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Acta Astronautica

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Gender specific changes in cortical activation patterns duringexposure to artificial gravity

Stefan Schneider a,b,n, Ryan Robinson a, Craig Smith a, Melanie von der Wiesche c,Nandu Goswami d

a Institute of Movement and Neurosciences, German Sport University Cologne, Am Sportpark Müngersdorf 6, 50933 Köln, Germanyb Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Maroochydore, Queensland, Australiac Institute of Aerospace Medicine, German Aerospace Center (DLR), Cologne, Germanyd Institute of Physiology, Medical University Graz, Austria

a r t i c l e i n f o

Article history:Received 16 December 2013Received in revised form21 February 2014Accepted 4 March 2014

Keywords:EEGArtificial gravityExerciseBrain cortical activityAlpha activityGender

x.doi.org/10.1016/j.actaastro.2014.03.00365/& 2014 IAA. Published by Elsevier Ltd. A

esponding author at: Institute for MovemenSport University Cologne, Am Sportpark M

ermany. Tel.: þ49 173 7078760; fax: þ49 22ail address: schneider@dshs-koeln.de (S. Sch

e cite this article as: S. Schneider, ecial gravity, Acta Astronautica (2014

a b s t r a c t

Keeping astronauts healthy during long duration spaceflight remains a challenge. Artificialgravity (AG) generated by a short arm human centrifuges (SAHC) is proposed as the nextgeneration of integrated countermeasure devices that will allow human beings to safelyspend extended durations in space, although comparatively little is known about anypsychological side effects of AG on brain function.

16 participants (8 male and 8 female, GENDER) were exposed to 10 min at a baselinegravitational load (G-Load) of þ .03 Gz, then 10 min at þ .6 Gz for females and þ .8 Gz formales, before being exposed to increasing levels of AG in a stepped manner by increasingthe acceleration by þ .1 Gz every 3 min until showing signs of pre-syncope. EEGrecordings were taken of brain activity during 2 min time periods at each AG level.Analysing the results of the mixed total population of participants by two way ANOVA,a significant effect of centrifugation on alpha and beta activity was found (po .01).Furthermore results revealed a significant interaction between G-LOAD and GENDERalpha-activity (po .01), but not for beta-activity.

Although the increase in alpha and beta activity with G-LOAD does not reflecta general model of cortical arousal and therefore cannot support previous findingsreporting that AG may be a cognitively arousing environment, the gender specificresponses identified in this study may have wider implications for EEG and AG research.

& 2014 IAA. Published by Elsevier Ltd. All rights reserved.

1. Introduction

Artificial gravity (AG) has been suggested as a keyintegrated countermeasure for astronauts to combat thephysiological deconditioning that occurs during long dura-tion spaceflight [1]. Centrifugal forces would impart þGz

ll rights reserved.

t and Neurosciences,üngersdorf 6, 509331 4973454.neider).

t al., Gender specific c), http://dx.doi.org/10

acceleration to the body and these ‘head to toe’ forces wouldprovide sufficient gravitational loading to stimulate variousphysiological systems of the body in a way to preserve theirnormal physiological functions as for example bone andmuscle strength [2]. However, the optimal ‘dose’ of AG forastronauts has not yet been determined [3].

Beside a study by Biernacki et al. [4] reporting no changesin subjective enjoyment during centrifugation, but insteadpositive changes in arousal such as increased energy andreduced tension currently no further information exist con-cerning psychophysiological effects of artificial gravity and

hanges in cortical activation patterns during exposure to.1016/j.actaastro.2014.03.003i

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accordingly further work seems necessary to determineexactly how AG is affecting cognition and the brain. AlthoughAG may indeed bring benefits in terms of preventing thephysiological deconditioning normally associated with longduration spaceflight, if it is lowering mood, raising thestress levels [5,6] or impairing the cognitive abilities [7] ofastronauts already working in a pressured and technicalenvironment, then its suitability as a countermeasure duringspaceflight may have to be reconsidered.

