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Changes in intrinsic functional brain connectivity after first-time exposure to parabolic flight.

Angelique Van Ombergen1*, Floris L. Wuyts1, Ben Jeurissen1, Jan Sijbers1, Floris Vanhevel2, Steven D. Jillings1, Paul M. Parizel1, Stefan Sunaert3, Paul H. Van De Heyning1, Vincent Dousset4, Steven Laureys5 and Athena Demertzi5
  • 1 University of Antwerp, Belgium
  • 2 Antwerp University Hospital, Belgium
  • 3 KU Leuven, Belgium
  • 4 Centre Hospitalier Universitaire (CHU) de Bordeaux, France
  • 5 University of Liege, Belgium

Space is a hostile environment for humans and spaceflight induces several physiological changes in the human body, such as fluid shifts, neurovestibular disturbances, bone loss and muscle atrophy1. Space crew are known to adapt fairly well to some of these detrimental effects, depending on the site of action and the applied countermeasures1. The central nervous system also seems capable of adaptation to microgravity by the process of neuroplasticity, as previously shown in animals2–4. Yet, little is known about the effects of microgravity and gravity transitions on the human brain5. Recently, in a functional MRI study with a single cosmonaut, we showed that long-duration spaceflight induced functional changes in the right insula and in sensorimotor-cerebellar connectivity6. In addition, head-down bed rest studies, a spaceflight analog, have also shown alterations in brain functional connectivity, particularly in sensorimotor areas7. In parallel to spaceflight research, ground-based models have been developed to overcome some of the logistic challenges related to human spaceflight research. Such a “ground-based” alternative is parabolic flight (PF), during which a specific parabolic trajectory is carried out, wherein the acceleration of the aircraft cancels the gravity acceleration. A hypergravity phase, characterized by 1.5-1.8g, precedes and follows the microgravity phase. Microgravity resembles zero g and lasts around 20–25s. In between parabolas, the aircraft flies in normal 1g conditions8. PF consists of gravity transitions, (microgravity, hypergravity and normal gravity phases), generated during 31 parabolas. An entire flight lasts around 3 to 3.5h (Figure 1). The present study aimed to measure the effects of acute gravitational transitions, as induced by PF, on the brain of naïve human subjects. During a PF, and especially during the microgravity phase, the vestibular input is largely disturbed and therefore might cause an incongruity with the normal terrestrial expectations regarding verticality and spatial orientation9. As no previous neuroimaging investigations have been performed under these conditions5,10,11, a data-driven approach was implemented to investigate changes in fMRI functional connectivity during resting state. To this aim, we included 28 healthy participants (11 female; mean(SD) age of 31 (7) years). Each volunteer participated in one parabolic flight of an ESA parabolic flight campaign in Bordeaux, France (flown by Novespace), over the course of 2014-2015. Prior to the PF, all selected participants received scopolamine (0.25mg/1mL; 0.7mL for males and 0.5mL for females), a muscarinic receptor antagonist known to alleviate motion sickness12. To account for the effects of the drug, an independent control group of 12 adults (4 female; mean (SD) age 24 (3) years) who received scopolamine was also included. These participants had no previous experience with PFs. Each participant received two 3T resting-state functional MRI scans. For the PF group, pre- and post-flight data were acquired on a 3T GE MR 750 W (GE Healthcare, Milwaukee, Wisconsin, USA) MRI scanner at the University of Bordeaux and University Hospital of Bordeaux (France), using a 32-channel head coil. For the scopolamine control group (non-PF): two scanning sessions took place, a baseline medication-free session and 3 hours after the administration of scopolamine (Antwerp University Hospital, Belgium). Pre- and post-scopolamine data were acquired on a 3T Siemens MAGNETOM Prisma scanner (Siemens, Erlangen, Germany), using a 32-channel head coil. During the resting state scanning period, an identical MRI sequence was used as for the PF group. For a full overview of sequence parameters, readers are referred to the full publication13. Data preprocessing was performed with Statistical Parametric Mapping 12 (SPM12; www.fil.ion.ucl.ac.uk/spm) and statistical analysis with the CONN v.16 functional connectivity toolbox (www.nitrc.org/projects/conn). Statistical analysis adopted a hypothesis-free (voxel-to-voxel) approach and made use of the intrinsic connectivity contrast (ICC)14, which characterizes the strength of the global connectivity pattern between each voxel and the rest of the brain. For a full overview of data preprocessing and analysis, readers are referred to the full publication13. For the ICC analysis, the main effects of each group at pre- and post-scan were investigated. For the PF group, between-condition differences were identified in posterior cingulate cortex and right parietal gyrus. For the non-PF group, no post-pre scan differences in ICC connectivity were found. The interaction analysis revealed that the modification of the connectivity pattern was observed in the right temporo-parietal junction (rTPJ)/the angular gyrus (rAG) in the PF group in comparison to the scopolamine group, at post-scan as compared to pre-scan assessment (T(38)= -3.32, p<.001 FWE cluster-level, permutation testing; cluster size: 260 voxels, peak coordinate x,y,z=[58 -64 18]) (Figure 2). With no a priori assumptions, we found a decrease of the ICC scores in the rTPJ/rAG after the PF. These results suggest the rAG/TPG has reduced participation in whole-brain connectivity after short-term exposure to altered gravity, most possibly related to vestibular function alterations. Previous investigations also suggest that the rAG is involved in the processing and integration of vestibular, visual and proprioceptive input15. For example, inhibition of the right TPJ caused difficulties with the perception of the upright and maintaining an internal representation of verticality16,17. These results are relevant for long-duration spaceflight, as well as for space tourism, where less-trained humans will be exposed to similar and even more extreme gravitational transitions. Taken together, our findings shed light on the understanding of how the brain is affected by short-term alteration of gravitational input and the internalization of gravity in the human brain. Full publication: Van Ombergen A, Wuyts FL, Jeurissen B, et al. Intrinsic functional connectivity reduces after first-time exposure to short-term gravitational alterations induced by parabolic flight. Sci Rep 2017;7:3061.

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Acknowledgements

This work was supported by the European Space Agency (ESA), BELSPO Prodex, the Research Foundation Flanders (FWO Vlaanderen) the Belgian National Funds for Scientific Research (FRS-FNRS), IAP research network P7/06 of the Belgian Government (Belgian Science Policy), the European Commission, the Human Brain Project (EU-H2020-FETFLAGSHIP-HBP-SGA1-GA720270) and the LUMINOUS project (EU-H2020-FETOPEN-GA686764).

References

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Keywords: parabolic flight, microgravity, fMRI — functional magnetic resonance imaging, rsfMRI = resting state fMRI, brain connectivity, Aerospace

Conference: 39th ISGP Meeting & ESA Life Sciences Meeting, Noordwijk, Netherlands, 18 Jun - 22 Jun, 2018.

Presentation Type: Extended abstract

Topic: Neurosciences and psychology

Citation: Van Ombergen A, Wuyts FL, Jeurissen B, Sijbers J, Vanhevel F, Jillings SD, Parizel PM, Sunaert S, Van De Heyning PH, Dousset V, Laureys S and Demertzi A (2019). Changes in intrinsic functional brain connectivity after first-time exposure to parabolic flight.. Front. Physiol. Conference Abstract: 39th ISGP Meeting & ESA Life Sciences Meeting. doi: 10.3389/conf.fphys.2018.26.00017

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Received: 02 Dec 2018; Published Online: 16 Jan 2019.

* Correspondence: Dr. Angelique Van Ombergen, University of Antwerp, Antwerp, Belgium, Angelique.van.ombergen@esa.int