Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion
Autor(a) principal: | |
---|---|
Data de Publicação: | 2020 |
Outros Autores: | , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/1822/62385 |
Resumo: | Deficits in decoding rewarding (and aversive) signals are present in several neuropsychiatric conditions such as depression and addiction, emphasising the importance of studying the underlying neural circuits in detail. One of the key regions of the reward circuit is the nucleus accumbens (NAc). The classical view on the field postulates that NAc dopamine receptor D1-expressing medium spiny neurons (D1-MSNs) convey reward signals, while dopamine receptor D2-expressing MSNs (D2-MSNs) encode aversion. Here, we show that both MSN subpopulations can drive reward and aversion, depending on their neuronal stimulation pattern. Brief D1- or D2-MSN optogenetic stimulation elicited positive reinforcement and enhanced cocaine conditioning. Conversely, prolonged activation induced aversion, and in the case of D2-MSNs, decreased cocaine conditioning. Brief stimulation was associated with increased ventral tegmenta area (VTA) dopaminergic tone either directly (for D1-MSNs) or indirectly via ventral pallidum (VP) (for D1- and D2-MSNs). Importantly, prolonged stimulation of either MSN subpopulation induced remarkably distinct electrophysiological effects in these target regions. We further show that blocking κ-opioid receptors in the VTA (but not in VP) abolishes the behavioral effects induced by D1-MSN prolonged stimulation. In turn, blocking δ-opioid receptors in the VP (but not in VTA) blocks the behavioral effects elicited by D2-MSN prolonged stimulation. Our findings demonstrate that D1- and D2-MSNs can bidirectionally control reward and aversion, explaining the existence of controversial studies in the field, and highlights that the proposed striatal functional opposition needs to be reconsidered. |
id |
RCAP_0196cdf6f098bd22d511f88f9f9a9945 |
---|---|
oai_identifier_str |
oai:repositorium.sdum.uminho.pt:1822/62385 |
network_acronym_str |
RCAP |
network_name_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
repository_id_str |
7160 |
spelling |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversionCiências Médicas::Medicina BásicaScience & TechnologyDeficits in decoding rewarding (and aversive) signals are present in several neuropsychiatric conditions such as depression and addiction, emphasising the importance of studying the underlying neural circuits in detail. One of the key regions of the reward circuit is the nucleus accumbens (NAc). The classical view on the field postulates that NAc dopamine receptor D1-expressing medium spiny neurons (D1-MSNs) convey reward signals, while dopamine receptor D2-expressing MSNs (D2-MSNs) encode aversion. Here, we show that both MSN subpopulations can drive reward and aversion, depending on their neuronal stimulation pattern. Brief D1- or D2-MSN optogenetic stimulation elicited positive reinforcement and enhanced cocaine conditioning. Conversely, prolonged activation induced aversion, and in the case of D2-MSNs, decreased cocaine conditioning. Brief stimulation was associated with increased ventral tegmenta area (VTA) dopaminergic tone either directly (for D1-MSNs) or indirectly via ventral pallidum (VP) (for D1- and D2-MSNs). Importantly, prolonged stimulation of either MSN subpopulation induced remarkably distinct electrophysiological effects in these target regions. We further show that blocking κ-opioid receptors in the VTA (but not in VP) abolishes the behavioral effects induced by D1-MSN prolonged stimulation. In turn, blocking δ-opioid receptors in the VP (but not in VTA) blocks the behavioral effects elicited by D2-MSN prolonged stimulation. Our findings demonstrate that D1- and D2-MSNs can bidirectionally control reward and aversion, explaining the existence of controversial studies in the field, and highlights that the proposed striatal functional opposition needs to be reconsidered.FCT -Fundação para a Ciência e a Tecnologia(30/2016)Nature Publishing Group (NPG)Universidade do MinhoSoares-Cunha, CarinaVasconcelos, Nivaldo António PortelaCoimbra, BárbaraDomingues, Ana VerónicaSilva, Joana M.Loureiro-Campos, EduardoGaspar, RitaSotiropoulos, I.Sousa, NunoRodrigues, Ana João20202020-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/1822/62385engSoares-Cunha, C., de Vasconcelos, N. A., Coimbra, B., Domingues, A. V., et. al. (2020). Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion. Molecular psychiatry, 1-15.1359-41841476-557810.1038/s41380-019-0484-331462765https://www.nature.com/articles/s41380-019-0484-3info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-21T11:55:56Zoai:repositorium.sdum.uminho.pt:1822/62385Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T18:45:31.971033Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
