The photosensitive phase acts as a sensitive window for seasonal multisensory neuroplasticity in male and female starlings

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    Evaluation Summary:

    This paper will be of interest to a diverse range of scientist as the questions span animal behavior, neuroscience and sex differences in brain-behavior relations. The study used non-invasive brain imaging to track large changes in structures involved in controlling communication between brain regions. The data reveal exciting sex-specific changes in key brain regions involved in learning and memory. The study is well designed, and the key claims of the manuscript appear to be well supported by the data. The imaging approaches employed are thoughtful and rigorous.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

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Abstract

Traditionally, research unraveling seasonal neuroplasticity in songbirds has focused on the male song control system and testosterone. We longitudinally monitored the song and neuroplasticity in male and female starlings during multiple photoperiods using Diffusion Tensor and Fixel-Based techniques. These exploratory data-driven whole-brain methods resulted in a population-based tractogram uncovering microstructural sexual dimorphisms in the song control system and beyond. Male brains showed microstructural hemispheric asymmetries, whereas females had higher interhemispheric connectivity, which could not be attributed to brain size differences. Only females with large brains sing but differ from males in their song behavior by showing involvement of the hippocampus. Both sexes experienced multisensory neuroplasticity in the song control, auditory and visual system, and the cerebellum, mainly during the photosensitive period. This period with low gonadal hormones might represent a ‘sensitive window’ during which different sensory and motor systems in telencephalon and cerebellum can be seasonally re-shaped in both sexes.

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  1. Author Response:

    Reviewer #1:

    The manuscript by Jasmien Orije and colleagues has used advanced Diffusion Tensor and Fixel-Based brain imaging methods to examine brain plasticity in male and female European starlings. Songbirds provide a unique animal model to interrogate how the brain controls a complex, learned behaviour: song. The authors used DT imaging to identify known and uncover new structural changes in grey and white matter in male and female brains. The choice of the European starling as a model songbird was smart as this bird has a larger brain to facilitate anatomical localization, clear sex differences in song behavior and well-characterized photoperiod-induced changes in reproductive state. The authors are commended for using both male and female starlings. The photoperiodic treatment used was optimal to capture the key …

  2. Evaluation Summary:

    This paper will be of interest to a diverse range of scientist as the questions span animal behavior, neuroscience and sex differences in brain-behavior relations. The study used non-invasive brain imaging to track large changes in structures involved in controlling communication between brain regions. The data reveal exciting sex-specific changes in key brain regions involved in learning and memory. The study is well designed, and the key claims of the manuscript appear to be well supported by the data. The imaging approaches employed are thoughtful and rigorous.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their names with the authors.)

  3. Reviewer #1 (Public Review):

    The manuscript by Jasmien Orije and colleagues has used advanced Diffusion Tensor and Fixel-Based brain imaging methods to examine brain plasticity in male and female European starlings. Songbirds provide a unique animal model to interrogate how the brain controls a complex, learned behaviour: song. The authors used DT imaging to identify known and uncover new structural changes in grey and white matter in male and female brains. The choice of the European starling as a model songbird was smart as this bird has a larger brain to facilitate anatomical localization, clear sex differences in song behavior and well-characterized photoperiod-induced changes in reproductive state. The authors are commended for using both male and female starlings. The photoperiodic treatment used was optimal to capture the key …

  4. Reviewer #2 (Public Review):

    Orije et al. employed diffusion weighted imaging to longitudinally monitor the plasticity of the song control system during multiple photoperiods in male and female starlings. The authors found that both sexes experience similar seasonal neuroplasticity in multisensory systems and cerebellum during the photosensitive phase. The authors' findings are convincing and rely on a set of well-designed longitudinal investigations encompassing previously validated imaging methods. The authors' identification of a putative sensitive window during which sensory and motor systems can be seasonally re-shaped in both sexes is an interesting finding that advances our understanding of the neural basis of seasonal structural neuroplasticity in songbirds.

    Overall, this is a strong paper whose major strengths are:

    1. The …

  5. Reviewer #3 (Public Review):

    In their paper, Orije et al used MRI imaging to study sexual dimorphisms in brains of European starlings during multiple photoperiods and how this seasonal neuroplasticity is dependent in brain size, song rates and hormonal levels. The authors main findings include difference in hemispheric asymmetries between the sexes, multisensory neuroplasticity in the song control system and beyond it in both sexes and some dependence of singing behavior in females with large brains. The authors use different methods to quantify the changes in the MRI data to support various possible mechanisms that could be the basis of the differences they see. They also record the birds' song rates and hormonal levels to correlate the neural findings with biological relevant variables.

    The analysis is very impressive, taking into …