To further investigate how the brain responds tohypergravity, it is necessary to record brain activity duringcentrifugation itself. Given the practical limitations ofworking within such an environment [8], electroencepha-lographic (EEG) recordings are an ideal method to employfor such a task. The location of particular interest is thefrontal cortex, as it is associated with higher cognition,mood and motivation [9]. Traditionally alpha activity inthe frontal cortex has been the main focus of investiga-tions. The traditional model of arousal assumes that theslower alpha activity (8–12 Hz) is predominant in a morerelaxed state, whilst a decrease of alpha activity and anincrease in beta activity (12–35 Hz) is associated withstress and arousal [10].

As gender differences in cognition and responses tostressful situations have been observed previously [11],and coupled with the fact that males and females showdifferences in þGz acceleration tolerance [12], it seemslikely that centrifugation may have some gender specificeffects on the brain in terms of mood and cognition.

This study was carried out under the hypothesis thatcentrifugation would induce a stress related state withinindividuals and would result in observable changes infrontal cortex activity, with beta activity expected toincrease whilst alpha activity decreases. This hypothesiswas tested by using a short arm human centrifuge toexpose participants to increasing levels of AG and measur-ing cortical activity using EEG in the alpha and betafrequency bands. Additionally, by testing a mixed popula-tion, gender specific differences in responses to centrifu-gation were hypothesised.

2. Methods

2.1. Participants and procedures

After providing informed consent, 16 healthy volun-teers (8 male and 8 female; mean age 26.774.43 years)with no prior history of vasovagal syncope were selectedfor this study. None of the participants had any experiencewith artificial gravity or microgravity. Participants com-pleted a medical examination to confirm suitability, nofurther exclusion or inclusion criteria existed. Ethicalapproval was obtained for this study (Ethik-Kommisssionder Ärztekammer Nordrhein, Düsseldorf, Germany) inaccordance with the ethical standards laid down in the1964 Declaration of Helsinki. Participants could withdrawfrom the study or terminate participation at any time.

The European Space Agency (ESA) Short Arm HumanCentrifuge (SAHC) (Verhaert Space, Belgium) at the DLRInstitute for Aerospace Medicine (Cologne, Germany) wasused to expose participants to increasing levels of artificial

Please cite this article as: S. Schneider, et al., Gender specific cartificial gravity, Acta Astronautica (2014), http://dx.doi.org/10

gravity in a stepped manner. One participant at a time laysupine on a nacelle of the SAHC, positioned with theirheads towards the centre and feet pointing outwards. Allparticipants were instructed to remain relaxed and refrainfrom head movements during the experiment. Twoseparate protocols for males and females were used basedon previous findings of gender differences in þGz toler-ance [12]. The protocol began with 60 min in a 61 headdown tilt position to simulate the cardiovascular shiftsthat occurs during spaceflight before returning to a supineposition to begin the centrifugation run. Next, participantswere exposed to 10 min of a BASELINE centrifugationspeed of 5 rpm, producing þ .03 Gz (Note that all þGzlevels quoted in this study are as measured at heart level),followed by 10 min of þ .8 Gz for males or þ .6 Gz forfemales. The differences between male and female werechosen in order to guarantee a sufficient number of stagesto be completed before signs of presyncope occur. Previousexperience with the SAHC showed that female participantsshow signs of presyncope earlier than male participants(unpublished observation by the SAHC team at DLR).Female participants were tested in the middle of theirmenstrual cycle.

From this point the artificial gravity level was increasedby þ .1 Gz every 3 min. Centrifugation increased in thismanner until the point at which any symptoms of pre-syncope occurred, as identified by a trained medicalmonitor.

