Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict.
Successful resolution of approach-avoidance conflict (AAC) is fundamentally important for survival, and its dysregulation is a hallmark of many neuropsychiatric disorders, and yet the underlying neural circuit mechanisms are not well elucidated. Converging human and animal research has implicated th...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2025-01-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3002722 |
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| author | Dylan Patterson Nisma Khan Emily A Collins Norman R Stewart Kian Sassaninejad Dylan Yeates Andy C H Lee Rutsuko Ito |
| author_facet | Dylan Patterson Nisma Khan Emily A Collins Norman R Stewart Kian Sassaninejad Dylan Yeates Andy C H Lee Rutsuko Ito |
| author_sort | Dylan Patterson |
| collection | DOAJ |
| description | Successful resolution of approach-avoidance conflict (AAC) is fundamentally important for survival, and its dysregulation is a hallmark of many neuropsychiatric disorders, and yet the underlying neural circuit mechanisms are not well elucidated. Converging human and animal research has implicated the anterior/ventral hippocampus (vHPC) as a key node in arbitrating AAC in a region-specific manner. In this study, we sought to target the vHPC CA1 projection pathway to the nucleus accumbens (NAc) to delineate its contribution to AAC decision-making, particularly in the arbitration of learned reward and punishment signals, as well as innate signals. To this end, we used pathway-specific chemogenetics in male and female Long Evans rats to inhibit the NAc shell projecting vHPC CA1 neurons while rats underwent a test in which cues of positive and negative valence were presented concurrently to elicit AAC. Additional behavioral assays of social preference and memory, reward and punishment cue processing, anxiety, and novelty processing were administered to further interrogate the conditions under which the vCA1-NAc shell pathway is recruited. Chemogenetic inhibition of the vCA1-NAc shell circuit resulted in animals exhibiting increased decision-making time and avoidance bias specifically in the face of motivational conflict, as the same behavioral phenotype was absent in separate conditioned cue preference and avoidance tests. vCA1-NAc shell inhibition also led to a reduction in seeking social interaction with a novel rat but did not alter anxiety-like behaviors. The vCA1-NAc shell circuit is therefore critically engaged in biasing decisions to approach in the face of social novelty and approach-avoidance conflict. Dysregulation of this circuit could lead to the precipitation of addictive behaviors in substance abuse, or maladaptive avoidance in situations of approach-avoidance conflict. |
| format | Article |
| id | doaj-art-bc7ddce98a754218900d7edd543478f2 |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-bc7ddce98a754218900d7edd543478f22025-02-05T05:30:20ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-01-01231e300272210.1371/journal.pbio.3002722Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict.Dylan PattersonNisma KhanEmily A CollinsNorman R StewartKian SassaninejadDylan YeatesAndy C H LeeRutsuko ItoSuccessful resolution of approach-avoidance conflict (AAC) is fundamentally important for survival, and its dysregulation is a hallmark of many neuropsychiatric disorders, and yet the underlying neural circuit mechanisms are not well elucidated. Converging human and animal research has implicated the anterior/ventral hippocampus (vHPC) as a key node in arbitrating AAC in a region-specific manner. In this study, we sought to target the vHPC CA1 projection pathway to the nucleus accumbens (NAc) to delineate its contribution to AAC decision-making, particularly in the arbitration of learned reward and punishment signals, as well as innate signals. To this end, we used pathway-specific chemogenetics in male and female Long Evans rats to inhibit the NAc shell projecting vHPC CA1 neurons while rats underwent a test in which cues of positive and negative valence were presented concurrently to elicit AAC. Additional behavioral assays of social preference and memory, reward and punishment cue processing, anxiety, and novelty processing were administered to further interrogate the conditions under which the vCA1-NAc shell pathway is recruited. Chemogenetic inhibition of the vCA1-NAc shell circuit resulted in animals exhibiting increased decision-making time and avoidance bias specifically in the face of motivational conflict, as the same behavioral phenotype was absent in separate conditioned cue preference and avoidance tests. vCA1-NAc shell inhibition also led to a reduction in seeking social interaction with a novel rat but did not alter anxiety-like behaviors. The vCA1-NAc shell circuit is therefore critically engaged in biasing decisions to approach in the face of social novelty and approach-avoidance conflict. Dysregulation of this circuit could lead to the precipitation of addictive behaviors in substance abuse, or maladaptive avoidance in situations of approach-avoidance conflict.https://doi.org/10.1371/journal.pbio.3002722 |
| spellingShingle | Dylan Patterson Nisma Khan Emily A Collins Norman R Stewart Kian Sassaninejad Dylan Yeates Andy C H Lee Rutsuko Ito Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict. PLoS Biology |
| title | Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict. |
| title_full | Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict. |
| title_fullStr | Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict. |
| title_full_unstemmed | Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict. |
| title_short | Ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict. |
| title_sort | ventral hippocampus to nucleus accumbens shell circuit regulates approach decisions during motivational conflict |
| url | https://doi.org/10.1371/journal.pbio.3002722 |
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