Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds
Accurate timing is a critical aspect of motor control, yet the temporal structure of many mature behaviors emerges during learning from highly variable exploratory actions. How does a developing brain acquire the precise control of timing in behavioral sequences? To investigate the development of ti...
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| Format: | Article |
| Language: | en_US |
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Society for Neuroscience
2012
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| Online Access: | http://hdl.handle.net/1721.1/73131 https://orcid.org/0000-0001-7539-1745 |
| _version_ | 1826200968672313344 |
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| author | Aronov, Dmitriy Veit, Lena Goldberg, Jesse H. Fee, Michale S. |
| author2 | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences |
| author_facet | Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Aronov, Dmitriy Veit, Lena Goldberg, Jesse H. Fee, Michale S. |
| author_sort | Aronov, Dmitriy |
| collection | MIT |
| description | Accurate timing is a critical aspect of motor control, yet the temporal structure of many mature behaviors emerges during learning from highly variable exploratory actions. How does a developing brain acquire the precise control of timing in behavioral sequences? To investigate the development of timing, we analyzed the songs of young juvenile zebra finches. These highly variable vocalizations, akin to human babbling, gradually develop into temporally stereotyped adult songs. We find that the durations of syllables and silences in juvenile singing are formed by a mixture of two distinct modes of timing: a random mode producing broadly distributed durations early in development, and a stereotyped mode underlying the gradual emergence of stereotyped durations. Using lesions, inactivations, and localized brain cooling, we investigated the roles of neural dynamics within two premotor cortical areas in the production of these temporal modes. We find that LMAN (lateral magnocellular nucleus of the nidopallium) is required specifically for the generation of the random mode of timing and that mild cooling of LMAN causes an increase in the durations produced by this mode. On the contrary, HVC (used as a proper name) is required specifically for producing the stereotyped mode of timing, and its cooling causes a slowing of all stereotyped components. These results show that two neural pathways contribute to the timing of juvenile songs and suggest an interesting organization in the forebrain, whereby different brain areas are specialized for the production of distinct forms of neural dynamics. |
| first_indexed | 2024-09-23T11:44:33Z |
| format | Article |
| id | mit-1721.1/73131 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T11:44:33Z |
| publishDate | 2012 |
| publisher | Society for Neuroscience |
| record_format | dspace |
| spelling | mit-1721.1/731312022-09-27T21:35:13Z Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds Aronov, Dmitriy Veit, Lena Goldberg, Jesse H. Fee, Michale S. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Aronov, Dmitriy Veit, Lena Goldberg, Jesse H. Fee, Michale S. Accurate timing is a critical aspect of motor control, yet the temporal structure of many mature behaviors emerges during learning from highly variable exploratory actions. How does a developing brain acquire the precise control of timing in behavioral sequences? To investigate the development of timing, we analyzed the songs of young juvenile zebra finches. These highly variable vocalizations, akin to human babbling, gradually develop into temporally stereotyped adult songs. We find that the durations of syllables and silences in juvenile singing are formed by a mixture of two distinct modes of timing: a random mode producing broadly distributed durations early in development, and a stereotyped mode underlying the gradual emergence of stereotyped durations. Using lesions, inactivations, and localized brain cooling, we investigated the roles of neural dynamics within two premotor cortical areas in the production of these temporal modes. We find that LMAN (lateral magnocellular nucleus of the nidopallium) is required specifically for the generation of the random mode of timing and that mild cooling of LMAN causes an increase in the durations produced by this mode. On the contrary, HVC (used as a proper name) is required specifically for producing the stereotyped mode of timing, and its cooling causes a slowing of all stereotyped components. These results show that two neural pathways contribute to the timing of juvenile songs and suggest an interesting organization in the forebrain, whereby different brain areas are specialized for the production of distinct forms of neural dynamics. National Institutes of Health (U.S.) (Grant R01DC009183) Fannie and John Hertz Foundation (Silvio Micali Fellowship) 2012-09-24T19:04:14Z 2012-09-24T19:04:14Z 2011-11 2011-09 Article http://purl.org/eprint/type/JournalArticle 0270-6474 1529-2401 http://hdl.handle.net/1721.1/73131 Aronov, D. et al. “Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds.” Journal of Neuroscience 31.45 (2011): 16353–16368. Web. https://orcid.org/0000-0001-7539-1745 en_US http://dx.doi.org/10.1523/jneurosci.3009-11.2011 Journal of Neuroscience 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 Society for Neuroscience SFN |
| spellingShingle | Aronov, Dmitriy Veit, Lena Goldberg, Jesse H. Fee, Michale S. Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds |
| title | Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds |
| title_full | Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds |
| title_fullStr | Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds |
| title_full_unstemmed | Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds |
| title_short | Two Distinct Modes of Forebrain Circuit Dynamics Underlie Temporal Patterning in the Vocalizations of Young Songbirds |
| title_sort | two distinct modes of forebrain circuit dynamics underlie temporal patterning in the vocalizations of young songbirds |
| url | http://hdl.handle.net/1721.1/73131 https://orcid.org/0000-0001-7539-1745 |
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