2.2. EEG recordings

Two minute EEG recordings were taken at each level ofcentrifugation, during which time the participants wereasked to close their eyes so that artefacts from muscleactivity such as blinking would be minimised and wereasked not to move or speak. During set up, participantswere fitted with an EEG cap with 32 active Ag/AgClelectrode sensor sites (ActiCap – Brain Products, Germany)in the positions FP1, FP2, F7, F3, Fz, F4, F8, FC5, FC1, FC2,FC6, T7, C3, Cz, C4, T8, TP9, CP5, CP1, CP2, CP6, TP10, P7, P3,Pz, P4, P8, PO9, O1, Oz, O2, and PO10 as per the interna-tional 10–20 system [13]. Two additional references elec-trodes (GROUND and REF) were also used. To aid signaltransduction, prior to fitting the EEG cap each electrodewas pre-filled with electrolyte gel (SuperVisc™, EasyCapGmbH, Herrsching, Germany). Additional electrolyte gelwas applied using a syringe and blunt cannula to ensuresufficient conductivity between the scalp and the elec-trode. Sufficient conductivity was confirmed by checkingto ensure the impedance of all electrodes did not exceedten kilo Ohm (kΩ). Analogue EEG signals were convertedto digital and stored using a Brain Vision Amplifier andRecView software (Brain Products GmbH, Munich, Germany)with a sample rate of 500 Hz.

2.3. EEG data analysis

EEG data was analysed offline using Brain VisionAnalyser (Brain Products GmbH, Munich, Germany). Highand low pass filters were applied so that the majority ofsignals below and above between .5 and 70 Hz were

hanges in cortical activation patterns during exposure to.1016/j.actaastro.2014.03.003i

Fig. 1. Diagram of centrifugation profile. Different protocols were used for males and females. Boxes labelled ‘EEG’ denote the time periods during whichEEG recordings were analysed. The protocol continued increasing the þGz acceleration in the stepped manner observed until the symptoms of presyncopeoccurred.

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eliminated (time constant .318 s; 24 dB/octave). A notch filterwas also applied at 50 Hz to remove interference signalsfrom power sources. 10 s sections at the beginning and endof each 2 min ‘eyes closed’ period were discarded, leavinga 100 s recording to analyse. This was segmented furtherinto 4 s sections, with a 10% overlap between each section.A combination of automatic artefact rejection (maximalamplitude¼200 μV; minimal amplitude¼�200 μV; gradi-ent o50 μV/ms) and manual artefact rejection (visualinspection of the data for excessive noise, movement arte-facts or electrodes producing no signal) allowed for theidentification and removal of abnormal electrodes signalsor segments. Any electrodes signals that were removed insuch a manner were recalculated using topographic inter-polation (spline interpolation; order¼4; degree¼10;lambda¼1e�05). Abnormal segments were not recalculated.Application of a fast Fourier transformation (half spectrum;maximum resolution; Hanning Window¼10%) allowed foranalysis of frequency spectra within EEG signals. The remain-ing segments were then combined, producing an averagedfrequency activity for each electrode at a specific þGz level.Finally, the activity from electrodes covering five main areasof the cortex were pooled together (frontal¼Fp1, Fp2, F3, F4,F7, F8, FC1, FC2, FC5, FC6, Fz; temporal¼T7, T8, TP9, TP10;parietal¼P3, P4, P7, P8, PO9, PO10, Pz; central¼C3, C4, CP1,CP2, CP5, CP6, Cz; occipital¼O1, O2, Oz), with raw sums ofactivity exported for alpha activity (7.5–12.5 Hz) and betaactivity (12.5–35) in each pooled region.

2.4. Statistics

For statistical analysis data was normalised by using log-transformation [V0 ¼ ln(V)]. To analyse differences in genderas well as to indicate whether possible changes in frontalactivity are region specific, a two way ANOVA was used withfactors GENDER (Male, Female), REGION (frontal, parietal,central, temporal, occipital) and G-LOAD (repeated mea-sures: BASELINE, BASELINEþ1, MAXIMUM�1, MAXIMUM).If ANOVA results were significant, post-hoc analysis wascarried out using Fisher's LSD test Fig. 1.

Please cite this article as: S. Schneider, et al., Gender specific cartificial gravity, Acta Astronautica (2014), http://dx.doi.org/10

3. Results

3.1. Alpha activity

Whereas the statistical analysis revealed no significantinteractions between GENDER, REGION and G-LOAD(F(12, 210)¼ .19, p¼ .99), an effect of G-LOAD and GENDERwas noticeable (F(3, 210)¼4.19, po .01 – Fig. 2). Post hocanalysis revealed a significant increase of alpha activity formale participants comparing the three measurementsduring G-load with baseline data (po .01). No effect forG-LOAD and REGION was noticeable (F(12, 210)¼1.37,p¼ .18).

