Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior
Habit formation is a behavioral adaptation that automates routine actions. Habitual behavior correlates with broad reconfigurations of dorsolateral striatal (DLS) circuit properties that increase gain and shift pathway timing. The mechanism(s) for these circuit adaptations are unknown and could be r...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-09-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/26231 |
| _version_ | 1828376216492572672 |
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| author | Justin K O'Hare Haofang Li Namsoo Kim Erin Gaidis Kristen Ade Jeff Beck Henry Yin Nicole Calakos |
| author_facet | Justin K O'Hare Haofang Li Namsoo Kim Erin Gaidis Kristen Ade Jeff Beck Henry Yin Nicole Calakos |
| author_sort | Justin K O'Hare |
| collection | DOAJ |
| description | Habit formation is a behavioral adaptation that automates routine actions. Habitual behavior correlates with broad reconfigurations of dorsolateral striatal (DLS) circuit properties that increase gain and shift pathway timing. The mechanism(s) for these circuit adaptations are unknown and could be responsible for habitual behavior. Here we find that a single class of interneuron, fast-spiking interneurons (FSIs), modulates all of these habit-predictive properties. Consistent with a role in habits, FSIs are more excitable in habitual mice compared to goal-directed and acute chemogenetic inhibition of FSIs in DLS prevents the expression of habitual lever pressing. In vivo recordings further reveal a previously unappreciated selective modulation of SPNs based on their firing patterns; FSIs inhibit most SPNs but paradoxically promote the activity of a subset displaying high fractions of gamma-frequency spiking. These results establish a microcircuit mechanism for habits and provide a new example of how interneurons mediate experience-dependent behavior. |
| first_indexed | 2024-04-14T07:56:34Z |
| format | Article |
| id | doaj.art-3c600e84e8f64b2f932ef2a8bf66d748 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:56:34Z |
| publishDate | 2017-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-3c600e84e8f64b2f932ef2a8bf66d7482022-12-22T02:05:01ZengeLife Sciences Publications LtdeLife2050-084X2017-09-01610.7554/eLife.26231Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behaviorJustin K O'Hare0https://orcid.org/0000-0002-7363-6064Haofang Li1Namsoo Kim2Erin Gaidis3Kristen Ade4Jeff Beck5Henry Yin6Nicole Calakos7https://orcid.org/0000-0002-9918-3294Department of Neurobiology, Duke University Medical Center, Durham, United States; Department of Neurology, Duke University Medical Center, Durham, United StatesDepartment of Psychology and Neuroscience, Duke University, Durham, United StatesDepartment of Psychology and Neuroscience, Duke University, Durham, United StatesDepartment of Psychology and Neuroscience, Duke University, Durham, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United States; Department of Neurology, Duke University Medical Center, Durham, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United StatesDepartment of Psychology and Neuroscience, Duke University, Durham, United StatesDepartment of Neurobiology, Duke University Medical Center, Durham, United States; Department of Neurology, Duke University Medical Center, Durham, United StatesHabit formation is a behavioral adaptation that automates routine actions. Habitual behavior correlates with broad reconfigurations of dorsolateral striatal (DLS) circuit properties that increase gain and shift pathway timing. The mechanism(s) for these circuit adaptations are unknown and could be responsible for habitual behavior. Here we find that a single class of interneuron, fast-spiking interneurons (FSIs), modulates all of these habit-predictive properties. Consistent with a role in habits, FSIs are more excitable in habitual mice compared to goal-directed and acute chemogenetic inhibition of FSIs in DLS prevents the expression of habitual lever pressing. In vivo recordings further reveal a previously unappreciated selective modulation of SPNs based on their firing patterns; FSIs inhibit most SPNs but paradoxically promote the activity of a subset displaying high fractions of gamma-frequency spiking. These results establish a microcircuit mechanism for habits and provide a new example of how interneurons mediate experience-dependent behavior.https://elifesciences.org/articles/26231habitstriatumfast-spiking interneuron |
| spellingShingle | Justin K O'Hare Haofang Li Namsoo Kim Erin Gaidis Kristen Ade Jeff Beck Henry Yin Nicole Calakos Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior eLife habit striatum fast-spiking interneuron |
| title | Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior |
| title_full | Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior |
| title_fullStr | Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior |
| title_full_unstemmed | Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior |
| title_short | Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior |
| title_sort | striatal fast spiking interneurons selectively modulate circuit output and are required for habitual behavior |
| topic | habit striatum fast-spiking interneuron |
| url | https://elifesciences.org/articles/26231 |
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