Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum
Rhythmic brain activity is thought to reflect, and to help organize, spike activity in populations of neurons during on-going behavior. We report that during learning, a major transition occurs in task-related oscillatory activity in the ventromedial striatum, a striatal region related to motivation...
| Main Authors: | , , , , |
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| Other Authors: | |
| Format: | Article |
| Language: | en_US |
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National Academy of Sciences (U.S.)
2012
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| Online Access: | http://hdl.handle.net/1721.1/70923 https://orcid.org/0000-0002-4326-7720 |
| _version_ | 1811069025416904704 |
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| author | Howe, Mark William Atallah, Hicham McCool, Andrew D. Gibson, Daniel J. Graybiel, Ann M. |
| author2 | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences |
| author_facet | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Howe, Mark William Atallah, Hicham McCool, Andrew D. Gibson, Daniel J. Graybiel, Ann M. |
| author_sort | Howe, Mark William |
| collection | MIT |
| description | Rhythmic brain activity is thought to reflect, and to help organize, spike activity in populations of neurons during on-going behavior. We report that during learning, a major transition occurs in task-related oscillatory activity in the ventromedial striatum, a striatal region related to motivation-dependent learning. Early on as rats learned a T-maze task, bursts of 70- to 90-Hz high-γ activity were prominent during T-maze runs, but these gradually receded as bursts of 15- to 28-Hz β-band activity became pronounced. Populations of simultaneously recorded neurons synchronized their spike firing similarly during both the high-γ–band and β-band bursts. Thus, the structure of spike firing was reorganized during learning in relation to different rhythms. Spiking was concentrated around the troughs of the β-oscillations for fast-spiking interneurons and around the peaks for projection neurons, indicating alternating periods of firing at different frequencies as learning progressed. Spike-field synchrony was primarily local during high-γ–bursts but was widespread during β-bursts. The learning-related shift in the probability of high-γ and β-bursting thus could reflect a transition from a mainly focal rhythmic inhibition during early phases of learning to a more distributed mode of rhythmic inhibition as learning continues and behavior becomes habitual. These dynamics could underlie changing functions of the ventromedial striatum during habit formation. More generally, our findings suggest that coordinated changes in the spatiotemporal relationships of local field potential oscillations and spike activity could be hallmarks of the learning process. |
| first_indexed | 2024-09-23T08:04:31Z |
| format | Article |
| id | mit-1721.1/70923 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T08:04:31Z |
| publishDate | 2012 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/709232022-09-30T07:17:41Z Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum Howe, Mark William Atallah, Hicham McCool, Andrew D. Gibson, Daniel J. Graybiel, Ann M. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Graybiel, Ann M. Graybiel, Ann M. Howe, Mark William Atallah, Hicham McCool, Andrew D. Gibson, Daniel J. Rhythmic brain activity is thought to reflect, and to help organize, spike activity in populations of neurons during on-going behavior. We report that during learning, a major transition occurs in task-related oscillatory activity in the ventromedial striatum, a striatal region related to motivation-dependent learning. Early on as rats learned a T-maze task, bursts of 70- to 90-Hz high-γ activity were prominent during T-maze runs, but these gradually receded as bursts of 15- to 28-Hz β-band activity became pronounced. Populations of simultaneously recorded neurons synchronized their spike firing similarly during both the high-γ–band and β-band bursts. Thus, the structure of spike firing was reorganized during learning in relation to different rhythms. Spiking was concentrated around the troughs of the β-oscillations for fast-spiking interneurons and around the peaks for projection neurons, indicating alternating periods of firing at different frequencies as learning progressed. Spike-field synchrony was primarily local during high-γ–bursts but was widespread during β-bursts. The learning-related shift in the probability of high-γ and β-bursting thus could reflect a transition from a mainly focal rhythmic inhibition during early phases of learning to a more distributed mode of rhythmic inhibition as learning continues and behavior becomes habitual. These dynamics could underlie changing functions of the ventromedial striatum during habit formation. More generally, our findings suggest that coordinated changes in the spatiotemporal relationships of local field potential oscillations and spike activity could be hallmarks of the learning process. National Institutes of Health (U.S.) (Grant R01 MH060379) Mark Gorenberg Graduate Student Fellowship Award 2012-05-24T15:34:06Z 2012-05-24T15:34:06Z 2011-10 2011-08 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/70923 Howe, M. W. et al. “Habit Learning Is Associated with Major Shifts in Frequencies of Oscillatory Activity and Synchronized Spike Firing in Striatum.” Proceedings of the National Academy of Sciences 108.40 (2011): 16801–16806. Web. https://orcid.org/0000-0002-4326-7720 en_US http://dx.doi.org/10.1073/pnas.1113158108 Proceedings of the National Academy of Sciences of the United States of America Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Howe, Mark William Atallah, Hicham McCool, Andrew D. Gibson, Daniel J. Graybiel, Ann M. Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| title | Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| title_full | Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| title_fullStr | Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| title_full_unstemmed | Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| title_short | Habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| title_sort | habit learning is associated with major shifts in frequencies of oscillatory activity and synchronized spike firing in striatum |
| url | http://hdl.handle.net/1721.1/70923 https://orcid.org/0000-0002-4326-7720 |
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