Uncovering a ‘sensitive window’ of multisensory and motor neuroplasticity in the cerebrum and cerebellum of 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 behavior 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 confirming microstructural sexual dimorphisms in the song control system. Furthermore, male brains showed hemispheric asymmetries in the pallium, 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 cerebellum, mainly during the photosensitive period. This period with low gonadal hormone levels might represent a 'sensitive window' during which different sensory and motor systems in the cerebrum and cerebellum can be seasonally re-shaped in both sexes.

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

“…The photorefractory period depends on thyroid hormones to prevent reproductive maturation in response to long day length ( Nicholls et al, 1988 ). The photoperiodic changes in song control nuclei are not exclusive to male starlings, also female starlings experience seasonal changes in song behavior, which have been associated to seasonal changes in song control nuclei ( Van Meir et al, 2006 ; Orije et al, 2021b ). Photorefractoriness not only forms a brake on gonadal maturation, but also prevents an increase in singing activity in female starlings in response to testosterone treatment, in contrast to photosensitive females treated with testosterone ( Rouse et al, 2015 ).…”

“…Diffusion data were analyzed with MRtrix3 version 3.0 ( Tournier et al, 2012 ) following the same processing steps as described in Orije et al (2021b) . Preprocessing of the individual DW-images included the following steps: denoising ( Veraart et al, 2016 ), correction for Gibbs ringing ( Kellner et al, 2016 ), motion and distortion correction using FSL ( Jenkinson et al, 2012 ), bias field correction using ANTS (Advanced Normalization Tool; Avants et al, 2010 ), whole brain extraction and upsampling to isotropic voxels of 1.75 mm.…”

A brain for all seasons: An in vivo MRI perspective on songbirds

“…The before mentioned longitudinal study by (Orije et al, 2021) determined the temporal profile of multisensory neuroplasticity, but also established sex differences in seasonal neuroplasticity and related them to the song behavior. The data show that the majority of seasonal neuroplasticity occurred similarly in both male and female starlings but some specific parts of the SCS (the surroundings of bilateral HVC and left RA) and auditory system (left NCM) only showed increased FA F I G U R E 4 (a) Overview of the experimental setup where we repeatedly monitored song behavior, hormone plasma levels and structural neuroplastic changes using Diffusion Tensor Imaging (DTI) and structural 3D scans in male and female starlings.…”

“…If two time points share the same letter, the FA values are not significantly different from each other. Adapted with permission from Orije et al (2021). CA, anterior commissure; CO, optic chiasm; CP, posterior commissure; CSt, Caudal part of the lateral striatum; DLM, medial part of the dorsolateral nucleus of the anterior thalamus; DSD, Decussatio supraoptica dorsalis; E, Entopallium; FPL, lateral forebrain bundle; GP, globus pallidus; HA, apical part of the hyperpallium; HD, densocellular part of the hyperpallium; HVC, used as a proper name (high vocal center); LAD, dorsal arcopallial lamina; LaM, mesopallial lamina; LFM, supreme frontal lamina; LFS, superior frontal lamina; LMAN, lateral magnocellular nucleus of the anterior nidopallium; LPS, pallial-subpallial lamina; LSt, lateral striatum; M, mesopallium; MLD-DM-ICO, intercollicular nucleus complex; MSt, medial striatum; N, nidopallium; NCM, caudomedial nidopallium; OM, occipito-mesencephalic tract; Pt, pretectal nucleus; RA, robust nucleus of arcopallium; Rt, Nucleus rotundus; surr, surroundings; TeO, optic tectum; tFA, fronto-arcopallial tract; TFM, Tractus thalamo-frontalis; TrO, optic tract; TSM, septopallio-mesencephalic tract values in males and were absent in female starlings.…”

“…The image layout is the same as (b). (c-e) present unpublished extended analysis on song data from Orije et al (2021).…”