Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches

by K. Hamaguchi, K. Tschida, I. Yoon, B. R. Donald, and R. Mooney
Duke University

eLife 2014;e01833.

Summary: Whenever we speak, sing, or play a musical instrument, we use auditory feedback to fine-tune our movements to achieve the sound that we want. This same process is used by songbirds to learn and maintain their songs. As juvenile birds practice singing, they compare their vocalizations with their father's song, which they will previously have stored in memory, and continually tweak their own song until the two versions match.

It has been suggested that auditory feedback is integrated with song motor commands--the instructions from the brain to move the muscles required for singing--in a region of the songbird brain called the song premotor nucleus HVC. The structure of certain neurons in this region, known as HVCx cells, rapidly changes when a bird is deafened, which suggests that these HVCx cells detect auditory feedback.

We tested this idea by using fine electrodes to record the signals in HVCx cells in male zebra finches as they sang. The cells changed their activity patterns whenever the birds changed their vocalizations. By contrast, these patterns did not change when the birds heard a distorted version of their own song played back to them as they sang. This suggests that HVCx cells are insensitive to auditory feedback, and that they mainly encode song motor commands instead.

If HVCx cells don't detect feedback, then why does deafening affect them? HVCx cells send signals indirectly to a brain region called the LMAN (which is short for the lateral magnocellular nucleus of the anterior nidopallium). Normally, if a bird becomes deaf, the quality of their song begins to deteriorate, but this deterioration can be prevented by destroying the LMAN. We used high resolution imaging to show that destroying the LMAN also prevents deafening from altering the structure of HVCx cells. Again, this suggests that auditory feedback is not relayed from the HVC to the LMAN; instead the flow of information is in the opposite direction.

This surprising finding--namely, that HVCx cells do not integrate auditory feedback and song motor commands--raises the question of which brain region is in fact responsible for this process. Further experiments will be required to identify the underlying circuitry in the brains of songbirds.

DOI: 10.7554/eLife.01833.002

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