Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation

Summary: Early life exposure to cannabis can result in long-lasting deficits in spatial navigation. We ask if the development of this behavior is subject to early life activity of type I cannabinoid receptor (CB1R) in the vestibular nucleus. In rodents, we found that local exposure to CB1R agonist w...

Full description

Saved in:
Bibliographic Details
Main Authors: Wei Shi, Kenneth Lap-Kei Wu, Mengliu Yang, Francisco Paulo De Nogueira Botelho, Oscar Wing-Ho Chua, Hui-Jing Hu, Ka-Pak Ng, Ulysses Tsz-Fung Lam, Kin-Wai Tam, Chun-Wai Ma, Daisy Kwok-Yan Shum, Ying-Shing Chan
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225008272
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849387501094961152
author Wei Shi
Kenneth Lap-Kei Wu
Mengliu Yang
Francisco Paulo De Nogueira Botelho
Oscar Wing-Ho Chua
Hui-Jing Hu
Ka-Pak Ng
Ulysses Tsz-Fung Lam
Kin-Wai Tam
Chun-Wai Ma
Daisy Kwok-Yan Shum
Ying-Shing Chan
author_facet Wei Shi
Kenneth Lap-Kei Wu
Mengliu Yang
Francisco Paulo De Nogueira Botelho
Oscar Wing-Ho Chua
Hui-Jing Hu
Ka-Pak Ng
Ulysses Tsz-Fung Lam
Kin-Wai Tam
Chun-Wai Ma
Daisy Kwok-Yan Shum
Ying-Shing Chan
author_sort Wei Shi
collection DOAJ
description Summary: Early life exposure to cannabis can result in long-lasting deficits in spatial navigation. We ask if the development of this behavior is subject to early life activity of type I cannabinoid receptor (CB1R) in the vestibular nucleus. In rodents, we found that local exposure to CB1R agonist within the first postnatal week, but not thereafter, led to a decline in the induction efficacy of long-term depression at GABAergic synapses (LTDGABA), a key step in the hard-wiring of vestibular circuits. Within this critical period, endocannabinoid-mediated LTDGABA at inhibitory neurons was selectively triggered by cholecystokinin, whereas that at excitatory neurons was by serotonin. Neonatal exposure to cannabinoids extended the phase of high GABAergic synaptic plasticity and overrode the synapse-specific, modulatory mechanism for plasticity. Such treatment delayed the postnatal emergence of vestibular-dependent reflexes and deranged adult navigational behavior. Deficits in higher functions are thus attributable to the maldevelopment of sensory processing circuits resulting from early cannabis exposure.
format Article
id doaj-art-ab2cb3d89424492fb876c205b5996fda
institution Kabale University
issn 2589-0042
language English
publishDate 2025-06-01
publisher Elsevier
record_format Article
series iScience
spelling doaj-art-ab2cb3d89424492fb876c205b5996fda2025-08-20T03:53:47ZengElsevieriScience2589-00422025-06-0128611256610.1016/j.isci.2025.112566Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigationWei Shi0Kenneth Lap-Kei Wu1Mengliu Yang2Francisco Paulo De Nogueira Botelho3Oscar Wing-Ho Chua4Hui-Jing Hu5Ka-Pak Ng6Ulysses Tsz-Fung Lam7Kin-Wai Tam8Chun-Wai Ma9Daisy Kwok-Yan Shum10Ying-Shing Chan11School of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Beijing Advanced Innovation Center for Big Data-based Precision Medicine, School of Engineering and Medicine, Beihang University, Beijing, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Neuroscience Research Centre, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaBeijing Advanced Innovation Center for Big Data-based Precision Medicine, School of Engineering and Medicine, Beihang University, Beijing, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Neuroscience Research Centre, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. ChinaSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Neuroscience Research Centre, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Corresponding authorSchool of Biomedical Sciences, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Neuroscience Research Centre, The University of Hong Kong, Pokfulam, Hong Kong SAR, P.R. China; Corresponding authorSummary: Early life exposure to cannabis can result in long-lasting deficits in spatial navigation. We ask if the development of this behavior is subject to early life activity of type I cannabinoid receptor (CB1R) in the vestibular nucleus. In rodents, we found that local exposure to CB1R agonist within the first postnatal week, but not thereafter, led to a decline in the induction efficacy of long-term depression at GABAergic synapses (LTDGABA), a key step in the hard-wiring of vestibular circuits. Within this critical period, endocannabinoid-mediated LTDGABA at inhibitory neurons was selectively triggered by cholecystokinin, whereas that at excitatory neurons was by serotonin. Neonatal exposure to cannabinoids extended the phase of high GABAergic synaptic plasticity and overrode the synapse-specific, modulatory mechanism for plasticity. Such treatment delayed the postnatal emergence of vestibular-dependent reflexes and deranged adult navigational behavior. Deficits in higher functions are thus attributable to the maldevelopment of sensory processing circuits resulting from early cannabis exposure.http://www.sciencedirect.com/science/article/pii/S2589004225008272Natural sciencesBiological sciencesNeuroscience
spellingShingle Wei Shi
Kenneth Lap-Kei Wu
Mengliu Yang
Francisco Paulo De Nogueira Botelho
Oscar Wing-Ho Chua
Hui-Jing Hu
Ka-Pak Ng
Ulysses Tsz-Fung Lam
Kin-Wai Tam
Chun-Wai Ma
Daisy Kwok-Yan Shum
Ying-Shing Chan
Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation
iScience
Natural sciences
Biological sciences
Neuroscience
title Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation
title_full Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation
title_fullStr Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation
title_full_unstemmed Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation
title_short Cannabinoid overrides triggers of GABAergic plasticity in vestibular circuits and distorts the development of navigation
title_sort cannabinoid overrides triggers of gabaergic plasticity in vestibular circuits and distorts the development of navigation
topic Natural sciences
Biological sciences
Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2589004225008272
work_keys_str_mv AT weishi cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT kennethlapkeiwu cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT mengliuyang cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT franciscopaulodenogueirabotelho cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT oscarwinghochua cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT huijinghu cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT kapakng cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT ulyssestszfunglam cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT kinwaitam cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT chunwaima cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT daisykwokyanshum cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation
AT yingshingchan cannabinoidoverridestriggersofgabaergicplasticityinvestibularcircuitsanddistortsthedevelopmentofnavigation