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Cholinergic basal forebrain and hippocampal structure influence visuospatial memory in Parkinson’s disease

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Abstract

Visuospatial impairment in Parkinson’s disease (PD) heralds the onset of a progressive dementia syndrome and might be associated with cholinergic dysfunction. It remains unclear however, whether degeneration of the cholinergic basal forebrain is directly related to cognitive decline, or whether relationships between this region and cognitive function are mediated by closely related brain structures such as those in the medial temporal lobe. To evaluate relationships between structure of the cholinergic basal forebrain, medial temporal lobe and cognition, 27 PD patients without dementia and 20 controls underwent neuropsychological assessment and MRI. Volumes of the cholinergic basal forebrain nuclei, the entorhinal cortex, the hippocampus and its subfields were measured. Regression models utilised basal forebrain and hippocampal volumetric measures to predict cognitive performance. In PD, visuospatial memory (but not verbal memory or executive function) was correlated with hippocampal volume, particularly CA2-3, and basal forebrain subregion Ch1-2, but not Ch4. In addition, hippocampal volume was correlated with Ch1-2 in PD. The relationship between Ch1-2 and visuospatial memory was mediated by CA2-3 integrity. There were no correlations between cognitive and volumetric measures in controls. Our data imply that the integrity of the cholinergic basal forebrain is associated with subregional hippocampal volume. Additionally, a relationship between visuospatial function and cholinergic nuclei does exist, but is fully mediated by variations in hippocampal structure. These findings are consistent with the recent hypothesis that forebrain cholinergic system degeneration results in cognitive deficits via cholinergic denervation, and subsequent structural degeneration, of its target regions.

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Funding

This work was supported by the Slovenian Research Agency (principal investigator ZP, Research Grant No. L3-4255). MJG is supported by the "Miguel Servet" program [CP19/00031] of the Spanish Instituto de Salud Carlos III (ISCIIIFEDER). NJR received funding from the Wellcome Trust and the Eleanor Countess Peel Trust.

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Correspondence to Rok Berlot.

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The authors declare that they have no conflicts of interest with respect to the research, authorship and/or publication of this article.

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Ethical approval for the study was provided by the Republic of Slovenia National Medical Ethics Committee.

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All participants provided informed written consent in accordance with the Declaration of Helsinki.

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Berlot, R., Pirtošek, Z., Brezovar, S. et al. Cholinergic basal forebrain and hippocampal structure influence visuospatial memory in Parkinson’s disease. Brain Imaging and Behavior 16, 118–129 (2022). https://doi.org/10.1007/s11682-021-00481-0

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  • DOI: https://doi.org/10.1007/s11682-021-00481-0

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