3.2. Beta activity

No significant interactions between GENDER, REGION andG-LOAD could be obtained for beta activity (F(12, 210)¼ .25,p¼ .99). In contrast to alpha activity, no G-LOADnGENDEReffect was noticeable (F(3, 210)¼1.01, p¼ .39) but a main effectfor G-LOAD was noticeable (F(3, 210)¼4.96, po.01 – Fig. 2).A following post-hoc analysis revealed an increase comparingBASELINE with BASELINEþ1 (po.001) and MAXIMUM(po.01) whereas MAXIMUM-1 missed significance margin-ally (p¼ .08). Again no differences between REGIONS overG-LOAD were detectable (F(12, 210)¼ .88, p¼ .57).

4. Discussion

This study was designed to study the effects of artificialgravity on the activity of the frontal regions of the braincommonly associated with mood and cognition. EEGrecording was chosen as the most suitable form of brainimaging technique to be used during artificial gravity.Beside a global increase of cortical beta frequency rangeswith increasing G-loads, a male specific increase in globalalpha activity could be noted within this study.

hanges in cortical activation patterns during exposure to.1016/j.actaastro.2014.03.003i

Fig. 2. Changes in alpha-activity (bottom) and beta-activity (top) across G-LOAD (Baseline, Baselineþ1, Maximum�1, Maximum) differentiated betweenGENDER (female n¼8, dashed line, male n¼8, solid line). An increase within the male population in alpha-activity as well as an increase in beta-activity forboth populations could be obtained under G-load. Graphs show means 7 .95 confident intervals. nnn indicates po .001, nn indicates po .01.

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4.1. Changes in brain activity related to G-load

Although alpha- and beta-activity in the frontal cortexincreased with G-load, these changes where mirrored inglobal activity and therefore could not necessarily beidentified to reflect specific emotional or mental changes.Whilst previous studies [5,6] reported increased arousalduring artificial gravity being related to changes in frontalcortex activity, this is not reflected in an increase of beta ordecrease of alpha activity ion in this study.

It must be noted that one difficulty in assessing thecontext of the findings of this study within the wider EEGliterature is partly down to the variability results pre-viously reported. In a review paper summarising thechanges in EEG activity that accompany meditation, Cahnand Polich [14] showed that from several dozen studiesthere is no clear consensus on whether specific frequencybands increase or decrease during meditation. Compound-ing these issues is the fact that different classifications forEEG frequency bands have been used previously, withsome studies labelling the frequency range of 6–9 Hz astheta activity, whilst labelled this range as ‘sub alpha’activity [15]. Additionally, the majority of EEG studies with

Please cite this article as: S. Schneider, et al., Gender specific cartificial gravity, Acta Astronautica (2014), http://dx.doi.org/10

altered gravity levels have come from studies with dataonly from males [4,16]. In terms of previous studiesinvestigating EEG responses to stimuli, Corsi-Cabereraet al. [17] reported that during a task solving experimentrelative alpha power decreased equally for both sexeswhilst theta power increased, although this study specifi-cally looked at the parietal lobes. This discrepancybetween the EEG changes during task based responsesand this current study (where alpha power increased onlyin males and did not change in females) may hint at someof the unique cognitive processes that occur during stress.

But also the reliability of a general model of arousal, i.e.that alpha activity decreases in response to stress, whilstbeta activity increases, is questionable. Recent studiesreporting changes in brain cortical activity after exercise,provoking similar cardiovascular effects as reported duringartificial gravity, revealed that changes in the lower (delta,theta) as well as the higher (beta, gamma) frequencybands were of similar magnitude to those observed inthe alpha range [18,19]. Therefore no more than an overallcortical activation after exercise could be posited. Whilstthe described model of arousal seems to be a decent wayto analyse changes in psychological arousal, such cortical

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activation patterns might be superposed by physiologicalarousal and therefore a different way of analysis like forexample cortical current density as proposed by Smithet al. [6] seems more applicable. Further research seemsnecessary to distinguish different ways of analysis in onecohort of participants.

