Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits

Abstract Chronic methamphetamine (METH) use, a prevalent psychostimulant, is known to impair attention, yet the cellular mechanisms driving these deficits remain poorly understood. Here, we employed a rat model of repeated passive METH injections and evaluated attentional performance using the 5-cho...

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Main Authors: Xiaotian Qu, Pingyuan Yang, Rongwei Zhai, Zhi-Qi Xiong
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Acta Neuropathologica Communications
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Online Access:https://doi.org/10.1186/s40478-024-01890-0
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author Xiaotian Qu
Pingyuan Yang
Rongwei Zhai
Zhi-Qi Xiong
author_facet Xiaotian Qu
Pingyuan Yang
Rongwei Zhai
Zhi-Qi Xiong
author_sort Xiaotian Qu
collection DOAJ
description Abstract Chronic methamphetamine (METH) use, a prevalent psychostimulant, is known to impair attention, yet the cellular mechanisms driving these deficits remain poorly understood. Here, we employed a rat model of repeated passive METH injections and evaluated attentional performance using the 5-choice serial reaction time task (5-CSRTT). Using single-nucleus RNA sequencing, immunofluorescence and in situ hybridization, we characterized the response of neurons in the reticulotegmental nucleus (RtTg) to METH exposure. Our results indicate that METH exposure disrupts RtTg neurons at the transcriptional level and results in an increased activation ratio of RtTg under 5-CSRTT conditions. Crucially, chemogenetic inactivation of these neurons or RtTg lesion attenuated METH-induced attention deficits, whereas their activation reproduced the deficits. These findings underscore the critical role of RtTg neurons in mediating METH-induced attention deficits, positioning RtTg as a promising therapeutic target for the treatment of attention deficits linked to chronic METH use.
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institution OA Journals
issn 2051-5960
language English
publishDate 2024-11-01
publisher BMC
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series Acta Neuropathologica Communications
spelling doaj-art-b3edd3bde2e5486ab1a73ce9b083ff852025-08-20T02:33:32ZengBMCActa Neuropathologica Communications2051-59602024-11-0112111510.1186/s40478-024-01890-0Inhibition of RtTg neurons reverses methamphetamine-induced attention deficitsXiaotian Qu0Pingyuan Yang1Rongwei Zhai2Zhi-Qi Xiong3Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence TechnologyShanghai Mental Health Center, Shanghai Jiao Tong University School of MedicineLin Gang LaboratoryInstitute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence TechnologyAbstract Chronic methamphetamine (METH) use, a prevalent psychostimulant, is known to impair attention, yet the cellular mechanisms driving these deficits remain poorly understood. Here, we employed a rat model of repeated passive METH injections and evaluated attentional performance using the 5-choice serial reaction time task (5-CSRTT). Using single-nucleus RNA sequencing, immunofluorescence and in situ hybridization, we characterized the response of neurons in the reticulotegmental nucleus (RtTg) to METH exposure. Our results indicate that METH exposure disrupts RtTg neurons at the transcriptional level and results in an increased activation ratio of RtTg under 5-CSRTT conditions. Crucially, chemogenetic inactivation of these neurons or RtTg lesion attenuated METH-induced attention deficits, whereas their activation reproduced the deficits. These findings underscore the critical role of RtTg neurons in mediating METH-induced attention deficits, positioning RtTg as a promising therapeutic target for the treatment of attention deficits linked to chronic METH use.https://doi.org/10.1186/s40478-024-01890-0Methamphetamine (METH)AttentionSingle-nuclei RNA sequencing (snRNA-seq)Reticulotegmental nucleus (RtTg)Five-choice serial reaction time task (5-CSRTT)Designer receptors exclusively activated by designer drugs (DREADD)
spellingShingle Xiaotian Qu
Pingyuan Yang
Rongwei Zhai
Zhi-Qi Xiong
Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits
Acta Neuropathologica Communications
Methamphetamine (METH)
Attention
Single-nuclei RNA sequencing (snRNA-seq)
Reticulotegmental nucleus (RtTg)
Five-choice serial reaction time task (5-CSRTT)
Designer receptors exclusively activated by designer drugs (DREADD)
title Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits
title_full Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits
title_fullStr Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits
title_full_unstemmed Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits
title_short Inhibition of RtTg neurons reverses methamphetamine-induced attention deficits
title_sort inhibition of rttg neurons reverses methamphetamine induced attention deficits
topic Methamphetamine (METH)
Attention
Single-nuclei RNA sequencing (snRNA-seq)
Reticulotegmental nucleus (RtTg)
Five-choice serial reaction time task (5-CSRTT)
Designer receptors exclusively activated by designer drugs (DREADD)
url https://doi.org/10.1186/s40478-024-01890-0
work_keys_str_mv AT xiaotianqu inhibitionofrttgneuronsreversesmethamphetamineinducedattentiondeficits
AT pingyuanyang inhibitionofrttgneuronsreversesmethamphetamineinducedattentiondeficits
AT rongweizhai inhibitionofrttgneuronsreversesmethamphetamineinducedattentiondeficits
AT zhiqixiong inhibitionofrttgneuronsreversesmethamphetamineinducedattentiondeficits