Neural-activity mapping of memory-based dominance in the crow: neural networks integrating individual discrimination and social behaviour control

Abstract

Large-billed crows (Corvus macrorhynchos), highly social birds, form stable dominance relationships based on the memory of win/loss outcomes of first encounters and on individual discrimination. This socio-cognitive behaviour predicts the existence of neural mechanisms for integration of social behaviour control and individual discrimination. This study aimed to elucidate the neural substrates of memory-based dominance in crows. First, the formation of dominance relationships was confirmed between males in a dyadic encounter paradigm. Next, we examined whether neural activities in 22 focal nuclei of pallium and subpallium were correlated with social behaviour and stimulus familiarity after exposure to dominant/subordinate familiar individuals and unfamiliar conspecifics. Neural activity was determined by measuring expression level of the immediate-early-gene (IEG) protein Zenk. Crows displayed aggressive and/or submissive behaviour to opponents less frequently but more discriminatively in subsequent encounters, suggesting stable dominance based on memory, including win/loss outcomes of the first encounters and individual discrimination. Neural correlates of aggressive and submissive behaviour were found in limbic subpallium including septum, bed nucleus of the striae terminalis (BST), and nucleus taeniae of amygdala (TnA), but also those to familiarity factor in BST and TnA. Contrastingly, correlates of social behaviour were little in pallium and those of familiarity with exposed individuals were identified in hippocampus, medial meso-/nidopallium, and ventro-caudal nidopallium. Given the anatomical connection and neural response patterns of the focal nuclei, neural networks connecting pallium and limbic subpallium via hippocampus could be involved in the integration of individual discrimination and social behaviour control in memory-based dominance in the crow.