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Long ‐ term acclimatization to high ‐ altitude hypoxia modifies interhemispheric functional and structural connectivity in the adult brain

View Article: PubMed Central - PubMed

ABSTRACT

Background: Structural and functional networks can be reorganized to adjust to environmental pressures and physiologic changes in the adult brain, but such processes remain unclear in prolonged adaptation to high‐altitude (HA) hypoxia. This study aimed to characterize the interhemispheric functionally and structurally coupled modifications in the brains of adult HA immigrants.

Methods: We performed resting‐state functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI) in 16 adults who had immigrated to the Qinghai‐Tibet Plateau (2300–4400 m) for 2 years and in 16 age‐matched sea‐level (SL) controls. A recently validated approach of voxel‐mirrored homotopic connectivity (VMHC) was employed to examine the interhemispheric resting‐state functional connectivity. Areas showing changed VMHC in HA immigrants were selected as regions of interest for follow‐up DTI tractography analysis. The fiber parameters of fractional anisotropy and fiber length were obtained. Cognitive and physiological assessments were made and correlated with the resulting image metrics.

Results: Compared with SL controls, VMHC in the bilateral visual cortex was significantly increased in HA immigrants. The mean VMHC value extracted within the visual cortex was positively correlated with hemoglobin concentration. Moreover, the path length of the commissural fibers connecting homotopic visual areas was increased in HA immigrants, covarying positively with VMHC.

Conclusions: These observations are the first to demonstrate interhemispheric functional and structural connectivity resilience in the adult brain after prolonged HA acclimatization independent of inherited and developmental effects, and the coupled modifications in the bilateral visual cortex indicate important neural compensatory mechanisms underlying visual dysfunction in physiologically well‐acclimatized HA immigrants. The study of human central adaptation to extreme environments promotes the understanding of our brain's capacity for survival.

No MeSH data available.


Related in: MedlinePlus

Between group comparison for VMHC. (A) Seven symmetric axial slices show group differences in homotopic voxel‐mirrored connectivity (VMHC). The visual area for which the HA group exhibited significantly stronger VMHC than the control group (Z > 2.57, cluster level P < 0.05, corrected). (B) For a more accurate spatial localization, population‐based probabilistic maps of the significantly increased VMHC regions (visual cortex) were projected onto the FreeSurfer‐derived sphere surface. The outlines were labels according to Brodmann area (BA) 17, 18, and 19. (C). Scatterplots show the between‐group differences in VMHC in the bilateral visual cortex. (D) Correlation between the mean z‐VMHC index and the hemoglobin concentration in both SL controls and HA adults (P < 0.05, Bonferroni corrected). RH, right hemisphere; cs, calcarine sulcus; pos, parietooccipital sulcus; ls, lingual sulcus.
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brb3512-fig-0001: Between group comparison for VMHC. (A) Seven symmetric axial slices show group differences in homotopic voxel‐mirrored connectivity (VMHC). The visual area for which the HA group exhibited significantly stronger VMHC than the control group (Z > 2.57, cluster level P < 0.05, corrected). (B) For a more accurate spatial localization, population‐based probabilistic maps of the significantly increased VMHC regions (visual cortex) were projected onto the FreeSurfer‐derived sphere surface. The outlines were labels according to Brodmann area (BA) 17, 18, and 19. (C). Scatterplots show the between‐group differences in VMHC in the bilateral visual cortex. (D) Correlation between the mean z‐VMHC index and the hemoglobin concentration in both SL controls and HA adults (P < 0.05, Bonferroni corrected). RH, right hemisphere; cs, calcarine sulcus; pos, parietooccipital sulcus; ls, lingual sulcus.

Mentions: One subject in the control group was excluded for further analysis because of excessive head movement (>2 mm translation). SL controls and HA immigrants differed on global mean VMHC. Specifically, global VMHC was significantly increased in the HA group (HA immigrations = 0.45 ± 0.03; SL controls = 0.40 ± 0.06; t = 2.740, P = 0.01). Compared to SL controls, regional differences in VMHC were detected in the bilateral visual cortex with an increase in HA immigrants (P < 0.05, corrected) (Fig. 1; Table 3) controlling for age and years of education. No significant differences were detected in the SL controls >HA immigrants contrast after correction for multiple comparisons. According to Figure 1B, the significant clusters of the visual cortex for each subject were mainly located in the calcarine, parietooccipital, and lingual sulci. The results did not change after controlling for the hematocrit level or voxel gray matter volume in the statistical analysis.


