Cooperativity, information gain, and energy cost during early LTP in dendritic spines

Fuente: arXiv
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Auteurs principaux: Karbowski, Jan, Urban, Paulina
Format: Preprint
Publié: 2024
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author Karbowski, Jan
Urban, Paulina
author_facet Karbowski, Jan
Urban, Paulina
contents We investigate a mutual relationship between information and energy during early phase of LTP induction and maintenance in a large-scale system of mutually coupled dendritic spines, with discrete internal states and probabilistic dynamics, within the framework of nonequilibrium stochastic thermodynamics. In order to analyze this computationally intractable stochastic multidimensional system, we introduce a pair approximation, which allows us to reduce the spine dynamics into a lower dimensional manageable system of closed equations. It is found that the rates of information gain and energy attain their maximal values during an initial period of LTP (i.e. during stimulation), and after that they recover to their baseline low values, as opposed to a memory trace that lasts much longer. This suggests that learning phase is much more energy demanding than the memory phase. We show that positive correlations between neighboring spines increase both a duration of memory trace and energy cost during LTP, but the memory time per invested energy increases dramatically for very strong positive synaptic cooperativity, suggesting a beneficial role of synaptic clustering on memory duration. In contrast, information gain after LTP is the largest for negative correlations, and energy efficiency of that information generally declines with increasing synaptic cooperativity. We also find that dendritic spines can use sparse representations for encoding of long-term information, as both energetic and structural efficiencies of retained information and its lifetime exhibit maxima for low fractions of stimulated synapses during LTP. In general, our stochastic thermodynamics approach provides a unifying framework for studying, from first principles, information encoding and its energy cost during learning and memory in stochastic systems of interacting synapses.
format Preprint
id arxiv_https___arxiv_org_abs_2404_14123
institution arXiv
publishDate 2024
record_format arxiv
spellingShingle Cooperativity, information gain, and energy cost during early LTP in dendritic spines
Karbowski, Jan
Urban, Paulina
Neurons and Cognition
Disordered Systems and Neural Networks
Statistical Mechanics
Computational Physics
Quantitative Methods
We investigate a mutual relationship between information and energy during early phase of LTP induction and maintenance in a large-scale system of mutually coupled dendritic spines, with discrete internal states and probabilistic dynamics, within the framework of nonequilibrium stochastic thermodynamics. In order to analyze this computationally intractable stochastic multidimensional system, we introduce a pair approximation, which allows us to reduce the spine dynamics into a lower dimensional manageable system of closed equations. It is found that the rates of information gain and energy attain their maximal values during an initial period of LTP (i.e. during stimulation), and after that they recover to their baseline low values, as opposed to a memory trace that lasts much longer. This suggests that learning phase is much more energy demanding than the memory phase. We show that positive correlations between neighboring spines increase both a duration of memory trace and energy cost during LTP, but the memory time per invested energy increases dramatically for very strong positive synaptic cooperativity, suggesting a beneficial role of synaptic clustering on memory duration. In contrast, information gain after LTP is the largest for negative correlations, and energy efficiency of that information generally declines with increasing synaptic cooperativity. We also find that dendritic spines can use sparse representations for encoding of long-term information, as both energetic and structural efficiencies of retained information and its lifetime exhibit maxima for low fractions of stimulated synapses during LTP. In general, our stochastic thermodynamics approach provides a unifying framework for studying, from first principles, information encoding and its energy cost during learning and memory in stochastic systems of interacting synapses.
title Cooperativity, information gain, and energy cost during early LTP in dendritic spines
topic Neurons and Cognition
Disordered Systems and Neural Networks
Statistical Mechanics
Computational Physics
Quantitative Methods
url https://arxiv.org/abs/2404.14123