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

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.

Unraveling the Role of Thyroid Hormones in Seasonal Neuroplasticity in European Starlings (Sturnus vulgaris)

“…In general both groups presented similar neuroplasticity changes, both in volume and diffusion parameters, starting during the photosensitive period, as thyroid hormones decline. In line with the prior longitudinal MRI study ( Orije et al, 2021a ), the FA value of several parts of the song motor pathway, anterior forebrain pathway but also visual system and molecular layer of the cerebellum increase gradually over time. Post-hoc linear mixed model analysis revealed subtle interactions over time between the different groups.…”

“…However, starlings have far less PNNs, compared to closed-ended learning zebra finches, suggesting that PNN might play less of a role in the control of seasonal neuroplasticity of open-ended learning starlings ( Cornez et al, 2017 ). Our prior studies suggested myelination rather than PNNs as another candidate mechanism that contributes to ending a sensitive window in open-ended learners like starlings ( Orije et al, 2021a ). In the control group, several tracts including OM, TrO and tFA increased in FA value upon photostimulation, due to decreased radial diffusivity, which implies an increase in myelination ( Song et al, 2002 , 2005 ; De Groof et al, 2008 ).…”

“…Our results further corroborate that cerebellar lobules VI-VII retain the neural substrate for song behavior. Furthermore, these parts of the cerebellum show seasonal neuroplasticity, both in male and female starlings ( Orije et al, 2021a ).…”

“…Once we had established the spatial and temporal expression patterns of thyroid hormone regulating genes (and thyroid hormone plasma levels) during different photoperiods, we induced hypothyroidism during the photosensitive and photostimulated stage to investigate the impact on song production and seasonal neuroplasticity using in vivo MRI. In a previous MRI study, we showed that seasonally increased neuroplasticity starts during the photosensitive period, which acts as a sensitive window for multisensory neuroplasticity as it shows involvement of the song control, visual and auditory system and even the cerebellum ( Orije et al, 2021a ). Furthermore, in vivo MRI is a powerful tool to study neural substrate changes associated with singing behavior or hormonal changes ( Hamaide et al, 2020 ; Orije et al, 2020 , 2021a ).…”

“…In a previous MRI study, we showed that seasonally increased neuroplasticity starts during the photosensitive period, which acts as a sensitive window for multisensory neuroplasticity as it shows involvement of the song control, visual and auditory system and even the cerebellum ( Orije et al, 2021a ). Furthermore, in vivo MRI is a powerful tool to study neural substrate changes associated with singing behavior or hormonal changes ( Hamaide et al, 2020 ; Orije et al, 2020 , 2021a ).…”