Long ‐ term acclimatization to high ‐ altitude hypoxia modifies interhemispheric functional and structural connectivity in the adult brain
Between group comparison for VMHC. (A) Seven symmetric axial slices show group differences in homotopic voxel‐mirrored connectivity (VMHC). The visual area for which the HA group exhibited significantly stronger VMHC than the control group (Z > 2.57, cluster level P < 0.05, corrected). (B) For a more accurate spatial localization, population‐based probabilistic maps of the significantly increased VMHC regions (visual cortex) were projected onto the FreeSurfer‐derived sphere surface. The outlines were labels according to Brodmann area (BA) 17, 18, and 19. (C). Scatterplots show the between‐group differences in VMHC in the bilateral visual cortex. (D) Correlation between the mean z‐VMHC index and the hemoglobin concentration in both SL controls and HA adults (P < 0.05, Bonferroni corrected). RH, right hemisphere; cs, calcarine sulcus; pos, parietooccipital sulcus; ls, lingual sulcus.
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brb3512-fig-0001: Between group comparison for VMHC. (A) Seven symmetric axial slices show group differences in homotopic voxel‐mirrored connectivity (VMHC). The visual area for which the HA group exhibited significantly stronger VMHC than the control group (Z > 2.57, cluster level P < 0.05, corrected). (B) For a more accurate spatial localization, population‐based probabilistic maps of the significantly increased VMHC regions (visual cortex) were projected onto the FreeSurfer‐derived sphere surface. The outlines were labels according to Brodmann area (BA) 17, 18, and 19. (C). Scatterplots show the between‐group differences in VMHC in the bilateral visual cortex. (D) Correlation between the mean z‐VMHC index and the hemoglobin concentration in both SL controls and HA adults (P < 0.05, Bonferroni corrected). RH, right hemisphere; cs, calcarine sulcus; pos, parietooccipital sulcus; ls, lingual sulcus.
Mentions: One subject in the control group was excluded for further analysis because of excessive head movement (>2 mm translation). SL controls and HA immigrants differed on global mean VMHC. Specifically, global VMHC was significantly increased in the HA group (HA immigrations = 0.45 ± 0.03; SL controls = 0.40 ± 0.06; t = 2.740, P = 0.01). Compared to SL controls, regional differences in VMHC were detected in the bilateral visual cortex with an increase in HA immigrants (P < 0.05, corrected) (Fig. 1; Table 3) controlling for age and years of education. No significant differences were detected in the SL controls >HA immigrants contrast after correction for multiple comparisons. According to Figure 1B, the significant clusters of the visual cortex for each subject were mainly located in the calcarine, parietooccipital, and lingual sulci. The results did not change after controlling for the hematocrit level or voxel gray matter volume in the statistical analysis.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Structural and functional networks can be reorganized to adjust to environmental pressures and physiologic changes in the adult brain, but such processes remain unclear in prolonged adaptation to high&#8208;altitude (HA) hypoxia. This study aimed to characterize the interhemispheric functionally and structurally coupled modifications in the brains of adult HA immigrants.

Methods: We performed resting&#8208;state functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI) in 16 adults who had immigrated to the Qinghai&#8208;Tibet Plateau (2300&ndash;4400&nbsp;m) for 2&nbsp;years and in 16 age&#8208;matched sea&#8208;level (SL) controls. A recently validated approach of voxel&#8208;mirrored homotopic connectivity (VMHC) was employed to examine the interhemispheric resting&#8208;state functional connectivity. Areas showing changed VMHC in HA immigrants were selected as regions of interest for follow&#8208;up DTI tractography analysis. The fiber parameters of fractional anisotropy and fiber length were obtained. Cognitive and physiological assessments were made and correlated with the resulting image metrics.

Results: Compared with SL controls, VMHC in the bilateral visual cortex was significantly increased in HA immigrants. The mean VMHC value extracted within the visual cortex was positively correlated with hemoglobin concentration. Moreover, the path length of the commissural fibers connecting homotopic visual areas was increased in HA immigrants, covarying positively with VMHC.

Conclusions: These observations are the first to demonstrate interhemispheric functional and structural connectivity resilience in the adult brain after prolonged HA acclimatization independent of inherited and developmental effects, and the coupled modifications in the bilateral visual cortex indicate important neural compensatory mechanisms underlying visual dysfunction in physiologically well&#8208;acclimatized HA immigrants. The study of human central adaptation to extreme environments promotes the understanding of our brain's capacity for survival.

No MeSH data available.


Related in: MedlinePlus