Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments

The songbird area X is a basal ganglia homolog that contains two pallidal cell types—local neurons that project within the basal ganglia and output neurons that project to the thalamus. Based on these projections, it has been proposed that these classes are structurally homologous to the primate ext...

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Main Authors: Goldberg, Jesse H., Adler, Avital, Bergman, Hagai, Fee, Michale S.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: Society for Neuroscience 2012
Online Access:http://hdl.handle.net/1721.1/70504
https://orcid.org/0000-0001-7539-1745
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author Goldberg, Jesse H.
Adler, Avital
Bergman, Hagai
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
Goldberg, Jesse H.
Adler, Avital
Bergman, Hagai
Fee, Michale S.
author_sort Goldberg, Jesse H.
collection MIT
description The songbird area X is a basal ganglia homolog that contains two pallidal cell types—local neurons that project within the basal ganglia and output neurons that project to the thalamus. Based on these projections, it has been proposed that these classes are structurally homologous to the primate external (GPe) and internal (GPi) pallidal segments. To test the hypothesis that the two area X pallidal types are functionally homologous to GPe and GPi neurons, we recorded from neurons in area X of singing juvenile male zebra finches, and directly compared their firing patterns to neurons recorded in the primate pallidus. In area X, we found two cell classes that exhibited high firing (HF) rates (>60 Hz) characteristic of pallidal neurons. HF-1 neurons, like most GPe neurons we examined, exhibited large firing rate modulations, including bursts and long pauses. In contrast, HF-2 neurons, like GPi neurons, discharged continuously without bursts or long pauses. To test whether HF-2 neurons were the output neurons that project to the thalamus, we next recorded directly from pallidal axon terminals in thalamic nucleus DLM, and found that all terminals exhibited singing-related firing patterns indistinguishable from HF-2 neurons. Our data show that singing-related neural activity distinguishes two putative pallidal cell types in area X: thalamus-projecting neurons that exhibit activity similar to the primate GPi, and non-thalamus-projecting neurons that exhibit activity similar to the primate GPe. These results suggest that song learning in birds and motor learning in mammals use conserved basal ganglia signaling strategies.
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spelling mit-1721.1/705042022-09-26T10:59:56Z Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments Goldberg, Jesse H. Adler, Avital Bergman, Hagai Fee, Michale S. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Fee, Michale S. Goldberg, Jesse H. Fee, Michale S. The songbird area X is a basal ganglia homolog that contains two pallidal cell types—local neurons that project within the basal ganglia and output neurons that project to the thalamus. Based on these projections, it has been proposed that these classes are structurally homologous to the primate external (GPe) and internal (GPi) pallidal segments. To test the hypothesis that the two area X pallidal types are functionally homologous to GPe and GPi neurons, we recorded from neurons in area X of singing juvenile male zebra finches, and directly compared their firing patterns to neurons recorded in the primate pallidus. In area X, we found two cell classes that exhibited high firing (HF) rates (>60 Hz) characteristic of pallidal neurons. HF-1 neurons, like most GPe neurons we examined, exhibited large firing rate modulations, including bursts and long pauses. In contrast, HF-2 neurons, like GPi neurons, discharged continuously without bursts or long pauses. To test whether HF-2 neurons were the output neurons that project to the thalamus, we next recorded directly from pallidal axon terminals in thalamic nucleus DLM, and found that all terminals exhibited singing-related firing patterns indistinguishable from HF-2 neurons. Our data show that singing-related neural activity distinguishes two putative pallidal cell types in area X: thalamus-projecting neurons that exhibit activity similar to the primate GPi, and non-thalamus-projecting neurons that exhibit activity similar to the primate GPe. These results suggest that song learning in birds and motor learning in mammals use conserved basal ganglia signaling strategies. National Institutes of Health (U.S.) (Grant R01DC009183) Damon Runyon Cancer Research Foundation (Fellowship) Medical Foundation, inc. (Health Resources in Action, Charles A. King Trust Postdoctoral Research Fellowship Program) 2012-05-04T16:49:42Z 2012-05-04T16:49:42Z 2010-05 2010-03 Article http://purl.org/eprint/type/JournalArticle 0270-6474 1529-2401 http://hdl.handle.net/1721.1/70504 Goldberg, J. H. et al. “Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments.” Journal of Neuroscience 30.20 (2010): 7088–7098. Web.© 2010 by the Society for Neuroscience. https://orcid.org/0000-0001-7539-1745 en_US http://dx.doi.org/10.1523/jneurosci.0168-10.2010 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 Goldberg, Jesse H.
Adler, Avital
Bergman, Hagai
Fee, Michale S.
Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments
title Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments
title_full Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments
title_fullStr Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments
title_full_unstemmed Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments
title_short Singing-Related Neural Activity Distinguishes Two Putative Pallidal Cell Types in the Songbird Basal Ganglia: Comparison to the Primate Internal and External Pallidal Segments
title_sort singing related neural activity distinguishes two putative pallidal cell types in the songbird basal ganglia comparison to the primate internal and external pallidal segments
url http://hdl.handle.net/1721.1/70504
https://orcid.org/0000-0001-7539-1745
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