Evaluation of the Alterations in Central Cholinergic Neurotransmission in Aging and Amyloid Precursor Protein Knock-In Mice

J Neurochem. 2025 May;169(5):e70081. doi: 10.1111/jnc.70081.

Abstract

A progressive decline in cognitive function occurs as a result of aging and Alzheimer's disease (AD) and is primarily associated with diminished cholinergic neurotransmission. However, the precise mechanisms contributing to cholinergic dysfunction are not fully elucidated. Herein, we evaluated the cholinergic system in wild type (WT) mice and AD-model (AppNL-G-F) mice exhibiting overproduction of amyloid-beta 42 (Aβ42). In superfusion experiments, [3H]acetylcholine (ACh) release from the frontal cortex and hippocampal segments preloaded with [3H]choline exhibited no significant differences between adult (6-8 months old) and aged (12-17 months old) WT mice. Uptake of [3H]choline via the high-affinity choline transporter 1 (CHT1) and the subsequent formation/storage of [3H]ACh showed a moderate tendency to decrease associated with aging. In contrast, in AppNL-G-F mice, [3H]ACh release was significantly reduced in both the adult and aged groups, with reductions closely related to impaired CHT1 activity and diminished ACh synthesis/storage at cholinergic terminals. Presynaptic cholinergic feedback mechanisms regulating ACh release, as well as the density and subtype distribution of muscarinic ACh receptors, were minimally affected by both aging and Aβ42 overproduction. These results support the Aβ hypothesis, suggesting that presynaptic cholinergic dysfunction arises early and is specifically caused by decreased CHT1 function in the AD forebrain, independent of age-dependent degeneration.

Keywords: Alzheimer's disease; acetylcholine; aging; cholinergic.

MeSH terms

  • Acetylcholine* / metabolism
  • Aging* / genetics
  • Aging* / metabolism
  • Alzheimer Disease / genetics
  • Alzheimer Disease / metabolism
  • Amyloid beta-Peptides / metabolism
  • Amyloid beta-Protein Precursor* / genetics
  • Animals
  • Choline / metabolism
  • Cholinergic Neurons*
  • Gene Knock-In Techniques
  • Hippocampus / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Symporters / metabolism
  • Synaptic Transmission* / physiology

Substances

  • Amyloid beta-Protein Precursor
  • Acetylcholine
  • Amyloid beta-Peptides
  • Choline
  • Symporters