A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light

Olivier Brock; Cigdem Gelegen; Peter Sully; Irene  Salgarella; Polona Jager; Lucy Menage; Ishita Mehta; Jagoda Jęczmień-Łazur; Deyl Djama; Lauren Strother; Angelica Coculla; Anthony Vernon; Stephen G. Brickley; Philip Holland; Samuel Cooke; Alessio Delogu

doi:10.1523/JNEUROSCI.0112-21.2022

A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light

Olivier Brock, Cigdem Gelegen, Peter Sully, Irene Salgarella, Polona Jager, Lucy Menage, Ishita Mehta, Jagoda Jęczmień-Łazur, Deyl Djama, Lauren Strother, Angelica Coculla, Anthony Vernon, Stephen G. Brickley, Philip Holland, Samuel Cooke, Alessio Delogu

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Abstract

The thalamus is an important hub for sensory information and participates in sensory perception, regulation of attention, arousal and sleep. These functions are executed primarily by glutamatergic thalamocortical neurons that extend axons to the cortex and initiate cortico-thalamocortical connectional loops. However, the thalamus also contains projection GABAergic neurons that do not extend axons toward the cortex. Here, we have harnessed recent insight into the development of the intergeniculate leaflet (IGL) and the ventral lateral geniculate nucleus (LGv) to specifically target and manipulate thalamic projection GABAergic neurons in female and male mice. Our results show that thalamic GABAergic neurons of the IGL and LGv receive retinal input from diverse classes of retinal ganglion cells (RGCs) but not from the M1 intrinsically photosensitive retinal ganglion cell (ipRGC) type. We describe the synergistic role of the photoreceptor melanopsin and the thalamic neurons of the IGL/LGv in circadian entrainment to dim light. We identify a requirement for the thalamic IGL/LGv neurons in the rapid changes in vigilance states associated with circadian light transitions.

Original language	English
Pages (from-to)	9158-9179
Number of pages	22
Journal	The Journal of neuroscience : the official journal of the Society for Neuroscience
Volume	42
Issue number	49
DOIs	https://doi.org/10.1523/JNEUROSCI.0112-21.2022
Publication status	Published - 7 Dec 2022

Keywords

Animals
Female
Male
Mice
Circadian Rhythm/physiology
GABAergic Neurons/metabolism
Geniculate Bodies/physiology
Retina/metabolism
Retinal Ganglion Cells/physiology
Suprachiasmatic Nucleus/metabolism
Thalamus/metabolism
Light

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10.1523/JNEUROSCI.0112-21.2022Licence: CC BY

Brock et al., Journal of Neuroscience 2022Final published version, 12.3 MBLicence: CC BY

7 Citations
1 Article

A role for thalamic projection GABAergic neurons in circadian responses to light
Brock, O., Gelegen, C. E., Salgarella, I., Sully, P., Jager, P., Menage, L., Mehta, I., Jk eczmień-Łazur, J., Djama, D., Strother, L., Coculla, A., Vernon, A., Brickley, S., Holland, P., Cooke, S. & Delogu, A., 2022, In: bioRxiv.
Research output: Contribution to journal › Article

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Brock, O., Gelegen, C., Sully, P., Salgarella, I., Jager, P., Menage, L., Mehta, I., Jęczmień-Łazur, J., Djama, D., Strother, L., Coculla, A., Vernon, A., Brickley, S. G., Holland, P., Cooke, S., & Delogu, A. (2022). A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light. The Journal of neuroscience : the official journal of the Society for Neuroscience, 42(49), 9158-9179. https://doi.org/10.1523/JNEUROSCI.0112-21.2022

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title = "A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light",

abstract = "The thalamus is an important hub for sensory information and participates in sensory perception, regulation of attention, arousal and sleep. These functions are executed primarily by glutamatergic thalamocortical neurons that extend axons to the cortex and initiate cortico-thalamocortical connectional loops. However, the thalamus also contains projection GABAergic neurons that do not extend axons toward the cortex. Here, we have harnessed recent insight into the development of the intergeniculate leaflet (IGL) and the ventral lateral geniculate nucleus (LGv) to specifically target and manipulate thalamic projection GABAergic neurons in female and male mice. Our results show that thalamic GABAergic neurons of the IGL and LGv receive retinal input from diverse classes of retinal ganglion cells (RGCs) but not from the M1 intrinsically photosensitive retinal ganglion cell (ipRGC) type. We describe the synergistic role of the photoreceptor melanopsin and the thalamic neurons of the IGL/LGv in circadian entrainment to dim light. We identify a requirement for the thalamic IGL/LGv neurons in the rapid changes in vigilance states associated with circadian light transitions.",

keywords = "Animals, Female, Male, Mice, Circadian Rhythm/physiology, GABAergic Neurons/metabolism, Geniculate Bodies/physiology, Retina/metabolism, Retinal Ganglion Cells/physiology, Suprachiasmatic Nucleus/metabolism, Thalamus/metabolism, Light",

