004; Bai et al. 2007). Resting asymmetrical brain activity in the prefrontal cortex (PFC), recorded with EEG, can provide a biological marker of affect and emotion (Davidson 2003, 2004). Relatively higher left-sided frontal activity has been associated with approach-related motivation and greater selfreported happiness (Coan and Allen 2004) while relatively higher right-sided activity is associated with avoidancerelated motivation (Allen and Kline 2004; Schutter et al. 2008), negatively valenced stimuli (Coan and Allen 2004) and withdrawal behavior (Allen and Kline 2004; Schutter et al. 2008). Thus, resting frontal asymmetry can serve as a marker of emotional anxiety (Coan and Allen 2004) and affective processing after AG. To date only few studies exist which investigated the relationship between psychophysiological parameters and changed gravity conditions. Research during parabolic flights has shown that electrocortical activity mirrors emotional and stress hormone responses (Schneider et al. 2007; Schneider et al. 2008a, b). A previous study which used EEG during and after a single bout of AG has found similar effects with a relatively higher right PFC activity during 15 min of +3 Gz exposure, inside of a long arm centrifuge, which vanished immediately after the termination of AG exposure (Schneider et al. 2009b, c). A recent study providing AG on a short-arm human centrifuge (SAHC), until initial signs of syncope emerged, further confirmed this assumption of psychological factors being mirrored

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Eur J Appl Physiol

in brain cortical activity (Smith et al. 2013). A first study, using a potential countermeasure alike profile by Vogt et al. (2014), compared the effects of AG with the well-known positive effects of exercise on electrocortical activity, mood and cognitive performance. While after exercise relaxed cortical states and an increased cognitive performance was observed, AG did not induce similar responses. The authors observed a global increase of cortical activity in the frontal cortex after AG exposure, i.e. an increase in the alpha and beta frequency range, which contrasts the model of cortical arousal (Miller 2007) and the authors concluded that this increase might reflect AG-related psychological stress. Therefore, an in depth and more sophisticated investigation of the frontal lobe is necessary. Furthermore, since only a continuous profile was investigated, providing a constant level of orthostatic stress, it is necessary to investigate other profiles, which might expose participants to a lower level of physiological strain through intermittent exposure. The purpose of this study is to investigate the impact of two different hypergravity profiles on brain electrocortical activity of the prefrontal cortex, using the model of frontal asymmetry, mood and cognitive performance. Within this study, it is hypothesized that AG, produced by a shortarm human centrifuge providing a +2 Gz environment, will increase relatively greater right PFC activity, which is associated with negative emotions and decreases in mood. It is further hypothesized that participants’ subjective rating of mood will likely decrease after AG exposure and thus, show a coherence with changes in PFC activity. Since stress and negative emotions are linked to cognitive processes we further hypothesize cognitive performance to be decreased after AG exposure.

Materials and methods Participants A total of 16 healthy males (29.57 ± 6.61 years, 183.21  ± 5.11 cm, 82.14 ± 7.24 kg) participated in this study. Participants had a varied amount of experience in altered gravity conditions and none reported taking any medication during the study. All subjects underwent a preliminary medical screening carried out by trained personnel from the German Aerospace Center (DLR) and were provided with written informed consent to participate in this study. Furthermore they were informed about the experimental protocol and possible consequences of the acceleration (nausea, dizziness, etc.). All procedures were in accordance with national legislation and the Declaration of Helsinki and human research ethics approval was obtained from the Medical Council of North-Rhine (Ärztekammer Nordrhein, Germany).

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Experimental protocol and procedure European Space Agency (ESA) Short-Arm Human Centrifuge (Verhaert Space, Belgium) at the German Aerospace Center, Institute for Aerospace Medicine was used to provide participants with increased levels of artificial gravity. Therefore one participant at a time lay in a supine position, secured by a harness within a nacelle, with their heads towards the center of rotation and the gravitational acceleration towards the feet (+Gz axis). Gravitational acceleration in this study is reported at subjects’ center of mass due to interindividual differences in +Gz levels at the feet because of variations in height. All participants were instructed to remain relaxed and to avoid excessive head movements during the experiment, which was fixed to a cushion to prevent vestibular input, which might lead to nausea. Moreover, a hood was placed over the head

throughout the procedure, limiting visual input, to further prevent nausea. Subjects did not receive any medication to prevent motion sickness. A randomized counterbalanced crossover design was used to assign participants to two experimental sessions, with a time lag of at least 48 h in between, consisting of two different artificial gravity exposure protocols of 30 min. During a continuous protocol participants were exposed to continuous +2 Gz acceleration for 30 min. The second protocol contained intermittences during AG. Thereby subjects were exposed to +2 Gz for 3 min, following a 3-min rest of baseline centrifugation at 5RPM (+0.03 Gz) of the centrifuge, thus providing subjects with five phases of AG and baseline conditions, respectively. Prior to each protocol a standardized acceleration protocol of 2 min at +1, +2 and +3 Gz each served as familiarization. This ramp was also repeated after each protocol (Fig. 1).

