Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation

Mahesh M. Karnani; Cornelia Schöne; Edward F. Bracey; J. Antonio González; Paulius Viskaitis; Han-Tao Li; Antoine Adamantidis; Denis Burdakov

doi:10.1016/j.pneurobio.2020.101771

Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation

Mahesh M. Karnani^* (Corresponding Author), Cornelia Schöne, Edward F. Bracey, J. Antonio González, Paulius Viskaitis, Han-Tao Li, Antoine Adamantidis, Denis Burdakov

^*Corresponding author for this work

The Rowett Institute of Nutrition and Health

Research output: Contribution to journal › Article › peer-review

41 Citations (Scopus)

6 Downloads (Pure)

Abstract

Summary Appropriate motor control is critical for normal life, and requires hypothalamic hypocretin/orexin neurons (HONs). HONs are slowly regulated by nutrients, but also display rapid (subsecond) activity fluctuations in vivo. The necessity of these activity bursts for sensorimotor control and their roles in specific phases of movement are unknown. Here we show that temporally-restricted optosilencing of spontaneous or sensory-evoked HON bursts disrupts locomotion initiation, but does not affect ongoing locomotion. Conversely, HON optostimulation initiates locomotion with subsecond delays in a frequency-dependent manner. Using 2-photon volumetric imaging of activity of >300 HONs during sensory stimulation and self-initiated locomotion, we identify several locomotion-related HON subtypes, which distinctly predict the probability of imminent locomotion initiation, display distinct sensory responses, and are differentially modulated by food deprivation. By causally linking HON bursts to locomotion initiation, these findings reveal the sensorimotor importance of rapid spontaneous and evoked fluctuations in HON ensemble activity.

Original language	English
Article number	101771
Number of pages	17
Journal	Progress in Neurobiology
Volume	187
Early online date	11 Feb 2020
DOIs	https://doi.org/10.1016/j.pneurobio.2020.101771
Publication status	Published - 1 Apr 2020

Bibliographical note

Funding Information:
We thank Markus Marks and other Fatih Yanik lab members for help with machine learning, Lise T. Jensen and Lars Fugger for sharing O-DTR mice, Takeshi Sakurai for sharing the orexin promoter used for generating HON specific constructs, Alan Ling and Adam Hurst at the Francis Crick Institute mechanical workshop for making recording arenas, staff at Vigene for technical assistance with viruses, Bruno Pichler and Dale Elgar for microscope design, Troy Margrie for sharing equipment, and all Burdakov lab members for useful comments and help. This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement DRIVOME (grant agreement 701986 ). This work was funded by The Francis Crick Institute , which receives its core funding from Cancer Research UK ( FC001055 ), the UK Medical Research Council ( FC001055 ), and the Wellcome Trust ( FC001055 ). AA was supported by the Human Frontier Science Program , Inselspital University Hospital Bern , Swiss National Science Foundation , European Research Council , the University of Bern and the Bern University Hospital .

Keywords

hypothalamus
orexin/hypocretin neurons
locomotion
sensorimotor processing
ensemble imaging
Locomotion
Ensemble imaging

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1016/j.pneurobio.2020.101771Licence: CC BY

Karnani_etal_PN_Role_of_spontaneous_VOR
Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).
Final published version, 16.6 MBLicence: CC BY

http://www.sciencedirect.com/science/article/pii/S0301008220300265

Cite this

@article{a95d7c911c1c4ccb8d2761ffda5907ba,

title = "Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation",

abstract = "Summary Appropriate motor control is critical for normal life, and requires hypothalamic hypocretin/orexin neurons (HONs). HONs are slowly regulated by nutrients, but also display rapid (subsecond) activity fluctuations in vivo. The necessity of these activity bursts for sensorimotor control and their roles in specific phases of movement are unknown. Here we show that temporally-restricted optosilencing of spontaneous or sensory-evoked HON bursts disrupts locomotion initiation, but does not affect ongoing locomotion. Conversely, HON optostimulation initiates locomotion with subsecond delays in a frequency-dependent manner. Using 2-photon volumetric imaging of activity of >300 HONs during sensory stimulation and self-initiated locomotion, we identify several locomotion-related HON subtypes, which distinctly predict the probability of imminent locomotion initiation, display distinct sensory responses, and are differentially modulated by food deprivation. By causally linking HON bursts to locomotion initiation, these findings reveal the sensorimotor importance of rapid spontaneous and evoked fluctuations in HON ensemble activity.",

keywords = "hypothalamus, orexin/hypocretin neurons, locomotion, sensorimotor processing, ensemble imaging, Locomotion, Ensemble imaging",

author = "Karnani, {Mahesh M.} and Cornelia Sch{\"o}ne and Bracey, {Edward F.} and Gonz{\'a}lez, {J. Antonio} and Paulius Viskaitis and Han-Tao Li and Antoine Adamantidis and Denis Burdakov",