author = "Olivier Brock and Cigdem Gelegen and Peter Sully and Irene Salgarella and Polona Jager and Lucy Menage and Ishita Mehta and Jagoda J{\c e}czmie{\'n}-{\L}azur and Deyl Djama and Lauren Strother and Angelica Coculla and Anthony Vernon and Brickley, {Stephen G.} and Philip Holland and Samuel Cooke and Alessio Delogu",

note = "Copyright {\textcopyright} 2022 Brock et al.",

year = "2022",

month = dec,

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doi = "10.1523/JNEUROSCI.0112-21.2022",

language = "English",

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Brock, O , Gelegen, C , Sully, P, Salgarella, I, Jager, P , Menage, L , Mehta, I, Jęczmień-Łazur, J, Djama, D, Strother, L, Coculla, A, Vernon, A, Brickley, SG, Holland, P , Cooke, S & Delogu, A 2022, 'A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light', The Journal of neuroscience : the official journal of the Society for Neuroscience, vol. 42, no. 49, pp. 9158-9179. https://doi.org/10.1523/JNEUROSCI.0112-21.2022

TY - JOUR

T1 - A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light

AU - Brock, Olivier

AU - Gelegen, Cigdem

AU - Sully, Peter

AU - Salgarella, Irene

AU - Jager, Polona

AU - Menage, Lucy

AU - Mehta, Ishita

AU - Jęczmień-Łazur, Jagoda

AU - Djama, Deyl

AU - Strother, Lauren

AU - Coculla, Angelica

AU - Vernon, Anthony

AU - Brickley, Stephen G.

AU - Holland, Philip

AU - Cooke, Samuel

AU - Delogu, Alessio

PY - 2022/12/7

Y1 - 2022/12/7

N2 - The thalamus is an important hub for sensory information and participates in sensory perception, regulation of attention, arousal and sleep. These functions are executed primarily by glutamatergic thalamocortical neurons that extend axons to the cortex and initiate cortico-thalamocortical connectional loops. However, the thalamus also contains projection GABAergic neurons that do not extend axons toward the cortex. Here, we have harnessed recent insight into the development of the intergeniculate leaflet (IGL) and the ventral lateral geniculate nucleus (LGv) to specifically target and manipulate thalamic projection GABAergic neurons in female and male mice. Our results show that thalamic GABAergic neurons of the IGL and LGv receive retinal input from diverse classes of retinal ganglion cells (RGCs) but not from the M1 intrinsically photosensitive retinal ganglion cell (ipRGC) type. We describe the synergistic role of the photoreceptor melanopsin and the thalamic neurons of the IGL/LGv in circadian entrainment to dim light. We identify a requirement for the thalamic IGL/LGv neurons in the rapid changes in vigilance states associated with circadian light transitions.

AB - The thalamus is an important hub for sensory information and participates in sensory perception, regulation of attention, arousal and sleep. These functions are executed primarily by glutamatergic thalamocortical neurons that extend axons to the cortex and initiate cortico-thalamocortical connectional loops. However, the thalamus also contains projection GABAergic neurons that do not extend axons toward the cortex. Here, we have harnessed recent insight into the development of the intergeniculate leaflet (IGL) and the ventral lateral geniculate nucleus (LGv) to specifically target and manipulate thalamic projection GABAergic neurons in female and male mice. Our results show that thalamic GABAergic neurons of the IGL and LGv receive retinal input from diverse classes of retinal ganglion cells (RGCs) but not from the M1 intrinsically photosensitive retinal ganglion cell (ipRGC) type. We describe the synergistic role of the photoreceptor melanopsin and the thalamic neurons of the IGL/LGv in circadian entrainment to dim light. We identify a requirement for the thalamic IGL/LGv neurons in the rapid changes in vigilance states associated with circadian light transitions.

KW - Animals

KW - Female

KW - Male

KW - Mice

KW - Circadian Rhythm/physiology

KW - GABAergic Neurons/metabolism

KW - Geniculate Bodies/physiology

KW - Retina/metabolism

KW - Retinal Ganglion Cells/physiology

KW - Suprachiasmatic Nucleus/metabolism

KW - Thalamus/metabolism

KW - Light

U2 - 10.1523/JNEUROSCI.0112-21.2022

DO - 10.1523/JNEUROSCI.0112-21.2022

M3 - Article

C2 - 36280260

SN - 0270-6474

VL - 42

SP - 9158

EP - 9179

JO - The Journal of neuroscience : the official journal of the Society for Neuroscience

JF - The Journal of neuroscience : the official journal of the Society for Neuroscience

IS - 49

ER -

A Role for Thalamic Projection GABAergic Neurons in Circadian Responses to Light

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Keywords

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A role for thalamic projection GABAergic neurons in circadian responses to light

Cite this