Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.

In natural signals, such as the luminance value across of a visual scene, abrupt changes in intensity value are often more relevant to an organism than intensity values at other positions and times. Thus to reduce redundancy, sensory systems are specialized to detect the times and amplitudes of info...

Full description

Saved in:
Bibliographic Details
Main Authors: Danke Zhang, Si Wu, Malte J Rasch
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0118125&type=printable
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850023221209858048
author Danke Zhang
Si Wu
Malte J Rasch
author_facet Danke Zhang
Si Wu
Malte J Rasch
author_sort Danke Zhang
collection DOAJ
description In natural signals, such as the luminance value across of a visual scene, abrupt changes in intensity value are often more relevant to an organism than intensity values at other positions and times. Thus to reduce redundancy, sensory systems are specialized to detect the times and amplitudes of informative abrupt changes in the input stream rather than coding the intensity values at all times. In theory, a system that responds transiently to fast changes is called a differentiator. In principle, several different neural circuit mechanisms exist that are capable of responding transiently to abrupt input changes. However, it is unclear which circuit would be best suited for early sensory systems, where the dynamic range of the natural input signals can be very wide. We here compare the properties of different simple neural circuit motifs for implementing signal differentiation. We found that a circuit motif based on presynaptic inhibition (PI) is unique in a sense that the vesicle resources in the presynaptic site can be stably maintained over a wide range of stimulus intensities, making PI a biophysically plausible mechanism to implement a differentiator with a very wide dynamical range. Moreover, by additionally considering short-term plasticity (STP), differentiation becomes contrast adaptive in the PI-circuit but not in other potential neural circuit motifs. Numerical simulations show that the behavior of the adaptive PI-circuit is consistent with experimental observations suggesting that adaptive presynaptic inhibition might be a good candidate neural mechanism to achieve differentiation in early sensory systems.
format Article
id doaj-art-6192b6e9c3584ae5b6e33a99f36df8fe
institution DOAJ
issn 1932-6203
language English
publishDate 2015-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-6192b6e9c3584ae5b6e33a99f36df8fe2025-08-20T03:01:27ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01102e011812510.1371/journal.pone.0118125Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.Danke ZhangSi WuMalte J RaschIn natural signals, such as the luminance value across of a visual scene, abrupt changes in intensity value are often more relevant to an organism than intensity values at other positions and times. Thus to reduce redundancy, sensory systems are specialized to detect the times and amplitudes of informative abrupt changes in the input stream rather than coding the intensity values at all times. In theory, a system that responds transiently to fast changes is called a differentiator. In principle, several different neural circuit mechanisms exist that are capable of responding transiently to abrupt input changes. However, it is unclear which circuit would be best suited for early sensory systems, where the dynamic range of the natural input signals can be very wide. We here compare the properties of different simple neural circuit motifs for implementing signal differentiation. We found that a circuit motif based on presynaptic inhibition (PI) is unique in a sense that the vesicle resources in the presynaptic site can be stably maintained over a wide range of stimulus intensities, making PI a biophysically plausible mechanism to implement a differentiator with a very wide dynamical range. Moreover, by additionally considering short-term plasticity (STP), differentiation becomes contrast adaptive in the PI-circuit but not in other potential neural circuit motifs. Numerical simulations show that the behavior of the adaptive PI-circuit is consistent with experimental observations suggesting that adaptive presynaptic inhibition might be a good candidate neural mechanism to achieve differentiation in early sensory systems.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0118125&type=printable
spellingShingle Danke Zhang
Si Wu
Malte J Rasch
Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.
PLoS ONE
title Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.
title_full Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.
title_fullStr Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.
title_full_unstemmed Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.
title_short Circuit motifs for contrast-adaptive differentiation in early sensory systems: the role of presynaptic inhibition and short-term plasticity.
title_sort circuit motifs for contrast adaptive differentiation in early sensory systems the role of presynaptic inhibition and short term plasticity
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0118125&type=printable
work_keys_str_mv AT dankezhang circuitmotifsforcontrastadaptivedifferentiationinearlysensorysystemstheroleofpresynapticinhibitionandshorttermplasticity
AT siwu circuitmotifsforcontrastadaptivedifferentiationinearlysensorysystemstheroleofpresynapticinhibitionandshorttermplasticity
AT maltejrasch circuitmotifsforcontrastadaptivedifferentiationinearlysensorysystemstheroleofpresynapticinhibitionandshorttermplasticity