Neurochemistry and circuit organization of the lateral spiriform nucleus of birds: A uniquely nonmammalian direct pathway component of the basal ganglia

Reiner A, Medina L, Abellan A, Deng Y, Toledo CAB, Luksch H, Vega Zuniga TA, Riley NB, Hodos W, Karten HJ. 2024. Neurochemistry and circuit organization of the lateral spiriform nucleus of birds: A uniquely nonmammalian direct pathway component of the basal ganglia. Journal of Comparative Neurology. 532(5), e25620.

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Author
Reiner, Anton; Medina, Loreta; Abellan, Antonio; Deng, Yunping; Toledo, Claudio A.B.; Luksch, Harald; Vega Zuniga, Tomas AISTA; Riley, Nell B.; Hodos, William; Karten, Harvey J.
Department
Abstract
We used diverse methods to characterize the role of avian lateral spiriform nucleus (SpL) in basal ganglia motor function. Connectivity analysis showed that SpL receives input from globus pallidus (GP), and the intrapeduncular nucleus (INP) located ventromedial to GP, whose neurons express numerous striatal markers. SpL-projecting GP neurons were large and aspiny, while SpL-projecting INP neurons were medium sized and spiny. Connectivity analysis further showed that SpL receives inputs from subthalamic nucleus (STN) and substantia nigra pars reticulata (SNr), and that the SNr also receives inputs from GP, INP, and STN. Neurochemical analysis showed that SpL neurons express ENK, GAD, and a variety of pallidal neuron markers, and receive GABAergic terminals, some of which also contain DARPP32, consistent with GP pallidal and INP striatal inputs. Connectivity and neurochemical analysis showed that the SpL input to tectum prominently ends on GABAA receptor-enriched tectobulbar neurons. Behavioral studies showed that lesions of SpL impair visuomotor behaviors involving tracking and pecking moving targets. Our results suggest that SpL modulates brainstem-projecting tectobulbar neurons in a manner comparable to the demonstrated influence of GP internus on motor thalamus and of SNr on tectobulbar neurons in mammals. Given published data in amphibians and reptiles, it seems likely the SpL circuit represents a major direct pathway-type circuit by which the basal ganglia exerts its motor influence in nonmammalian tetrapods. The present studies also show that avian striatum is divided into three spatially segregated territories with differing connectivity, a medial striato-nigral territory, a dorsolateral striato-GP territory, and the ventrolateral INP motor territory.
Publishing Year
Date Published
2024-05-01
Journal Title
Journal of Comparative Neurology
Acknowledgement
We gratefully thank Marion Joni, Tony Laverghetta, Sherry Cuthbertson, Gary Henderson, and Patricia Lindaman for technical assistance. The research presented here has been supported by NIH grants NS-16857, NS-19620, NS-28721, and EY-05298, and The Methodist Hospitals Endowed Professorship in Neuroscience (A. R.), by grant number 09/50623-9 from the Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (C. A. B. T.), by NIH grant EY-00735 (W. H.), and by NIH grants NS-12078 and EY-02145 (H. J. K.).
Volume
532
Issue
5
Article Number
e25620
ISSN
eISSN
IST-REx-ID

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Reiner A, Medina L, Abellan A, et al. Neurochemistry and circuit organization of the lateral spiriform nucleus of birds: A uniquely nonmammalian direct pathway component of the basal ganglia. Journal of Comparative Neurology. 2024;532(5). doi:10.1002/cne.25620
Reiner, A., Medina, L., Abellan, A., Deng, Y., Toledo, C. A. B., Luksch, H., … Karten, H. J. (2024). Neurochemistry and circuit organization of the lateral spiriform nucleus of birds: A uniquely nonmammalian direct pathway component of the basal ganglia. Journal of Comparative Neurology. Wiley. https://doi.org/10.1002/cne.25620
Reiner, Anton, Loreta Medina, Antonio Abellan, Yunping Deng, Claudio A.B. Toledo, Harald Luksch, Tomas A Vega Zuniga, Nell B. Riley, William Hodos, and Harvey J. Karten. “Neurochemistry and Circuit Organization of the Lateral Spiriform Nucleus of Birds: A Uniquely Nonmammalian Direct Pathway Component of the Basal Ganglia.” Journal of Comparative Neurology. Wiley, 2024. https://doi.org/10.1002/cne.25620.
A. Reiner et al., “Neurochemistry and circuit organization of the lateral spiriform nucleus of birds: A uniquely nonmammalian direct pathway component of the basal ganglia,” Journal of Comparative Neurology, vol. 532, no. 5. Wiley, 2024.
Reiner A, Medina L, Abellan A, Deng Y, Toledo CAB, Luksch H, Vega Zuniga TA, Riley NB, Hodos W, Karten HJ. 2024. Neurochemistry and circuit organization of the lateral spiriform nucleus of birds: A uniquely nonmammalian direct pathway component of the basal ganglia. Journal of Comparative Neurology. 532(5), e25620.
Reiner, Anton, et al. “Neurochemistry and Circuit Organization of the Lateral Spiriform Nucleus of Birds: A Uniquely Nonmammalian Direct Pathway Component of the Basal Ganglia.” Journal of Comparative Neurology, vol. 532, no. 5, e25620, Wiley, 2024, doi:10.1002/cne.25620.

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