Optimal information gain at the onset of habituation to repeated stimuli

Biological and living systems process information across spatiotemporal scales, exhibiting the hallmark ability to constantly modulate their behavior to ever-changing and complex environments. In the presence of repeated stimuli, a distinctive response is the progressive reduction of the activity at...

Full description

Saved in:
Bibliographic Details
Main Authors: Giorgio Nicoletti, Matteo Bruzzone, Samir Suweis, Marco dal Maschio, Daniel Maria Busiello
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/99767
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850078801527046144
author Giorgio Nicoletti
Matteo Bruzzone
Samir Suweis
Marco dal Maschio
Daniel Maria Busiello
author_facet Giorgio Nicoletti
Matteo Bruzzone
Samir Suweis
Marco dal Maschio
Daniel Maria Busiello
author_sort Giorgio Nicoletti
collection DOAJ
description Biological and living systems process information across spatiotemporal scales, exhibiting the hallmark ability to constantly modulate their behavior to ever-changing and complex environments. In the presence of repeated stimuli, a distinctive response is the progressive reduction of the activity at both sensory and molecular levels, known as habituation. In this work, we solve a minimal microscopic model devoid of biological details, where habituation to an external signal is driven by negative feedback provided by a slow storage mechanism. We show that our model recapitulates the main features of habituation, such as spontaneous recovery, potentiation, subliminal accumulation, and input sensitivity. Crucially, our approach enables a complete characterization of the stochastic dynamics, allowing us to compute how much information the system encodes on the input signal. We find that an intermediate level of habituation is associated with a steep increase in information. In particular, we are able to characterize this region of maximal information gain in terms of an optimal trade-off between information and energy consumption. We test our dynamical predictions against experimentally recorded neural responses in a zebrafish larva subjected to repeated looming stimulations, showing that our model captures the main components of the observed neural habituation. Our work makes a fundamental step towards uncovering the functional mechanisms that shape habituation in biological systems from an information-theoretic and thermodynamic perspective.
format Article
id doaj-art-4d4111fe588e4c708f683fadcb6977d8
institution DOAJ
issn 2050-084X
language English
publishDate 2025-07-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-4d4111fe588e4c708f683fadcb6977d82025-08-20T02:45:28ZengeLife Sciences Publications LtdeLife2050-084X2025-07-011310.7554/eLife.99767Optimal information gain at the onset of habituation to repeated stimuliGiorgio Nicoletti0https://orcid.org/0000-0002-7682-0596Matteo Bruzzone1https://orcid.org/0000-0001-7683-8107Samir Suweis2https://orcid.org/0000-0002-1603-8375Marco dal Maschio3https://orcid.org/0000-0003-0150-6647Daniel Maria Busiello4https://orcid.org/0000-0002-6754-5019ECHO Laboratory, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; Quantitative Life Sciences section, The Abdus Salam International Center for Theoretical Physics (ICTP), Trieste, Italy; Department of Physics and Astronomy “Galileo Galilei”, University of Padova, Padova, ItalyDepartment of Biomedical Science, University of Padova, Padova, Italy; Padova Neuroscience Center, University of Padova, Padova, Italy; Department of Biology, University of Fribourg, Fribourg, SwitzerlandDepartment of Physics and Astronomy “Galileo Galilei”, University of Padova, Padova, Italy; Padova Neuroscience Center, University of Padova, Padova, ItalyDepartment of Biomedical Science, University of Padova, Padova, Italy; Padova Neuroscience Center, University of Padova, Padova, ItalyDepartment of Physics and Astronomy “Galileo Galilei”, University of Padova, Padova, Italy; Max Planck Institute for the Physics of Complex Systems, Dresden, GermanyBiological and living systems process information across spatiotemporal scales, exhibiting the hallmark ability to constantly modulate their behavior to ever-changing and complex environments. In the presence of repeated stimuli, a distinctive response is the progressive reduction of the activity at both sensory and molecular levels, known as habituation. In this work, we solve a minimal microscopic model devoid of biological details, where habituation to an external signal is driven by negative feedback provided by a slow storage mechanism. We show that our model recapitulates the main features of habituation, such as spontaneous recovery, potentiation, subliminal accumulation, and input sensitivity. Crucially, our approach enables a complete characterization of the stochastic dynamics, allowing us to compute how much information the system encodes on the input signal. We find that an intermediate level of habituation is associated with a steep increase in information. In particular, we are able to characterize this region of maximal information gain in terms of an optimal trade-off between information and energy consumption. We test our dynamical predictions against experimentally recorded neural responses in a zebrafish larva subjected to repeated looming stimulations, showing that our model captures the main components of the observed neural habituation. Our work makes a fundamental step towards uncovering the functional mechanisms that shape habituation in biological systems from an information-theoretic and thermodynamic perspective.https://elifesciences.org/articles/99767habituationinformation theorynonequilibrium systems
spellingShingle Giorgio Nicoletti
Matteo Bruzzone
Samir Suweis
Marco dal Maschio
Daniel Maria Busiello
Optimal information gain at the onset of habituation to repeated stimuli
eLife
habituation
information theory
nonequilibrium systems
title Optimal information gain at the onset of habituation to repeated stimuli
title_full Optimal information gain at the onset of habituation to repeated stimuli
title_fullStr Optimal information gain at the onset of habituation to repeated stimuli
title_full_unstemmed Optimal information gain at the onset of habituation to repeated stimuli
title_short Optimal information gain at the onset of habituation to repeated stimuli
title_sort optimal information gain at the onset of habituation to repeated stimuli
topic habituation
information theory
nonequilibrium systems
url https://elifesciences.org/articles/99767
work_keys_str_mv AT giorgionicoletti optimalinformationgainattheonsetofhabituationtorepeatedstimuli
AT matteobruzzone optimalinformationgainattheonsetofhabituationtorepeatedstimuli
AT samirsuweis optimalinformationgainattheonsetofhabituationtorepeatedstimuli
AT marcodalmaschio optimalinformationgainattheonsetofhabituationtorepeatedstimuli
AT danielmariabusiello optimalinformationgainattheonsetofhabituationtorepeatedstimuli