Dynamics and potential significance of spontaneous activity in the habenula

The habenula is an evolutionarily conserved structure of the vertebrate brain that is essential for behavioural flexibility and mood control. It is spontaneously active and is able to access diverse states when the animal is exposed to sensory stimuli. Here we investigate the dynamics of habenula sp...

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Main Authors: Suryadi, Cheng, Ruey-Kuang, Birkett, Elliot, Jesuthasan, Suresh, Chew, Lock Yue
Other Authors: School of Physical and Mathematical Sciences
Format: Article
Language:English
Published: 2023
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Online Access:https://hdl.handle.net/10356/164377
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Institution: Nanyang Technological University
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spelling sg-ntu-dr.10356-1643772023-02-28T20:10:13Z Dynamics and potential significance of spontaneous activity in the habenula Suryadi Cheng, Ruey-Kuang Birkett, Elliot Jesuthasan, Suresh Chew, Lock Yue School of Physical and Mathematical Sciences Lee Kong Chian School of Medicine (LKCMedicine) Institute of Molecular and Cell Biology Complexity Institute Science::Biological sciences Avalanche Criticality The habenula is an evolutionarily conserved structure of the vertebrate brain that is essential for behavioural flexibility and mood control. It is spontaneously active and is able to access diverse states when the animal is exposed to sensory stimuli. Here we investigate the dynamics of habenula spontaneous activity, to gain insight into how sensitivity is optimized. Two-photon calcium imaging was performed in resting zebrafish larvae at single cell resolution. An analysis of avalanches of inferred spikes suggests that the habenula is subcritical. Activity had low covariance and a small mean, arguing against dynamic criticality. A multiple regression estimator of autocorrelation time suggests that the habenula is neither fully asynchronous nor perfectly critical, but is reverberating. This pattern of dynamics may enable integration of information and high flexibility in the tuning of network properties, thus providing a potential mechanism for the optimal responses to a changing environment. Significance Statement: Spontaneous activity in neurons shapes the response to stimuli. One structure with a high level of spontaneous neuronal activity is the habenula, a regulator of broadly acting neuromodulators involved in mood and learning. How does this activity influence habenula function? We show here that the habenula of a resting animal is near criticality, in a state termed reverberation. This pattern of dynamics is consistent with high sensitivity and flexibility, and may enable the habenula to respond optimally to a wide range of stimuli. Ministry of Education (MOE) Published version This work was funded by the Singapore Ministry of Education through an Academic Research Fund Tier 1 Award (MOE2016-T1-001-152) and a Tier 2 Award (MOE2017-T2-1-058). 2023-01-18T05:03:42Z 2023-01-18T05:03:42Z 2022 Journal Article Suryadi, Cheng, R., Birkett, E., Jesuthasan, S. & Chew, L. Y. (2022). Dynamics and potential significance of spontaneous activity in the habenula. ENeuro, 9(5). https://dx.doi.org/10.1523/ENEURO.0287-21.2022 2373-2822 https://hdl.handle.net/10356/164377 10.1523/ENEURO.0287-21.2022 35981869 2-s2.0-85137338392 5 9 en MOE2016-T1-001-152 MOE2017-T2-1-058 eNeuro © 2022 Suryadi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. application/pdf
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Avalanche
Criticality
spellingShingle Science::Biological sciences
Avalanche
Criticality
Suryadi
Cheng, Ruey-Kuang
Birkett, Elliot
Jesuthasan, Suresh
Chew, Lock Yue
Dynamics and potential significance of spontaneous activity in the habenula
description The habenula is an evolutionarily conserved structure of the vertebrate brain that is essential for behavioural flexibility and mood control. It is spontaneously active and is able to access diverse states when the animal is exposed to sensory stimuli. Here we investigate the dynamics of habenula spontaneous activity, to gain insight into how sensitivity is optimized. Two-photon calcium imaging was performed in resting zebrafish larvae at single cell resolution. An analysis of avalanches of inferred spikes suggests that the habenula is subcritical. Activity had low covariance and a small mean, arguing against dynamic criticality. A multiple regression estimator of autocorrelation time suggests that the habenula is neither fully asynchronous nor perfectly critical, but is reverberating. This pattern of dynamics may enable integration of information and high flexibility in the tuning of network properties, thus providing a potential mechanism for the optimal responses to a changing environment. Significance Statement: Spontaneous activity in neurons shapes the response to stimuli. One structure with a high level of spontaneous neuronal activity is the habenula, a regulator of broadly acting neuromodulators involved in mood and learning. How does this activity influence habenula function? We show here that the habenula of a resting animal is near criticality, in a state termed reverberation. This pattern of dynamics is consistent with high sensitivity and flexibility, and may enable the habenula to respond optimally to a wide range of stimuli.
author2 School of Physical and Mathematical Sciences
author_facet School of Physical and Mathematical Sciences
Suryadi
Cheng, Ruey-Kuang
Birkett, Elliot
Jesuthasan, Suresh
Chew, Lock Yue
format Article
author Suryadi
Cheng, Ruey-Kuang
Birkett, Elliot
Jesuthasan, Suresh
Chew, Lock Yue
author_sort Suryadi
title Dynamics and potential significance of spontaneous activity in the habenula
title_short Dynamics and potential significance of spontaneous activity in the habenula
title_full Dynamics and potential significance of spontaneous activity in the habenula
title_fullStr Dynamics and potential significance of spontaneous activity in the habenula
title_full_unstemmed Dynamics and potential significance of spontaneous activity in the habenula
title_sort dynamics and potential significance of spontaneous activity in the habenula
publishDate 2023
url https://hdl.handle.net/10356/164377
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