Uncovering a 'sensitive window' of multisensory and motor neuroplasticity in the cerebrum and cerebellum of male and female starling

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.

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

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.

Mechanisms of recognition in birds and social Hymenoptera: from detection to information processing

In this opinion piece, we briefly review our knowledge of the mechanisms underlying auditory individual recognition in birds and chemical nest-mate recognition in social Hymenoptera. We argue that even though detection and perception of recognition cues are well studied in social Hymenoptera, the neural mechanisms remain a black box. We compare our knowledge of these insect systems with that of the well-studied avian ‘song control system’. We suggest that future studies on recognition should focus on the hypothesis of a distributed template instead of trying to locate the seat of the template as recent results do not seem to point in that direction. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Expression of oxytocin receptors in the zebra finch brain during vocal development

Juvenile male zebra finches memorize and learn to sing the song of a male caregiver, or “tutor”, during a complex vocal learning process. Juveniles are highly motivated to interact socially with their tutor, and these interactions are required for effective vocal learning. It is currently unknown what neurological mechanisms underlie attraction to tutors, but social motivation and affiliation in this and other species may be mediated by oxytocin and related nonapeptides. Here, we used qPCR to quantify expression of oxytocin receptor (OTR) mRNA in the lateral septum, auditory forebrain, and regions of the song control system in zebra finches throughout post-hatch development and vocal learning. We found that zebra finches express OTR mRNA in these regions from post-hatch day 5 to adulthood, encompassing the entire period of auditory and sensorimotor learning. We also mapped the binding of 125I-ornithine vasotocin, an oxytocin receptor antagonist that binds to oxytocin receptors in songbird brain, to understand the neuroanatomical distribution of oxytocin-like action during vocal development. This study provides the groundwork for the use of zebra finches as a model for understanding the mechanisms underlying social motivation and its role in vocal development.

Predict future learning accuracy by the structural properties of the brain, an in vivo longitudinal MRI study in songbirds

Human speech and bird song are acoustically complex communication signals that are learned by imitation during a sensitive period early in life. Although the neural networks indispensable for song learning are well established, it remains unclear which neural circuitries differentiate good from bad song copiers. By combining in vivo structural Magnetic Resonance Imaging with song analyses in juvenile male zebra finches during song learning and beyond, we discovered that song imitation accuracy correlates with the structural architecture of four distinct brain areas, none of which pertain to the song control system. Furthermore, the structural properties of a secondary auditory area in the left hemisphere, are capable to predict future song copying accuracy, already at the earliest stages of learning, before initiating vocal practicing. These findings appoint novel brain regions important for song learning outcome and inform that ultimate performance in part depends on factors experienced before vocal practicing.

Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning

The appearance of perineuronal nets (PNNs) represents one of the mechanisms that contribute to the closing of sensitive periods for neural plasticity. This relationship has mostly been studied in the ocular dominance model in rodents. Previous studies also indicated that PNN might control neural plasticity in the song control system of songbirds. To further elucidate this relationship, we quantified PNN expression and their localization around parvalbumin interneurons at key time-points during ontogeny in both male and female zebra finches, and correlated these data with the well-described development of song in this species. We also extended these analyses to the auditory system. The development of PNN during ontogeny correlated with song crystallization although the timing of PNN appearance in the four main telencephalic song control nuclei slightly varied between nuclei in agreement with the established role these nuclei play during song learning. Our data also indicate that very few PNN develop in the secondary auditory forebrain areas even in adult birds, which may allow constant adaptation to a changing acoustic environment by allowing synaptic reorganization during adulthood.