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

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.

Keywords: cross-frequency interactions; flight; goal directed; local field potentials; theta.

Figure 1

Pigeon Hp microelectrode array implantation. (a) Schematic diagram of implanting site and electrode arrays. (b) A pigeon after electrode implantation.

Figure 2

Goal-directed navigational experiment apparatus and environment. (a) Diagram of the ground-based maze apparatus. Red markers indicate infrared photobeam positions. (b) The release sites for outdoor homing flight navigation. DM: initial decision-making phase; LN: Local navigation around the home.

Figure 3

Steps in the computation of phase–amplitude distribution. (a) Raw local field potential signals were recorded from the hippocampus of pigeon. (b) Filtered theta band (3–6 Hz) signals and extracted low-frequency phases. (c) Filtered high-frequency oscillations (HFOs) band (120–160 Hz) signals (black line) and HFO amplitude (red line). (d) Two amplitude distributions (blue bar, orange bar, and tawny bar indicated the area where the two distributions overlap) with different phase bins.

Figure 4

High-frequency oscillations (HFOs) amplitude modulation of local field potential (LFP) rhythms enabled by the theta phase in the hippocampus during maze runs. (a) An example trail for the experiment in the maze, with black ellipses indicating the spatial positions where neural signals were sampled and red markers denoting photobeam positions. (b) (Upper) phase–amplitude coupling calculated from LFP recorded in the Hp during maze navigation. The pseudocolor scale represents modulation index values. (Lower) pseudocolor scale representation of average HFO amplitudes as a function of theta phase for each trial. (c) Statistical analysis of similarity in HFO amplitudes within theta phase distributions (**** p < 0.0001). (d) Angular histograms of the hippocampal theta phases where the HFO peaks occurred. The black bars indicate the number of peaks of HFOs occurring in the corresponding theta phase. The red arrow indicates the direction (avgAng ± 95% CI) and magnitude (r) of the mean resultant vector. Rayleigh test was used to detect an unimodal deviation from uniformity (p < 0.01). The numbers under the diagrams indicate the four pigeons that carried out Task 1.

Figure 5

Hp theta–high-frequency oscillation (HFO) coupling in pigeons was independent of the navigation path or goal. (a) Three navigational paths were taken by pigeons to reach the goal positions. Paths 1 and 2 corresponded to the same navigation goal, while Path 3 had a different goal but shared some overlapping routes with Paths 1 and 2. The black ellipse showed the spatial position of the sampled neural signal. (b) Phase–amplitude distribution map of HFOs for P082, with the black line representing the average phase–amplitude distribution for random data. (c) Comparative analysis of theta–HFO coupling strength and similarity in phase–amplitude distributions under different navigation paths and goals.

Figure 6

Phase-to-amplitude modulation in the Hp during outdoor flight. (a) A pigeon’s homing navigation trajectory at two release sites. (b) The mean phase-to-amplitude comodulograms were obtained from recorded local field potentials (LFPs) during different navigation phases. (c) Pseudocolor scale representation of beta2 amplitude as a function of theta phase during a complete homing flight of a pigeon, with the black line on the left representing the corresponding real-time speed and the red lines indicating boundaries between different phases. (d) Comparison of the correlation in beta2 amplitude distribution between en route navigation phase (ER) and local navigation around home (LN). (e) Comparison of modulation index (MI) along two navigational paths within the ER. Analyses were performed using the Mann–Whitney test with the significance level set at p < 0.05 (**** p < 0.0001; ns p > 0.05).