A

B

Fig.  1  a Experimental protocol of continuous artificial gravity exposure on a short-arm human centrifuge. Displayed are preparations (Prep) at acceleration speeds (±0 and baseline at +5 rpm) and AG levels (+1, +2 and +3 in Gz axis) including durations (1′, 2′, 15′ and 30′ min) of time spans. Two minutes of electro-cortical recordings (EEG) were performed prior (Pre) after 15 min of AG onset (Mid) and immediately after AG termination (Post). Mood perceptions (MOOD) and cognitive performance assessments (COG) were assessed prior pre resting EEG measurements and after post EEG measurements, in a time span of approximately 15 min. b Experimen-

tal protocol of intermittent artificial gravity exposure (AG) on a shortarm human centrifuge. Displayed are preparations (Prep) at acceleration speeds (±0 and baseline at +5 rpm) and AG levels (+1, +2 and +3 in Gz axis) including durations (1′, 2′, 3′ and 15′ min) of time spans. Two minutes of electro-cortical recordings (EEG) were performed prior (Pre), after 15 min of AG onset (Mid) and immediately after AG termination (Post). MOOD and COG were assessed prior pre resting EEG measurements and after post EEG measurements, in a time span of approximately 15 min

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On testing days the participants arrived 2 h prior to centrifugal acceleration. Electrocardiogram electrodes and a portable blood pressure system (Intellivue XDS, Phillips, Andover, USA) as well as a Finometer (Portapress, TVO, Amsterdam, Netherlands) giving beat-by-beat measurements, was used to monitor cardiovascular changes. A medical doctor determined immediate termination of the centrifugation, based on abnormal behavior of heart rate or impending signs of unconsciousness. In addition, audio and video loops, as well as a panic button, were available for the participants’ safety during the time of the acceleration. Resting electro-cortical activity was recorded for 2 min with participants’ eyes closed and in a supine position prior to the start of the session (Pre), during AG, i.e. 15 min after the onset of the protocol (Mid) and immediately after each session (Post). A profile of mood state and cognitive performance was assessed before and after AG exposure. Furthermore data of a control group (16 males with 20.56 ± 1.26 years, 182.56 ± 11.09 cm, 80.56 ± 11.56 kg) was collected for considering learning effects due to Pre– Post measurements of cognitive performance. EEG recording A portable EEG system (actiCAP, Brain Products, Munich, Germany) with 60 Ag/AgCl electrodes arranged in the international 10–20 system (Fp1, Fp2, F7, F5, F3, F1, Fz, F2, F4, F6, F8, FT9, FT7, FC5, FC3, FC1, FC2, FC4, FC6, FT8, FT10, T7, C5, C3, C1, Cz, C2, C4, C6, T8, TP9, TP7, CP5, CP3, CP1, CPz, CP2, CP4, CP6, TP8, TP10, P7, P5, P3, P1, Pz, P2, P4, P6, P8, PO7, PO3, POz, PO4, PO8, PO9, O1, Oz, O2, PO10) was mounted on the participants heads and position was secured by a chin strap. Selective positions served as reference (FCz) and ground (AFz) electrodes. The cap was suitable for different head sizes. To optimize conductivity and signal transduction electrodes were filled with electrode gel (SuperVisc™, Easycap GmbH, Herrsching, Germany) using a syringe and a blunt cannula. All electro-cortical signals were amplified and converted into digital signals (Brain Vision Recorder 1.1 software, Brain Products, Munich, Germany) with a sampling rate of 500 Hz. During EEG recording participants had their eyes closed and were asked to neither speak nor move. All recordings were supervised by a trained investigator.

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a participant’s current perceived physical state. Opposed to other psychological adjective scales (e.g., POMS), the Feelfinder allows for both psychological strain and motivational state assessments, including a short form of the ‘Eigenzustandsskala’ (EZ-scale; please refer to Kleinert (2006) and (Nitsch 1976) for developing details and operating modes of the MoodMeter®). The MoodMeter® used in this study contained two catalogues (Pre, Post), each consisting of the same 32 randomly presented adjectives. A 4-s time limit per adjective was set to obtain spontaneous answers within a six-step ranking scale, anchored to endpoints 0 = ‘not at all’ and 5 = ‘totally’. As given per instruction (‘Please, without any hesitation, to what extent does the following adjective apply to your physical state at this moment?’), participants took approximately 2 min to complete a catalogue. Cognitive performance The cognitive performance of each participant was assessed on a 3.5-inch touchscreen of a hand-held pocket PC based on computerized methods (Lumos Labs Inc., San Francisco, CA, USA). Three different standardized brain games (Chalkboard Challenge, Memory Matrix, Speed Brain) were used to assess executive functions. Chalkboard Challenge consisted of time-limited mental arithmetic with increasing levels of difficulty. Memory Matrix is based on an appearance-disappearance mode where complex patterns were to be memorized. Speed-related match-nomatch tasks were required in Speed Brain. Higher scores were achieved with greater accuracy in each brain game. As already performed in a previous study (Schneider et al. 2013) combined results formed a cognitive performance index, including executive functions, decision making, information processing and working memory. Cognitive performance index was computed by taking into account final scores of each brain game (consisting of the sum of all sub-categories for a brain game each, divided by the number of sub- categories), with the following equation: (score chalkboard challenge + score memory matrix + score speed brain)/3. Subjects performed the cognitive games in a seated position on the nacelle of the SAHC and took approximately 5 min to complete each cognitive performance assessment. EEG data analysis

Mood assessment Mood perceptions in this study were assessed using the MoodMeter® (Kleinert 2006) and consisted of Bodyfinder and Feelfinder modules. Traditionally developed for biomedically orientated research the Bodyfinder is very sensitive to short-term alterations in mood and determines

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EEG data was analyzed offline using Brain Vision Analyzer 2.0 (Brain Products, Munich Germany). A high pass filter of 0.5 Hz and a low pass filter of 50 Hz (time constant 0.3183099 s; 48 dB/octave) with an additional notch filter of 50 Hz was used to eliminate the majority of signals below and above the threshold. All channels exceeding an

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impedance of 10 kΩ were topographically interpolated to avoid exclusion from further analysis. Resting EEG periods were segmented into equally 4-s segments, with an overlap of 10 % between each section. After an automatic artifact rejection (gradient

Psychophysiological responses of artificial gravity exposure to humans.

The aim of this study was to determine psychophysiological responses and cognitive performance after a single bout of artificial gravity, in order to ...
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