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A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds

Nature Neuroscience volume 15, pages 620–627 (2012)Cite this article

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Abstract

The pallido-recipient thalamus transmits information from the basal ganglia to the cortex and is critical for motor initiation and learning. Thalamic activity is strongly inhibited by pallidal inputs from the basal ganglia, but the role of nonpallidal inputs, such as excitatory inputs from cortex, remains unclear. We simultaneously recorded from presynaptic pallidal axon terminals and postsynaptic thalamocortical neurons in a basal ganglia–recipient thalamic nucleus that is necessary for vocal variability and learning in zebra finches. We found that song-locked rate modulations in the thalamus could not be explained by pallidal inputs alone and persisted following pallidal lesion. Instead, thalamic activity was likely driven by inputs from a motor cortical nucleus that is also necessary for singing. These findings suggest a role for cortical inputs to the pallido-recipient thalamus in driving premotor signals that are important for exploratory behavior and learning.

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Figure 1: Firing patterns of thalamic neurons and their pallidal inputs during singing.
Figure 2: Simultaneous recordings of pallidal axon terminal and putative post-synaptic thalamic neurons during singing.
Figure 3: Song-locked rate modulations in thalamic neurons are also observed after basal ganglia lesions.
Figure 4: Anatomical verification of the RA projection to DLM in juvenile birds.
Figure 5: RA stimulation activates DLM neurons.
Figure 6: Singing-related firing patterns of corticothalamic RA neurons projecting to DLM.

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Acknowledgements

We thank A. Graybiel and M. Farries for comments on the manuscript. This work was supported by grants from the US National Institutes of Health (R01DC009183 to M.S.F. and K99NS067062 to J.H.G.), and post-doctoral fellowships from the Charles King Trust and Damon Runyon Research Foundation.

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  1. Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

    Jesse H Goldberg & Michale S Fee

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  1. Jesse H Goldberg
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J.H.G. and M.S.F. designed the experiments and wrote the manuscript. J.H.G. conducted the experiments.

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Correspondence to Michale S Fee.

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Goldberg, J., Fee, M. A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds. Nat Neurosci 15, 620–627 (2012). https://doi.org/10.1038/nn.3047

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