Morphological characterization of HVC projection neurons in the zebra finch (Taeniopygia guttata)

Sam E. Benezra; Rajeevan T. Narayanan; Robert Egger; Marcel Oberlaender; Michael A. Long

doi:10.1002/cne.24437

Morphological characterization of HVC projection neurons in the zebra finch (Taeniopygia guttata)

Sam E. Benezra, Rajeevan T. Narayanan, Robert Egger, Marcel Oberlaender, Michael A. Long

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Singing behavior in the adult male zebra finch is dependent upon the activity of a cortical region known as HVC (proper name). The vast majority of HVC projection neurons send primary axons to either the downstream premotor nucleus RA (robust nucleus of the arcopallium, or primary motor cortex) or Area X (basal ganglia), which play important roles in song production or song learning, respectively. In addition to these long-range outputs, HVC neurons also send local axon collaterals throughout that nucleus. Despite their implications for a range of circuit models, these local processes have never been completely reconstructed. Here, we use in vivo single-neuron Neurobiotin fills to examine 40 projection neurons across 31 birds with somatic positions distributed across HVC. We show that HVC(RA) and HVC(X) neurons have categorically distinct dendritic fields. Additionally, these cell classes send axon collaterals that are either restricted to a small portion of HVC (“local neurons”) or broadly distributed throughout the entire nucleus (“broadcast neurons”). Overall, these processes within HVC offer a structural basis for significant local processing underlying behaviorally relevant population activity.

Original language	English
Pages (from-to)	1673-1689
Journal	Journal of Comparative Neurology
Volume	526
Issue number	10
DOIs	https://doi.org/10.1002/cne.24437
Publication status	Published - 1 Jul 2018
Externally published	Yes

Funding

This research was supported by the NIH (R01NS075044) (M.L.), the New York Stem Cell Foundation (M.L.), the Rita Allen Foundation (M.L.), Simons Foundation (Global Brain Initiative) (M.L.), the German Research Foundation (DFG) EG 401/1-1 (R.E.), EMBO ALTF 348– 2017 (R.E.), the Center of Advanced European Studies and Research (caesar, M.O.), the Max Planck Institute for Biological Cybernetics (M.O.), the Bernstein Center for Computational Neuroscience, funded by German Federal Ministry of Education and Research Grant BMBF/FKZ 01GQ1002 (M.O.), and the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No 633428) (M.O.). We thank Madeleine Junkins for technical assistance and Margot Elma-leh, Elnaz Hozhabri, and Kalman Katlowitz for comments on earlier versions of this manuscript. This research was supported by the NIH (R01NS075044) (M.L.), the New York Stem Cell Foundation (M.L.), the Rita Allen Foundation (M.L.), Simons Foundation (Global Brain Initiative) (M.L.), the German Research Foundation (DFG) EG 401/1-1 (R.E.), EMBO ALTF 348–2017 (R.E.), the Center of Advanced European Studies and Research (caesar, M.O.), the Max Planck Institute for Biological Cybernetics (M.O.), the Bernstein Center for Computational Neuroscience, funded by German Federal Ministry of Education and Research Grant BMBF/FKZ 01GQ1002 (M.O.), and the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation program (grant agreement No 633428) (M.O.). We thank Madeleine Junkins for technical assistance and Margot Elmaleh, Elnaz Hozhabri, and Kalman Katlowitz for comments on earlier versions of this manuscript.

Funders	Funder number
Center of Advanced European Studies and Research
Max Planck Institute for Biological Cybernetics
National Institutes of Health
National Institute of Neurological Disorders and Stroke	R01NS075044
Simons Foundation
Rita Allen Foundation
New York Stem Cell Foundation
European Molecular Biology Organization	ALTF 348– 2017
California Department of Fish and Game
Horizon 2020 Framework Programme
European Research Council
Deutsche Forschungsgemeinschaft	EG 401/1-1
Bundesministerium für Bildung und Forschung	BMBF/FKZ 01GQ1002
Horizon 2020	633428

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title = "Morphological characterization of HVC projection neurons in the zebra finch (Taeniopygia guttata)",

abstract = "Singing behavior in the adult male zebra finch is dependent upon the activity of a cortical region known as HVC (proper name). The vast majority of HVC projection neurons send primary axons to either the downstream premotor nucleus RA (robust nucleus of the arcopallium, or primary motor cortex) or Area X (basal ganglia), which play important roles in song production or song learning, respectively. In addition to these long-range outputs, HVC neurons also send local axon collaterals throughout that nucleus. Despite their implications for a range of circuit models, these local processes have never been completely reconstructed. Here, we use in vivo single-neuron Neurobiotin fills to examine 40 projection neurons across 31 birds with somatic positions distributed across HVC. We show that HVC(RA) and HVC(X) neurons have categorically distinct dendritic fields. Additionally, these cell classes send axon collaterals that are either restricted to a small portion of HVC (“local neurons”) or broadly distributed throughout the entire nucleus (“broadcast neurons”). Overall, these processes within HVC offer a structural basis for significant local processing underlying behaviorally relevant population activity.",

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AU - Oberlaender, Marcel

AU - Long, Michael A.

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N2 - Singing behavior in the adult male zebra finch is dependent upon the activity of a cortical region known as HVC (proper name). The vast majority of HVC projection neurons send primary axons to either the downstream premotor nucleus RA (robust nucleus of the arcopallium, or primary motor cortex) or Area X (basal ganglia), which play important roles in song production or song learning, respectively. In addition to these long-range outputs, HVC neurons also send local axon collaterals throughout that nucleus. Despite their implications for a range of circuit models, these local processes have never been completely reconstructed. Here, we use in vivo single-neuron Neurobiotin fills to examine 40 projection neurons across 31 birds with somatic positions distributed across HVC. We show that HVC(RA) and HVC(X) neurons have categorically distinct dendritic fields. Additionally, these cell classes send axon collaterals that are either restricted to a small portion of HVC (“local neurons”) or broadly distributed throughout the entire nucleus (“broadcast neurons”). Overall, these processes within HVC offer a structural basis for significant local processing underlying behaviorally relevant population activity.

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Morphological characterization of HVC projection neurons in the zebra finch (Taeniopygia guttata)

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