Phase–Amplitude Coupling between Theta Rhythm and High-Frequency Oscillations in the Hippocampus of Pigeons during Navigation

Simple Summary The hippocampus (Hp) is involved in various aspects of spatial cognition during navigation, reflected in multiple neural oscillations across different frequencies. Given the structure homology between the avian and mammalian Hp, does it exhibit similar cross-frequency interaction mechanisms? Unlike rodents, birds can navigate by walking and flying. So, does the avian Hp share the same information interaction under different locomotor modes? In this study, we employed rock pigeons with exceptional spatial navigation abilities and conducted two goal-directed navigational experiments: a ground maze task with a circuitous paradigm and an outdoor homing flight task. These experiments were designed to explore the interactions between different frequency bands in the avian Hp during walking and flying navigation. The study revealed that phase–amplitude coupling (PAC) existed in the avian Hp during the navigational active phases. Meanwhile, the sub-frequency bands modulated by theta oscillations are different in different modes of locomotion. These findings support evidence for cross-frequency interactions in the avian Hp during spatial navigation and contribute to explaining the role of coupling, at least partially, in the ongoing cognitive demands during the navigation process. Abstract Navigation is a complex task in which the hippocampus (Hp), which plays an important role, may be involved in interactions between different frequency bands. However, little is known whether this cross-frequency interaction exists in the Hp of birds during navigation. Therefore, we examined the electrophysiological characteristics of hippocampal cross-frequency interactions of domestic pigeons (Columba livia domestica) during navigation. Two goal-directed navigation tasks with different locomotor modes were designed, and the local field potentials (LFPs) were recorded for analysis. We found that the amplitudes of high-frequency oscillations in Hp were dynamically modulated by the phase of co-occurring theta-band oscillations both during ground-based maze and outdoor flight navigation. The high-frequency amplitude sub-frequency bands modulated by the hippocampal theta phase were different at different tasks, and this process was independent of the navigation path and goal. These results suggest that phase–amplitude coupling (PAC) in the avian Hp may be more associated with the ongoing cognitive demands of navigational processes. Our findings contribute to the understanding of potential mechanisms of hippocampal PAC on multi-frequency informational interactions in avian navigation and provide valuable insights into cross-species evolution.