title |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
spellingShingle |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion Soares-Cunha, Carina Ciências Médicas::Medicina Básica Science & Technology |
title_short |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
title_full |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
title_fullStr |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
title_full_unstemmed |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
title_sort |
Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion |
author |
Soares-Cunha, Carina |
author_facet |
Soares-Cunha, Carina Vasconcelos, Nivaldo António Portela Coimbra, Bárbara Domingues, Ana Verónica Silva, Joana M. Loureiro-Campos, Eduardo Gaspar, Rita Sotiropoulos, I. Sousa, Nuno Rodrigues, Ana João |
author_role |
author |
author2 |
Vasconcelos, Nivaldo António Portela Coimbra, Bárbara Domingues, Ana Verónica Silva, Joana M. Loureiro-Campos, Eduardo Gaspar, Rita Sotiropoulos, I. Sousa, Nuno Rodrigues, Ana João |
author2_role |
author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade do Minho |
dc.contributor.author.fl_str_mv |
Soares-Cunha, Carina Vasconcelos, Nivaldo António Portela Coimbra, Bárbara Domingues, Ana Verónica Silva, Joana M. Loureiro-Campos, Eduardo Gaspar, Rita Sotiropoulos, I. Sousa, Nuno Rodrigues, Ana João |
dc.subject.por.fl_str_mv |
Ciências Médicas::Medicina Básica Science & Technology |
topic |
Ciências Médicas::Medicina Básica Science & Technology |
description |
Deficits in decoding rewarding (and aversive) signals are present in several neuropsychiatric conditions such as depression and addiction, emphasising the importance of studying the underlying neural circuits in detail. One of the key regions of the reward circuit is the nucleus accumbens (NAc). The classical view on the field postulates that NAc dopamine receptor D1-expressing medium spiny neurons (D1-MSNs) convey reward signals, while dopamine receptor D2-expressing MSNs (D2-MSNs) encode aversion. Here, we show that both MSN subpopulations can drive reward and aversion, depending on their neuronal stimulation pattern. Brief D1- or D2-MSN optogenetic stimulation elicited positive reinforcement and enhanced cocaine conditioning. Conversely, prolonged activation induced aversion, and in the case of D2-MSNs, decreased cocaine conditioning. Brief stimulation was associated with increased ventral tegmenta area (VTA) dopaminergic tone either directly (for D1-MSNs) or indirectly via ventral pallidum (VP) (for D1- and D2-MSNs). Importantly, prolonged stimulation of either MSN subpopulation induced remarkably distinct electrophysiological effects in these target regions. We further show that blocking κ-opioid receptors in the VTA (but not in VP) abolishes the behavioral effects induced by D1-MSN prolonged stimulation. In turn, blocking δ-opioid receptors in the VP (but not in VTA) blocks the behavioral effects elicited by D2-MSN prolonged stimulation. Our findings demonstrate that D1- and D2-MSNs can bidirectionally control reward and aversion, explaining the existence of controversial studies in the field, and highlights that the proposed striatal functional opposition needs to be reconsidered. |
publishDate |
2020 |
dc.date.none.fl_str_mv |
2020 2020-01-01T00:00:00Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/1822/62385 |
url |
http://hdl.handle.net/1822/62385 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Soares-Cunha, C., de Vasconcelos, N. A., Coimbra, B., Domingues, A. V., et. al. (2020). Nucleus accumbens medium spiny neurons subtypes signal both reward and aversion. Molecular psychiatry, 1-15. 1359-4184 1476-5578 10.1038/s41380-019-0484-3 31462765 https://www.nature.com/articles/s41380-019-0484-3 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
Nature Publishing Group (NPG) |
publisher.none.fl_str_mv |
Nature Publishing Group (NPG) |
dc.source.none.fl_str_mv |
reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação instacron:RCAAP |
instname_str |
Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
instacron_str |
RCAAP |
institution |
RCAAP |
reponame_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
collection |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
repository.name.fl_str_mv |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
repository.mail.fl_str_mv |
|
_version_ |
1799132208010625024 |