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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Bibliographic Details
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
Description
Summary: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.