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Pigeons are classic animal models for learning, memory, and cognition. The majority of the current understanding about avian neurobiology outside of the domain of the song system has been established using pigeons. Since MRI represents an increasingly relevant tool for comparative neuroscience, a 3-dimensional MRI-based atlas of the pigeon brain becomes essential. Using multiple imaging protocols, we delineated diverse ascending sensory and descending motor systems as well as the hippocampal formation. This pigeon brain atlas can easily be used to determine the stereotactic location of identified neural structures at any angle of the head. In addition, the atlas is useful to find the optimal angle of sectioning for slice experiments, stereotactic injections and electrophysiological recordings. This pigeon brain atlas is freely available for the scientific community.

The song control system (SCS) of songbirds displays a remarkable plasticity in species where song output changes seasonally. The mechanisms underlying this plasticity are barely understood and research has primarily been focused on the song nuclei themselves, largely neglecting their interconnections and connections with other brain regions. We investigated seasonal changes in the entire brain, including the song nuclei and their connections, of nine male starlings (Sturnus vulgaris). At two times of the year, during the breeding (April) and nonbreeding (July) seasons, we measured in the same subjects cellular attributes of brain regions using in vivo high-resolution diffusion tensor imaging (DTI) at 7 T. An increased fractional anisotropy in the HVC-RA pathway that correlates with an increase in axonal density (and myelination) was found during the breeding season, confirming multiple previous histological reports. Other parts of the SCS, namely the occipitomesencephalic axonal pathway, which contains fiber tracts important for song production, showed increased fractional anisotropy due to myelination during the breeding season and the connection between HVC and Area X showed an increase in axonal connectivity. Beyond the SCS we discerned fractional anisotropy changes that correlate with myelination changes in the optic chiasm and axonal organization changes in an interhemispheric connection, the posterior commissure. These results demonstrate an unexpectedly broad plasticity in the connectivity of the avian brain that might be involved in preparing subjects for the competitive and demanding behavioral tasks that are associated with successful reproduction.

Selection of sexual partners is among the most critical decisions that individuals make and is therefore strongly shaped by evolution. In social species, where communication signals can convey substantial information about the identity, state, or quality of the signaler, accurate interpretation of communication signals for mate choice is crucial. Despite the importance of social information processing, to date, relatively little is known about the neurobiological mechanisms that contribute to sexual decision making and preferences. In this study, we used a combination of whole-brain functional magnetic resonance imaging (fMRI), immediate early gene expression, and behavior tests to identify the circuits that are important for the perception and evaluation of courtship songs in a female songbird, the zebra finch (Taeniopygia guttata). Female zebra finches are sensitive to subtle differences in male song performance and strongly prefer the longer, faster, and more stereotyped courtship songs to non-courtship renditions. Using BOLD fMRI and EGR1 expression assays, we uncovered a novel region involved in auditory perceptual decision making located in a sensory integrative region of the avian central nidopallium outside the traditionally studied auditory forebrain pathways. Changes in activity in this region in response to acoustically similar but categorically divergent stimuli showed stronger parallels to behavioral responses than an auditory sensory region. These data highlight a potential role for the caudocentral nidopallium (NCC) as a novel node in the avian circuitry underlying the evaluation of acoustic signals and their use in mate choice.

The song control system (SCS) of seasonal songbirds shows remarkable seasonal plasticity. Male starlings (Sturnus vulgaris) sing throughout the year, but in the breeding season, when concentrations of testosterone are elevated, the song is highly sexually motivated. The main goal of this study was to investigate structural seasonal changes in regions involved in auditory processing and in socio-sexual behavior. Using in vivo Diffusion Tensor Imaging (DTI), we measured in breeding and nonbreeding seasons volume and tissue characteristics of several brain regions of nine adult male starlings. We demonstrate that the songbird brain exhibits an extreme seasonal plasticity not merely limited to the SCS. Volumetric analysis showed seasonal telencephalon volume changes and more importantly also a volumetric change in the caudal region of the nidopallium (NCM), a region analogous to the mammalian secondary auditory cortex. Analysis of the DTI data allowed detection of seasonal changes in cellular attributes in NCM and regions involved in social behavior. This study extends our view on a seasonally dynamic avian brain which not only hones its song control system but also auditory and social systems to be prepared for the breeding season.

h i g h l i g h t sFirst study to image the whole brain of awake pigeons. We show a habituation program for MR-sessions under awake and head-fixed conditions. Movement under these conditions is minimal. First measurement of functional connectivity in a non-mammalian species. Analyses of BOLD-response and functional connectivity are feasible. a r t i c l e i n f o b s t r a c tAt present, functional MRI (fMRI) is increasingly used in animal research but the disadvantage is that the majority of the imaging is applied in anaesthetized animals. Only a few articles present results obtained in awake rodents. In this study both traditional fMRI and resting state (rsfMRI) were applied to four pigeons, that were trained to remain still while being imaged, removing the need for anesthesia. This is the first time functional connectivity measurements are performed in a non-mammalian species. Since the visual system of pigeons is a well-known model for brain asymmetry, the focus of the study was on the neural substrate of the visual system. For fMRI a visual stimulus was used and functional connectivity measurements were done with the entopallium (E; analog for the primary visual cortex) as a seed region. Interestingly in awake pigeons the left E was significantly functionally connected to the right E. Moreover we compared connectivity maps for a seed region in both hemispheres resulting in a stronger bilateral connectivity starting from left E then from right E. These results could be used as a starting point for further imaging studies in awake birds and also provide a new window into the analysis of hemispheric dominance in the pigeon.

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