Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure
Abstract Accumulating evidence points to dysregulations of the Nucleus Accumbens (NAc) in eating disorders (ED), however its precise contribution to ED symptomatic dimensions remains unclear. Using chemogenetic manipulations in male mice, we found that activity of dopamine D1 receptor-expressing neu...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-03-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-46874-9 |
| _version_ | 1797247231418433536 |
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| author | Roman Walle Anna Petitbon Giulia R. Fois Christophe Varin Enrica Montalban Lola Hardt Andrea Contini Maria Florencia Angelo Mylène Potier Rodrigue Ortole Asma Oummadi Véronique De Smedt-Peyrusse Roger A. Adan Bruno Giros Francis Chaouloff Guillaume Ferreira Alban de Kerchove d’Exaerde Fabien Ducrocq François Georges Pierre Trifilieff |
| author_facet | Roman Walle Anna Petitbon Giulia R. Fois Christophe Varin Enrica Montalban Lola Hardt Andrea Contini Maria Florencia Angelo Mylène Potier Rodrigue Ortole Asma Oummadi Véronique De Smedt-Peyrusse Roger A. Adan Bruno Giros Francis Chaouloff Guillaume Ferreira Alban de Kerchove d’Exaerde Fabien Ducrocq François Georges Pierre Trifilieff |
| author_sort | Roman Walle |
| collection | DOAJ |
| description | Abstract Accumulating evidence points to dysregulations of the Nucleus Accumbens (NAc) in eating disorders (ED), however its precise contribution to ED symptomatic dimensions remains unclear. Using chemogenetic manipulations in male mice, we found that activity of dopamine D1 receptor-expressing neurons of the NAc core subregion facilitated effort for a food reward as well as voluntary exercise, but decreased food intake, while D2-expressing neurons have opposite effects. These effects are congruent with D2-neurons being more active than D1-neurons during feeding while it is the opposite during running. Chronic manipulations of each subpopulations had limited effects on energy balance. However, repeated activation of D1-neurons combined with inhibition of D2-neurons biased behavior toward activity-related energy expenditure, whilst the opposite manipulations favored energy intake. Strikingly, concomitant activation of D1-neurons and inhibition of D2-neurons precipitated weight loss in anorexia models. These results suggest that dysregulations of NAc dopaminoceptive neurons might be at the core of EDs. |
| first_indexed | 2024-04-24T19:55:24Z |
| format | Article |
| id | doaj.art-dd0a804b992d4f64bb491a79e353f3d3 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-04-24T19:55:24Z |
| publishDate | 2024-03-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-dd0a804b992d4f64bb491a79e353f3d32024-03-24T12:24:52ZengNature PortfolioNature Communications2041-17232024-03-0115111610.1038/s41467-024-46874-9Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditureRoman Walle0Anna Petitbon1Giulia R. Fois2Christophe Varin3Enrica Montalban4Lola Hardt5Andrea Contini6Maria Florencia Angelo7Mylène Potier8Rodrigue Ortole9Asma Oummadi10Véronique De Smedt-Peyrusse11Roger A. Adan12Bruno Giros13Francis Chaouloff14Guillaume Ferreira15Alban de Kerchove d’Exaerde16Fabien Ducrocq17François Georges18Pierre Trifilieff19Université de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniv. Bordeaux, CNRS, IMN, UMR5293 F-33000Laboratory of Neurophysiology, ULB Neuroscience Institute, WELBIO, Université Libre de Bruxelles (ULB)Université de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniversité de Bordeaux, INRAE, Bordeaux INP, NutriNeuroDepartment of Translational Neuroscience, UMC Utrecht Brain Center, University Medical Center Utrecht, Universiteitsweg 100Department of Psychiatry, Douglas Hospital, McGill UniversityEndocannabinoids and NeuroAdaptation, NeuroCentre INSERM U1215Université de Bordeaux, INRAE, Bordeaux INP, NutriNeuroLaboratory of Neurophysiology, ULB Neuroscience Institute, WELBIO, Université Libre de Bruxelles (ULB)Université de Bordeaux, INRAE, Bordeaux INP, NutriNeuroUniv. Bordeaux, CNRS, IMN, UMR5293 F-33000Université de Bordeaux, INRAE, Bordeaux INP, NutriNeuroAbstract Accumulating evidence points to dysregulations of the Nucleus Accumbens (NAc) in eating disorders (ED), however its precise contribution to ED symptomatic dimensions remains unclear. Using chemogenetic manipulations in male mice, we found that activity of dopamine D1 receptor-expressing neurons of the NAc core subregion facilitated effort for a food reward as well as voluntary exercise, but decreased food intake, while D2-expressing neurons have opposite effects. These effects are congruent with D2-neurons being more active than D1-neurons during feeding while it is the opposite during running. Chronic manipulations of each subpopulations had limited effects on energy balance. However, repeated activation of D1-neurons combined with inhibition of D2-neurons biased behavior toward activity-related energy expenditure, whilst the opposite manipulations favored energy intake. Strikingly, concomitant activation of D1-neurons and inhibition of D2-neurons precipitated weight loss in anorexia models. These results suggest that dysregulations of NAc dopaminoceptive neurons might be at the core of EDs.https://doi.org/10.1038/s41467-024-46874-9 |
| spellingShingle | Roman Walle Anna Petitbon Giulia R. Fois Christophe Varin Enrica Montalban Lola Hardt Andrea Contini Maria Florencia Angelo Mylène Potier Rodrigue Ortole Asma Oummadi Véronique De Smedt-Peyrusse Roger A. Adan Bruno Giros Francis Chaouloff Guillaume Ferreira Alban de Kerchove d’Exaerde Fabien Ducrocq François Georges Pierre Trifilieff Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure Nature Communications |
| title | Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure |
| title_full | Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure |
| title_fullStr | Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure |
| title_full_unstemmed | Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure |
| title_short | Nucleus accumbens D1- and D2-expressing neurons control the balance between feeding and activity-mediated energy expenditure |
| title_sort | nucleus accumbens d1 and d2 expressing neurons control the balance between feeding and activity mediated energy expenditure |
| url | https://doi.org/10.1038/s41467-024-46874-9 |
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