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. 2018 Feb 23;126(2):027012.
doi: 10.1289/EHP1876.

The Association between Lifelong Greenspace Exposure and 3-Dimensional Brain Magnetic Resonance Imaging in Barcelona Schoolchildren

Payam Dadvand  1   2   3 , Jesus Pujol  4   5 , Dídac Macià  4 , Gerard Martínez-Vilavella  4 , Laura Blanco-Hinojo  4   5 , Marion Mortamais  1   2   3 , Mar Alvarez-Pedrerol  1   2   3 , Raquel Fenoll  4 , Mikel Esnaola  1   2   3 , Albert Dalmau-Bueno  1   2   3 , Mónica López-Vicente  1   2   3 , Xavier Basagaña  1   2   3 , Michael Jerrett  6 , Mark J Nieuwenhuijsen  1   2   3 , Jordi Sunyer  1   2   3   7
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The Association between Lifelong Greenspace Exposure and 3-Dimensional Brain Magnetic Resonance Imaging in Barcelona Schoolchildren

Payam Dadvand et al. Environ Health Perspect. .

Abstract

Background: Proponents of the biophilia hypothesis believe that contact with nature, including green spaces, has a crucial role in brain development in children. Currently, however, we are not aware of evidence linking such exposure with potential effects on brain structure.

Objective: We determined whether lifelong exposure to residential surrounding greenness is associated with regional differences in brain volume based on 3-dimensional magnetic resonance imaging (3D MRI) among children attending primary school.

Methods: We performed a series of analyses using data from a subcohort of 253 Barcelona schoolchildren from the Brain Development and Air Pollution Ultrafine Particles in School Children (BREATHE) project. We averaged satellite-based normalized difference vegetation index (NDVI) across 100-m buffers around all residential addresses since birth to estimate each participant's lifelong exposure to residential surrounding greenness, and we used high-resolution 3D MRIs of brain anatomy to identify regional differences in voxel-wise brain volume associated with greenness exposure. In addition, we performed a supporting substudy to identify regional differences in brain volume associated with measures of working memory (d' from computerized n-back tests) and inattentiveness (hit reaction time standard error from the Attentional Network Task instrument) that were repeated four times over one year. We also performed a second supporting substudy to determine whether peak voxel tissue volumes in brain regions associated with residential greenness predicted cognitive function test scores.

Results: Lifelong exposure to greenness was positively associated with gray matter volume in the left and right prefrontal cortex and in the left premotor cortex and with white matter volume in the right prefrontal region, in the left premotor region, and in both cerebellar hemispheres. Some of these regions partly overlapped with regions associated with cognitive test scores (prefrontal cortex and cerebellar and premotor white matter), and peak volumes in these regions predicted better working memory and reduced inattentiveness.

Conclusion: Our findings from a study population of urban schoolchildren in Barcelona require confirmation, but they suggest that being raised in greener neighborhoods may have beneficial effects on brain development and cognitive function. https://doi.org/10.1289/EHP1876.

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Figures

Figure 1A is a 3D rendering of gray matter clusters in the right and left prefrontal and left promotor cortices associated with lifelong greenness exposure. Figure 1B is an orthogonal display of the brain including white matter clusters in cerebellum and left premotor regions associated with lifelong greenness exposure.
Figure 1.
Regional gray and white matter volumes associated with lifelong residential surrounding greenness. Results are displayed using conventional canonical templates [Cortex_20484 surface mesh in (A) and MNI152_T1 template in (B)] in Montreal Neurological Institute (MNI) space with statistical parametric mapping (SPM8; FIL Methods Group 2013) software. Yellow and white areas indicate regional clusters with volumes positively associated with greenness (larger t-statistics). (A) Three-dimensional (3D) renderings of cortical gray matter (Cortex_20484 render) showing significant clusters in the right and left prefrontal cortex (left and right panels, respectively) and in the left premotor cortex (right panel). Results were considered significant with clusters of 2.2mL (650 voxels) at a height threshold of p<0.01, which satisfied the family-wise error (FWE) rate correction of pFWE<0.05. (B) Orthogonal displays (sagittal, coronal, and axial views in the left, middle, and right panels, respectively, MNI152_T1 template) showing significant white matter clusters in the cerebellar hemispheres (all panels) and in the left premotor region (sagittal view). The right hemisphere appears on the right side of the axial and coronal views. Clusters with inverse associations between volumes and greenness would appear in cold colors (none identified.) See Table 2 for numeric data for each significant region. Residential greenness exposure was quantified based on the average Normalized Difference Vegetation Index (NDVI) within a 100-m buffer around all residences since birth, weighted by the time the participant spent at each address.
Figures 2A, 2C, and 2E are 3D renderings of right and left prefrontal cortex including clusters associated with lifelong greenness exposure as well as performance in cognitive tests. Figures 2B, 2D, and 2F are orthogonal displays of the brain including clusters associated with lifelong greenness exposure as well as performance in cognitive tests.
Figure 2.
Regional gray and white matter volumes associated with lifelong residential surrounding greenness and cognitive performance. Results are displayed using conventional canonical templates [Cortex_20484 surface mesh in (A), (C), and (E) and MNI152_T1 template in (B), (D), and (F)] in Montreal Neurological Institute (MNI) space with statistical parametric mapping (SPM8; FIL Methods Group 2013) software. Green areas indicate regional volumes significantly associated with greenness (see Figure 1). Results were considered significant with clusters of 2.2mL (650 voxels) at a height threshold of p<0.01, which satisfied the family-wise error (FWE) rate correction of pFWE<0.05. Red areas indicate regional clusters with volumes significantly associated with cognitive functions: hit reaction time standard error (HRT-SE; an indicator of inattentiveness) in (A) and (B); 2-back d′ (an indicator of working memory) in (C) and (D), and 3-back d′ (an indicator of superior working memory) in (E) and (F). The overlaps between regions associated with greenness and those associated with cognitive functions are shown in yellow. Voxels with significant results were binarized to the corresponding single color. (A) Three-dimensional (3D) renderings of cortical gray matter showing clusters negatively associated with HRT-SE in the right and left cortex (left and right panels, respectively). (B) Orthogonal displays (sagittal, coronal, and axial views in the left, middle, and right panels, respectively) showing white matter clusters negatively associated with HRT-SE. (C) 3D renderings of cortical gray matter showing clusters positively associated with 2-back. (D) Orthogonal displays showing white matter clusters positively associated with 2-back. (E) 3D renderings of cortical gray matter showing clusters positively associated with 3-back. (F) Orthogonal displays showing white matter clusters positively associated with 3-back. The right hemisphere appears on the right side of the axial and coronal views. See Table S3 for numeric data for each significant region. Residential greenness exposure was quantified based the average Normalized Difference Vegetation Index (NDVI) within a 100-m buffer around all residences since birth, weighted by the time the participant spent at each address. Bs, brainstem; Cer, cerebellum; Hp, hipoccampus; IPc, inferior parietal cortex; Op, operculum; PFc, prefrontal cortex; PM, premotor cortex; SM, sensorimotor cortex; Tc, temporal cortex; TOc, temporo-occipital cortex.
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