TY - JOUR
T1 - Severe hyposmia and aberrant functional connectivity in cognitively normal Parkinson’s disease
AU - Yoneyama, Noritaka
AU - Watanabe, Hirohisa
AU - Kawabata, Kazuya
AU - Bagarinao, Epifanio
AU - Hara, Kazuhiro
AU - Tsuboi, Takashi
AU - Tanaka, Yasuhiro
AU - Ohdake, Reiko
AU - Imai, Kazunori
AU - Masuda, Michihito
AU - Hattori, Tatsuya
AU - Ito, Mizuki
AU - Atsuta, Naoki
AU - Nakamura, Tomohiko
AU - Hirayama, Masaaki
AU - Maesawa, Satoshi
AU - Katsuno, Masahisa
AU - Sobue, Gen
N1 - Funding Information:
This research was supported in part by the following: a Grant-in-Aid from the Research Committee of Central Nervous System Degenerative Diseases by the Ministry of Health, Labour, and Welfare, Integrated Research on Neuropsychiatric Disorders project, carried out by SRBPS; a Grant-in-Aid for Scientific Research on Innovative Areas (Brain Protein Aging and Dementia Control 26117002) from the MEXT of Japan; Integrated Research on Neuropsychiatric Disorders carried out under the Strategic Research Program for Brain Sciences, Scientific Research on Innovative Areas (Comprehensive Brain Science Network); and Integrated Research on Depression, Dementia, and Development Disorders by the Strategic Research Program for Brain Sciences from the Japan Agency for Medical Research and Development (AMED).
Publisher Copyright:
© 2018 Yoneyama et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2018/1
Y1 - 2018/1
N2 - Objective Severe hyposmia is a risk factor of dementia in Parkinson’s disease (PD), while the underlying functional connectivity (FC) and brain volume alterations in PD patients with severe hyposmia (PD-SH) are unclear. Methods We examined voxel-based morphometric and resting state functional magnetic resonance imaging findings in 15 cognitively normal PD-SH, 15 cognitively normal patients with PD with no/mild hyposmia (PD-N/MH), and 15 healthy controls (HCs). Results Decreased gray matter volume (GMV) was observed in the bilateral cuneus, right associative visual area, precuneus, and some areas in anterior temporal lobes in PD-SH group compared to HCs. Both the PD-SH and PD-N/MH groups showed increased GMV in the bilateral posterior insula and its surrounding regions. A widespread significant decrease in amygdala FC beyond the decreased GMV areas and olfactory cortices were found in the PD-SH group compared with the HCs. Above all, decreased amygdala FC with the inferior parietal lobule, lingual gyrus, and fusiform gyrus was significantly correlated with both reduction of Addenbrooke’s Cognitive Examination-Revised scores and severity of hyposmia in all participants. Canonical resting state networks exhibited decreased FC in the precuneus and left executive control networks but increased FC in the primary and high visual networks of patients with PD compared with HCs. Canonical network FC to other brain regions was enhanced in the executive control, salience, primary visual, and visuospatial networks of the PD-SH. Conclusion PD-SH showed extensive decreased amygdala FC. Particularly, decreased FC between the amygdala and inferior parietal lobule, lingual gyrus, and fusiform gyrus were associated with the severity of hyposmia and cognitive performance. In contrast, relatively preserved canonical networks in combination with increased FC to brain regions outside of canonical networks may be related to compensatory mechanisms, and preservation of brain function.
AB - Objective Severe hyposmia is a risk factor of dementia in Parkinson’s disease (PD), while the underlying functional connectivity (FC) and brain volume alterations in PD patients with severe hyposmia (PD-SH) are unclear. Methods We examined voxel-based morphometric and resting state functional magnetic resonance imaging findings in 15 cognitively normal PD-SH, 15 cognitively normal patients with PD with no/mild hyposmia (PD-N/MH), and 15 healthy controls (HCs). Results Decreased gray matter volume (GMV) was observed in the bilateral cuneus, right associative visual area, precuneus, and some areas in anterior temporal lobes in PD-SH group compared to HCs. Both the PD-SH and PD-N/MH groups showed increased GMV in the bilateral posterior insula and its surrounding regions. A widespread significant decrease in amygdala FC beyond the decreased GMV areas and olfactory cortices were found in the PD-SH group compared with the HCs. Above all, decreased amygdala FC with the inferior parietal lobule, lingual gyrus, and fusiform gyrus was significantly correlated with both reduction of Addenbrooke’s Cognitive Examination-Revised scores and severity of hyposmia in all participants. Canonical resting state networks exhibited decreased FC in the precuneus and left executive control networks but increased FC in the primary and high visual networks of patients with PD compared with HCs. Canonical network FC to other brain regions was enhanced in the executive control, salience, primary visual, and visuospatial networks of the PD-SH. Conclusion PD-SH showed extensive decreased amygdala FC. Particularly, decreased FC between the amygdala and inferior parietal lobule, lingual gyrus, and fusiform gyrus were associated with the severity of hyposmia and cognitive performance. In contrast, relatively preserved canonical networks in combination with increased FC to brain regions outside of canonical networks may be related to compensatory mechanisms, and preservation of brain function.
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U2 - 10.1371/journal.pone.0190072
DO - 10.1371/journal.pone.0190072
M3 - Article
C2 - 29304050
AN - SCOPUS:85040120803
SN - 1932-6203
VL - 13
JO - PLoS One
JF - PLoS One
IS - 1
M1 - e0190072
ER -