note = "Funding Information: We thank Markus Marks and other Fatih Yanik lab members for help with machine learning, Lise T. Jensen and Lars Fugger for sharing O-DTR mice, Takeshi Sakurai for sharing the orexin promoter used for generating HON specific constructs, Alan Ling and Adam Hurst at the Francis Crick Institute mechanical workshop for making recording arenas, staff at Vigene for technical assistance with viruses, Bruno Pichler and Dale Elgar for microscope design, Troy Margrie for sharing equipment, and all Burdakov lab members for useful comments and help. This project has received funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under the Marie Sk{\l}odowska-Curie grant agreement DRIVOME (grant agreement 701986 ). This work was funded by The Francis Crick Institute , which receives its core funding from Cancer Research UK ( FC001055 ), the UK Medical Research Council ( FC001055 ), and the Wellcome Trust ( FC001055 ). AA was supported by the Human Frontier Science Program , Inselspital University Hospital Bern , Swiss National Science Foundation , European Research Council , the University of Bern and the Bern University Hospital . ",

year = "2020",

month = apr,

day = "1",

doi = "10.1016/j.pneurobio.2020.101771",

language = "English",

volume = "187",

journal = "Progress in Neurobiology",

issn = "0301-0082",

publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation

AU - Karnani, Mahesh M.

AU - Schöne, Cornelia

AU - Bracey, Edward F.

AU - González, J. Antonio

AU - Viskaitis, Paulius

AU - Li, Han-Tao

AU - Adamantidis, Antoine

AU - Burdakov, Denis

N1 - Funding Information: We thank Markus Marks and other Fatih Yanik lab members for help with machine learning, Lise T. Jensen and Lars Fugger for sharing O-DTR mice, Takeshi Sakurai for sharing the orexin promoter used for generating HON specific constructs, Alan Ling and Adam Hurst at the Francis Crick Institute mechanical workshop for making recording arenas, staff at Vigene for technical assistance with viruses, Bruno Pichler and Dale Elgar for microscope design, Troy Margrie for sharing equipment, and all Burdakov lab members for useful comments and help. This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement DRIVOME (grant agreement 701986 ). This work was funded by The Francis Crick Institute , which receives its core funding from Cancer Research UK ( FC001055 ), the UK Medical Research Council ( FC001055 ), and the Wellcome Trust ( FC001055 ). AA was supported by the Human Frontier Science Program , Inselspital University Hospital Bern , Swiss National Science Foundation , European Research Council , the University of Bern and the Bern University Hospital .

PY - 2020/4/1

Y1 - 2020/4/1

N2 - Summary Appropriate motor control is critical for normal life, and requires hypothalamic hypocretin/orexin neurons (HONs). HONs are slowly regulated by nutrients, but also display rapid (subsecond) activity fluctuations in vivo. The necessity of these activity bursts for sensorimotor control and their roles in specific phases of movement are unknown. Here we show that temporally-restricted optosilencing of spontaneous or sensory-evoked HON bursts disrupts locomotion initiation, but does not affect ongoing locomotion. Conversely, HON optostimulation initiates locomotion with subsecond delays in a frequency-dependent manner. Using 2-photon volumetric imaging of activity of >300 HONs during sensory stimulation and self-initiated locomotion, we identify several locomotion-related HON subtypes, which distinctly predict the probability of imminent locomotion initiation, display distinct sensory responses, and are differentially modulated by food deprivation. By causally linking HON bursts to locomotion initiation, these findings reveal the sensorimotor importance of rapid spontaneous and evoked fluctuations in HON ensemble activity.

AB - Summary Appropriate motor control is critical for normal life, and requires hypothalamic hypocretin/orexin neurons (HONs). HONs are slowly regulated by nutrients, but also display rapid (subsecond) activity fluctuations in vivo. The necessity of these activity bursts for sensorimotor control and their roles in specific phases of movement are unknown. Here we show that temporally-restricted optosilencing of spontaneous or sensory-evoked HON bursts disrupts locomotion initiation, but does not affect ongoing locomotion. Conversely, HON optostimulation initiates locomotion with subsecond delays in a frequency-dependent manner. Using 2-photon volumetric imaging of activity of >300 HONs during sensory stimulation and self-initiated locomotion, we identify several locomotion-related HON subtypes, which distinctly predict the probability of imminent locomotion initiation, display distinct sensory responses, and are differentially modulated by food deprivation. By causally linking HON bursts to locomotion initiation, these findings reveal the sensorimotor importance of rapid spontaneous and evoked fluctuations in HON ensemble activity.

KW - hypothalamus

KW - orexin/hypocretin neurons

KW - locomotion

KW - sensorimotor processing

KW - ensemble imaging

KW - Locomotion

KW - Ensemble imaging

UR - http://www.scopus.com/inward/record.url?scp=85079851651&partnerID=8YFLogxK

U2 - 10.1016/j.pneurobio.2020.101771

DO - 10.1016/j.pneurobio.2020.101771

M3 - Article

SN - 0301-0082

VL - 187

JO - Progress in Neurobiology

JF - Progress in Neurobiology

M1 - 101771

ER -

Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation

Abstract

Bibliographical note

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Antonio Gonzalez

Cite this

Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation

Abstract

Bibliographical note

Keywords

UN SDGs

Access to Document

Other files and links

Fingerprint

Profiles

Antonio Gonzalez

Cite this