4.2. Gender differences

Alpha activity showed a significant interaction betweengender and the effects of centrifugation. Additional analy-sis confirmed an increase in alpha-activity in male but notfemale population. Gender differences in beta-activity andgender interactions with G-LOAD could not be identified.Whilst links between increased alpha activity andincreased cortical activity have been noted previously[20], questions remain as to the underlying reasons forthe observed gender differences.

In a study by Matud [11] comparing stress copingmechanisms, females were reported to suffer more stressthan men, and have more emotional based copingmechanisms. Women also showed significant changes inthe oxy-haemoglobin responses in the prefrontal cortex,whilst men did not, as measured by near infrared spectro-scopy [21]. In a study using a noxious heat stimulusapplied to the hand, Paulson et al. [22] found that femaleshad a significantly greater activation of the contralateralprefrontal cortex in comparison to males when as mea-sured by changes in regional cerebral blood flow asdetected by positron emission tomography (PET) and alsosubjectively rated a 50 1C stimulus as significantly moreintense than males. As alpha activity is negatively corre-lated with brain activity, the findings in this study supportthese ideas. Biernacki et al. [4] also reported increases inpositive arousal effects from centrifugation, and impor-tantly their study was composed of only male cadets asparticipants, who likely experienced centrifugation asmore of a ‘positive thrill’.

Gender differences in þGz tolerances could possiblyalso explain some of these changes, as however maximalG-loads experiences by both males and females werefound to be comparable.

Although gender differences were previously identifiedto exist with regards to baseline EEG activity and duringcognition tasks, this study is noteworthy in that it high-lights gender specific responses to the stimulus of centri-fugation. It will be important to confirm whether thiseffect seen in this study is unique to centrifugation aloneor whether this can be seen in response to other suchstimuli, perhaps then revealing if the physiologicaldemands of centrifugation are key to these findings.

4.3. Limitations and implications for AG as an effectivecountermeasure

AG devices are proposed to be a ‘next generationintegrated countermeasure’ that will enable astronauts tostay healthy during extended periods of microgravity.However, given the array of psychological challenges thatare likely to be faced during such missions [23], thenfurther studies are necessary determining whether higher

Please cite this article as: S. Schneider, et al., Gender specific cartificial gravity, Acta Astronautica (2014), http://dx.doi.org/10

intensities of AG are perhaps negatively affecting moodand cognition [6].

It may be important to use EEG imaging to determinewhether any lingering signs of negative mood or stressremain after AG exposure, or whether the changes identi-fied in this study are confined only to the period of AGitself. It would be also advisable to investigate whether themagnitude or duration of centrifugation could be reducedto the point where not only the physiological benefits ofAG remained but also that astronauts do not findthe experience unpleasant or stressful. Whereas higherG-loads seemed to be preferable for the adaptation of theskeletal system and longer duration (going along withlower G-loads) are preferred for cardiovascular adapta-tions, further investigation seems necessary to identify theindividual load and duration of AG in order to maximise itseffect on all physiological and psychological systems.

Future studies could also investigate whether changesin EEG activity are preserved, reduced or amplified duringthe exposure of daily centrifugation over several days insubjects with no prior experience of AG. If subsequently itis found that any negative changes in cognitive statesdiminished over time, then this would then lend weight tothe idea that astronauts should receive prior training andfamiliarisation with AG environments.

That gender in itself is a factor that must be accountedraises questions as to which other factors must also beconsidered, investigated and controlled to identify theirsignificance to cognition and mood. Prior experience to AGenvironments may be another factor worth investigating.

Future studies should try to combine records of sub-jective experiences as well as other markers of stress andarousal to determine the emotional nature of centrifuga-tion. Designing future experiments to carefully tease apartthe direct contribution of centrifugation may be a challen-ging task, but not insurmountable.

Acknowledgements

This study was funded by the European Space Agencies(ESA) Ground Based Facilities (GBF) program. In addition thisstudy was funded by German Space Agency (DLR50WB1161).The authors would like to thank all participants as well asthe SAHC team of the German Space Agency.

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