journal article Open Access Feb 18, 2021

Brain functional connectivity differs when viewing pictures from natural and built environments using fMRI resting state analysis

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Abstract
AbstractHuman beings evolved in “natural” environments. Many intervention studies have shown that exposure to natural environments (compared to built/urban environments) reduces stress and increases cognitive functioning. We set out to test differences in fMRI functional connectivity while showing participants photographs from natural versus built environments (matched in terms of scenicness ratings). No differences in self-reported perceived stress, rumination, valence, arousal or dominance were observed. However, functional connectivity was significantly higher when participants saw natural rather than built environmental photographs in circuits consisting of dorsal attention network (DAN) and ventral attention network (VAN), DAN and default mode network (DMN) and DMN and Somatomotor connections. In addition, we observed lower functional connectivity during the natural environment condition correlated with more years that individuals spent in major cities during upbringing. Future studies, linking changes in cognitive functioning due to nature exposure and alterations in functional connectivity, are warranted.
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References
57
[1]
Wilson, E. Biophilia: The Human Bond with Other Species (Harvard University Press, Cambridge, 1984). 10.4159/9780674045231
[2]
Ohly, H. et al. Attention restoration theory: a systematic review of the attention restoration potential of exposure to natural environments. J. Toxicol. Environ. Health B Crit. Rev. 19, 305–343. https://doi.org/10.1080/10937404.2016.1196155 (2016). 10.1080/10937404.2016.1196155
[3]
Attention Restoration Theory II: a systematic review to clarify attention processes affected by exposure to natural environments

Matt P. Stevenson, Theresa Schilhab, Peter Bentsen

Journal of Toxicology and Environmental Health, Pa... 2018 10.1080/10937404.2018.1505571
[4]
Jo, H., Song, C. & Miyazaki, Y. Physiological benefits of viewing nature: a systematic review of indoor experiments. Int. J. Environ. Res. Public Health 16, 1. https://doi.org/10.3390/ijerph16234739 (2019). 10.3390/ijerph16234739
[5]
Kaplan, R. & Kaplan, S. The Experience of Nature. A Psychological Perspective (Cambridge University Press, Cambridge, 1989).
[6]
Stress recovery during exposure to natural and urban environments

Roger S. Ulrich, Robert F. Simons, Barbara D. Losito et al.

Journal of Environmental Psychology 1991 10.1016/s0272-4944(05)80184-7
[7]
Ulrich, R. S. Natural versus urban scenes: some psychophysiological effects. Environ. Behav. 13, 523–556. https://doi.org/10.1177/0013916581135001 (1981). 10.1177/0013916581135001
[8]
Chang, C.-Y., Hammitt, W. E., Chen, P.-K., Machnik, L. & Su, W.-C. Psychophysiological responses and restorative values of natural environments in Taiwan. Landsc. Urban Plan. 85, 79–84. https://doi.org/10.1016/j.landurbplan.2007.09.010 (2008). 10.1016/j.landurbplan.2007.09.010
[9]
Chang, C. Y., Lin, Y. H. & Chou, M. T. Experiences and stress reduction of viewing natural environmental settings. Acta Hortic. https://doi.org/10.17660/ActaHortic.2008.775.16 (2008). 10.17660/actahortic.2008.775.16
[10]
Hassan, A. et al. Effects of walking in bamboo forest and city environments on brainwave activity in young adults. Evid Based Complement. Alternat. Med. 2018, 9653857. https://doi.org/10.1155/2018/9653857 (2018). 10.1155/2018/9653857
[11]
Kim, G. W. & Jeong, G. W. Brain activation patterns associated with the human comfortability of residential environments: 3.0-T functional MRI. NeuroReport 25, 915–920. https://doi.org/10.1097/WNR.0000000000000205 (2014). 10.1097/wnr.0000000000000205
[12]
Kim, G. W. et al. Functional neuroanatomy associated with natural and urban scenic views in the human brain: 3.0T functional MR imaging. Korean J. Radiol. 11, 507–513. https://doi.org/10.3348/kjr.2010.11.5.507 (2010). 10.3348/kjr.2010.11.5.507
[13]
Kim, T. H. et al. Human brain activation in response to visual stimulation with rural and urban scenery pictures: a functional magnetic resonance imaging study. Sci. Total Environ. 408, 2600–2607. https://doi.org/10.1016/j.scitotenv.2010.02.025 (2010). 10.1016/j.scitotenv.2010.02.025
[14]
Vedder, A. et al. Neurofunctional correlates of environmental cognition: an FMRI study with images from episodic memory. PLoS ONE 10, e0122470. https://doi.org/10.1371/journal.pone.0122470 (2015). 10.1371/journal.pone.0122470
[15]
Tang, I. C. et al. Using functional magnetic resonance imaging (fMRI) to analyze brain region activity when viewing landscapes. Landsc. Urban Plan. 162, 137–144. https://doi.org/10.1016/j.landurbplan.2017.02.007 (2017). 10.1016/j.landurbplan.2017.02.007
[16]
Seiyama, A. et al. Neural bases on cognitive aspect of landscape evaluation: a study using functional magnetic resonance imaging. J. Neurol. Neurosci. https://doi.org/10.21767/2171-6625.1000263 (2018). 10.21767/2171-6625.1000263
[17]
Pati, D. et al. Neural correlates of nature stimuli: an FMRI study. HERD 7, 9–28. https://doi.org/10.1177/193758671400700202 (2014). 10.1177/193758671400700202
[18]
Gould van Praag, C. D. et al. Mind-wandering and alterations to default mode network connectivity when listening to naturalistic versus artificial sounds. Sci. Rep. 7, 45273. https://doi.org/10.1038/srep45273 (2017). 10.1038/srep45273
[19]
Chen, Z., He, Y. & Yu, Y. Enhanced functional connectivity properties of human brains during in-situ nature experience. PeerJ 4, e2210. https://doi.org/10.7717/peerj.2210 (2016). 10.7717/peerj.2210
[20]
Greicius, M. D., Krasnow, B., Reiss, A. L. & Menon, V. Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100, 253–258. https://doi.org/10.1073/pnas.0135058100 (2003). 10.1073/pnas.0135058100
[21]
Geerligs, L., Rubinov, M., Cam, C. & Henson, R. N. State and trait components of functional connectivity: individual differences vary with mental state. J. Neurosci. 35, 13949–13961. https://doi.org/10.1523/JNEUROSCI.1324-15.2015 (2015). 10.1523/jneurosci.1324-15.2015
[22]
Kaplan, S., Kaplan, R. & Wendt, J. S. Rated preference and complexity for natural and urban visual material. Percept. Psychophys. 12, 354–356. https://doi.org/10.3758/bf03207221 (1972). 10.3758/bf03207221
[23]
Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion

Jonathan D. Power, Kelly A. Barnes, Abraham Z. Snyder et al.

NeuroImage 2012 10.1016/j.neuroimage.2011.10.018
[24]
Seresinhe, C. I., Preis, T. & Moat, H. S. Using deep learning to quantify the beauty of outdoor places. R. Soc. Open Sci. 4, 170170. https://doi.org/10.1098/rsos.170170 (2017). 10.1098/rsos.170170
[25]
Forlim, C. G. et al. Stereoscopic rendering via goggles elicits higher functional connectivity during virtual reality gaming. Front. Hum. Neurosci. 13, 365. https://doi.org/10.3389/fnhum.2019.00365 (2019). 10.3389/fnhum.2019.00365
[26]
Reduced Resting-State Connectivity in the Precuneus is correlated with Apathy in Patients with Schizophrenia

Caroline Garcia Forlim, Leonie Klock, Johanna Bächle et al.

Scientific Reports 2020 10.1038/s41598-020-59393-6
[27]
Pedersen, C. B. & Mortensen, P. B. Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk. Arch. Gen. Psychiatry 58, 1039–1046 (2001). 10.1001/archpsyc.58.11.1039
[28]
A Global Measure of Perceived Stress

Sheldon Cohen, Tom Kamarck, Robin Mermelstein

Journal of Health and Social Behavior 1983 10.2307/2136404
[29]
Brose, A., Schmiedek, F., Lovden, M. & Lindenberger, U. Normal aging dampens the link between intrusive thoughts and negative affect in reaction to daily stressors. Psychol. Aging 26, 488–502. https://doi.org/10.1037/a0022287 (2011). 10.1037/a0022287
[30]
Kühn, S. et al. The neural representation of intrusive thoughts. Soc. Cognit. Affect. Neurosci. 8, 688–693 (2013). 10.1093/scan/nss047
[31]
Kuhn, S., Vanderhasselt, M. A., De Raedt, R. & Gallinat, J. The neural basis of unwanted thoughts during resting state. Soc. Cognit. Affect Neurosci. 9, 1320–1324. https://doi.org/10.1093/scan/nst117 (2014). 10.1093/scan/nst117
[32]
Lang, P. J. In Technology in Mental Health Care Delivery Systems (eds Sidowski, J. B. et al.) 119–137 (Ablex, Norwood, 1980).
[33]
Suk, H.-J. Color and Emotion: A Study on the Affective Judgment Across Media and in Relation to Visual Stimuli. Dissertation (2006).
[34]
Song, X. W. et al. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE 6, e25031. https://doi.org/10.1371/journal.pone.0025031 (2011). 10.1371/journal.pone.0025031
[35]
Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain

N. Tzourio-Mazoyer, B. Landeau, D. Papathanassiou et al.

NeuroImage 2002 10.1006/nimg.2001.0978
[36]
The organization of the human cerebral cortex estimated by intrinsic functional connectivity

B. T. Thomas Yeo, Fenna M. Krienen, Jorge Sepulcre et al.

Journal of Neurophysiology 2011 10.1152/jn.00338.2011
[37]
Complex network measures of brain connectivity: Uses and interpretations

Mikail Rubinov, Olaf Sporns

NeuroImage 2010 10.1016/j.neuroimage.2009.10.003
[38]
Complex brain networks: graph theoretical analysis of structural and functional systems

Edward Bullmore, Olaf Sporns

Nature Reviews Neuroscience 2009 10.1038/nrn2575
[39]
Network-based statistic: Identifying differences in brain networks

Andrew Zalesky, Alex Fornito, Edward T. Bullmore

NeuroImage 2010 10.1016/j.neuroimage.2010.06.041
[40]
BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics

Mingrui Xia, Jinhui Wang, Yong He

PLoS ONE 2013 10.1371/journal.pone.0068910
[41]
Meidenbauer, K. L. et al. The affective benefits of nature exposure: What’s nature got to do with it?. J. Environ. Psychol. 72, 101498. https://doi.org/10.1016/j.jenvp.2020.101498 (2020). 10.1016/j.jenvp.2020.101498
[42]
The human brain is intrinsically organized into dynamic, anticorrelated functional networks

Michael D. Fox, Abraham Z. Snyder, Justin L. Vincent et al.

Proceedings of the National Academy of Sciences 2005 10.1073/pnas.0504136102
[43]
Fransson, P. Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum. Brain Mapp. 26, 15–29. https://doi.org/10.1002/hbm.20113 (2005). 10.1002/hbm.20113
[44]
Dixon, M. L. et al. Interactions between the default network and dorsal attention network vary across default subsystems, time, and cognitive states. Neuroimage 147, 632–649. https://doi.org/10.1016/j.neuroimage.2016.12.073 (2017). 10.1016/j.neuroimage.2016.12.073
[45]
Craig, M. M., Manktelow, A. E., Sahakian, B. J., Menon, D. K. & Stamatakis, E. A. Spectral diversity in default mode network connectivity reflects behavioral state. J. Cognit. Neurosci. 30, 526–539. https://doi.org/10.1162/jocn_a_01213 (2018). 10.1162/jocn_a_01213
[46]
Varangis, E., Razlighi, Q., Habeck, C. G., Fisher, Z. & Stern, Y. Between-network functional connectivity is modified by age and cognitive task domain. J. Cognit. Neurosci. 31, 607–622. https://doi.org/10.1162/jocn_a_01368 (2019). 10.1162/jocn_a_01368
[47]
Kwon, S., Watanabe, M., Fischer, E. & Bartels, A. Attention reorganizes connectivity across networks in a frequency specific manner. Neuroimage 144, 217–226. https://doi.org/10.1016/j.neuroimage.2016.10.014 (2017). 10.1016/j.neuroimage.2016.10.014
[48]
Kelly, A. M., Uddin, L. Q., Biswal, B. B., Castellanos, F. X. & Milham, M. P. Competition between functional brain networks mediates behavioral variability. Neuroimage 39, 527–537. https://doi.org/10.1016/j.neuroimage.2007.08.008 (2008). 10.1016/j.neuroimage.2007.08.008
[49]
Peen, J. & Dekker, J. Is urbanicity an environmental risk-factor for psychiatric disorders?. Lancet 363, 2012–2013. https://doi.org/10.1016/S0140-6736(04)16486-6 (2004). 10.1016/s0140-6736(04)16486-6
[50]
Peen, J., Schoevers, R. A., Beekman, A. T. & Dekker, J. The current status of urban–rural differences in psychiatric disorders. Acta Psychiatr. Scand. 121, 84–93. https://doi.org/10.1111/j.1600-0447.2009.01438.x (2010). 10.1111/j.1600-0447.2009.01438.x

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Published
Feb 18, 2021
Vol/Issue
11(1)
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Funding
European Union Award: ERC-2016-StG-Self-Control-677804
Projekt DEAL
German Science Foundation Award: SFB 936/C7
Cite This Article
Simone Kühn, Caroline Garcia Forlim, Anja Lender, et al. (2021). Brain functional connectivity differs when viewing pictures from natural and built environments using fMRI resting state analysis. Scientific Reports, 11(1). https://doi.org/10.1038/s41598-021-83246-5