Lesions in a songbird vocal circuit increase variability in song syntax

  1. Institute for Neurobiology, University of Tübingen, Germany
  2. Center for Integrative Neuroscience, University of California, San Francisco, USA and Howard Hughes Medical Institute
  3. Departments of Horticulture and Integrative Biology, Oregon State University, Corvallis, OR
  4. Department of Clinical Research, Noctrix Health, Inc., Pleasanton, CA

Peer review process

Not revised: This Reviewed Preprint includes the authors’ original preprint (without revision), an eLife assessment, and public reviews.

Read more about eLife’s peer review process.

Editors

  • Reviewing Editor
    Jesse Goldberg
    Cornell University, Ithaca, United States of America
  • Senior Editor
    Andrew King
    University of Oxford, Oxford, United Kingdom

Reviewer #1 (Public Review):

Summary:

Songbirds provide a tractable system to examine neural mechanisms of sequence generation and variability. In past work, the projection from LMAN to RA (output of the anterior forebrain pathway) was shown to be critical for driving vocal variability during babbling, learning, and adulthood. LMAN is immediately adjacent to MMAN, which projects to HVC. MMAN is less well understood but, anatomically, appears to resemble LMAN in that it is the cortical output of a BG-thalamocortical loop. Because it projects to HVC, a major sequence generator for both syllable phonology and sequence, a strong prediction would be that MMAN drives sequence variability in the same way that LMAN drives phonological variability. This hypothesis predicts that MMAN lesions in a Bengalese finch would reduce sequence variability. Here, the authors test this hypothesis. They provide a surprising and important result that is well motivated and well analyzed: MMAN lesions increase sequence variability - this is exactly the opposite result from what would be predicted based on the functions of LMAN.

Strengths:

1. A very important and surprising result shows that lesions of a frontal projection from MMAN to HVC, a sequence generator for birdsong, increase syntactical variability.

2. The choice of Bengalese finches, which have complex transition structures, to examine the mechanisms of sequence generation, enabled this important discovery.

3. The idea that frontal outputs of BG-cortical loops can generate vocal variability comes from lesions/inactivations of a parallel pathway from LMAN to RA. The difference between MMAN and LMAN functions is striking and important.

Weaknesses:

1. If more attention was paid to how syllable phonology was (or was not) affected by MMAN lesions then the claims could be stronger around the specific effects on sequence.

Reviewer #2 (Public Review):

Summary:

This study investigates the neural substrates of syntax variation in Bengalese finch songs. Here, the authors tested the effects of bilateral lesions of mMAN, a brain area with inputs to HVC, a premotor area required for song production. Lesions in mMAN induce variability in syntactic elements of song specifically through increased transition entropy, variability within stereotyped song elements known as chunks, and increases in the repeat number of individual syllables. These results suggest that mMAN projections to HVC contribute to multiple aspects of song syntax in the Bengalese finch. Overall the experiments are well-designed, the analysis excellent, and the results are of high interest.

Strengths:

The study identifies a novel role for mMAN, the medial magnocellular nucleus of the anterior nidopallium, in the control of syntactic variation within adult Bengalese finch song. This is of particular interest as multiple studies previously demonstrated that mMAN lesions do not affect song structure in zebra finches. The study undertakes a thorough analysis to characterise specific aspects of variability within the song of lesioned animals. The conclusions are well supported by the data.

Weaknesses:

The study would benefit from additional mechanistic information. A more fine-grained or reversible manipulation, such as brain cooling, might allow additional insights into how mMAN influences specific aspects of syntax structure. Are repeat number increases and transition entropy resulting from shared mechanisms within mMAN, or perhaps arising from differential output to downstream pathways (i.e. projections to HVC)? Similarly, unilateral manipulations would allow the authors to further test the hypothesis that mMAN is involved in inter-hemispheric synchronization.

  1. Howard Hughes Medical Institute
  2. Wellcome Trust
  3. Max-Planck-Gesellschaft
  4. Knut and Alice Wallenberg Foundation