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@ARTICLE{Mittag:256459,
author = {Mittag, Martin and Mediavilla, Laura and Remy, Stefan and
Cuntz, Hermann and Jedlicka, Peter},
title = {{M}odelling the contributions to hyperexcitability in a
mouse model of {A}lzheimer's disease.},
journal = {The journal of physiology},
volume = {601},
number = {15},
issn = {0022-3751},
address = {Hoboken, NJ},
publisher = {Wiley-Blackwell},
reportid = {DZNE-2023-00321},
pages = {3403-3437},
year = {2023},
note = {CC BY},
abstract = {Neuronal hyperexcitability is a pathological characteristic
of Alzheimer's disease (AD). Three main mechanisms have been
proposed to explain it: (i) dendritic degeneration leading
to increased input resistance, (ii) ion channel changes
leading to enhanced intrinsic excitability, and (iii)
synaptic changes leading to excitation-inhibition (E/I)
imbalance. However, the relative contribution of these
mechanisms is not fully understood. Therefore, we performed
biophysically realistic multi-compartmental modelling of
neuronal excitability in reconstructed CA1 pyramidal neurons
from wild-type and APP/PS1 mice, a well-established animal
model of AD. We show that, for synaptic activation, the
excitability-promoting effects of dendritic degeneration are
cancelled out by decreased excitation due to synaptic loss.
We find an interesting balance between excitability
regulation and an enhanced degeneration in the basal
dendrites of APP/PS1 cells, potentially leading to increased
excitation by the apical but decreased excitation by the
basal Schaffer collateral pathway. Furthermore, our
simulations reveal three pathomechanistic scenarios that can
account for the experimentally observed increase in firing
and bursting of CA1 pyramidal neurons in APP/PS1 mice:
scenario 1: enhanced E/I ratio; scenario 2: alteration of
intrinsic ion channels (IAHP down-regulated; INap , INa and
ICaT up-regulated) in addition to enhanced E/I ratio; and
scenario 3: increased excitatory burst input. Our work
supports the hypothesis that pathological network and ion
channel changes are major contributors to neuronal
hyperexcitability in AD. Overall, our results are in line
with the concept of multi-causality according to which
multiple different disruptions are separately sufficient but
no single particular disruption is necessary for neuronal
hyperexcitability. KEY POINTS: This work presents
simulations of synaptically driven responses in pyramidal
cells (PCs) with Alzheimer's disease (AD)-related dendritic
degeneration. Dendritic degeneration alone alters PC
responses to layer-specific input but additional
pathomechanistic scenarios are required to explain neuronal
hyperexcitability in AD as follows. Possible scenario 1:
AD-related increased excitatory input together with
decreased inhibitory input (E/I imbalance) can lead to
hyperexcitability in PCs. Possible scenario 2: changes in
E/I balance combined with altered ion channel properties can
account for hyperexcitability in AD. Possible scenario 3:
burst hyperactivity of the surrounding network can explain
hyperexcitability of PCs during AD.},
keywords = {Mice / Animals / Alzheimer Disease / Hippocampus:
physiology / Neurons: physiology / Pyramidal Cells:
physiology / Ion Channels: metabolism / Disease Models,
Animal / Ion Channels (NLM Chemicals) / degeneracy (Other) /
dendritic constancy (Other) / hippocampus (Other) /
morphological modelling (Other) / multi-causal pathogenesis
(Other)},
cin = {AG Remy},
ddc = {610},
cid = {I:(DE-2719)1013006},
pnm = {351 - Brain Function (POF4-351)},
pid = {G:(DE-HGF)POF4-351},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:36734280},
doi = {10.1113/JP283401},
url = {https://pub.dzne.de/record/256459},
}