High-Frequency Local Field Potential Oscillations for Pigeons in Effective Turning

Abstract

Flexible turning behavior endows Homing Pigeons (Columba livia domestica) with high adaptability and intelligence in long-distance flight, foraging, hazard avoidance, and social interactions. The present study recorded the activity pattern of their local field potential (LFP) oscillations and explored the relationship between different bands of oscillations and turning behaviors in the formatio reticularis medialis mesencephali (FRM). The results showed that the C (13-60 Hz) and D (61-130 Hz) bands derived from FRM nuclei oscillated significantly in active turning, while the D and E (131-200 Hz) bands oscillated significantly in passive turning. Additionally, compared with lower-frequency stimulation (40 Hz and 60 Hz), 80 Hz stimulation can effectively activate the turning function of FRM nuclei. Electrical stimulation elicited stronger oscillations of neural activity, which strengthened the pigeons' turning locomotion willingness, showing an enhanced neural activation effect. These findings suggest that different band oscillations play different roles in the turning behavior; in particular, higher-frequency oscillations (D and E bands) enhance the turning behavior. These findings will help us decode the complex relationship between bird brains and behaviors and are expected to facilitate the development of neuromodulation techniques for animal robotics.

Keywords: electrical stimulation; higher-frequency oscillations; homing pigeons; neural activity; turning behaviors.

Figure 1

Electrode placement locations and a pigeon with implanted electrodes. (a) Coordinate positions of implanted electrodes in the formatio reticularis medialis mesencephali (FRM) nuclei of the pigeon brain. FRM−L and FRM−R represent the FRM nuclei regions of the left and right hemispheres. HAI and VAI correspond to the horizontal and vertical axes of the brain stereotactic apparatus, while RE denotes the reference electrode implanted above the cerebellum. P1, P2, P3, and P4 were connected to the ground wire and implanted above the lateral suture of the double parietal bone. (b) Depth of implantation of the stimulating electrode and the recording electrode, respectively (10 mm), and the spacing between the tips of the two electrodes (50 μm). (c) A pigeon implanted with stimulation and recording electrodes (ID: P05). (d) Coronal slices of the pigeon brain demonstrating that the electrode was implanted in the FRM nucleus.

Figure 2

Behavioral experimental apparatus and experimental systems. (a) Customized T-maze apparatus for pigeons. (b) Overall system construction for turning behavior experiments in pigeons. TB: beginning of turning; TE: end of turning.

Figure 3

Experimental procedures and 2 s of typical local field potential (LFP) signal tracings for each channel. (a) Recording LFP signals in pigeons while awake and immobile. (b) Recording of LFP signals in pigeons during food-induced active turning. (c) Recording LFP signals of passive turning in pigeons at different electrical stimulation frequencies. L−FRM and R−FRM represent formatio reticularis medialis mesencephali (FRM) nuclei in the right and left brain hemispheres of pigeons, respectively.

Figure 4

Results of behavioral responses (left) and time–frequency plots of local field potential (LFP) oscillations (right) of pigeons under different stimulus conditions: (a) the awake and motionless state of the pigeon, (b) the active turning state of the pigeon, (c) the motionless state of the pigeon in response to the 40 Hz stimulus, (d) the slight head bobbing state of the pigeon in response to the 60 Hz stimulus, and (e) the passive turning state of the pigeon in response to the 80 Hz stimulus. Gray circles represent food boxes without food, red circles represent food boxes with food; yellow arrows are symbols of electrical stimulation; L−FRM and R−FRM represent formatio reticularis medialis mesencephali (FRM) nuclei in the right and left brain hemispheres of pigeons, respectively.

Figure 5

The mean absolute power spectra of pigeons across various behavioral states, with A, B, C, D, and E representing five different characteristic bands. The least-significant difference test (LSD) was employed for conducting pairwise comparisons between these different bands. Abbreviations: AI: pigeons’ awake immobile state; AT: pigeons actively turning, induced by food. The values 40 Hz, 60 Hz, and 80 Hz represent the different frequencies of electrical stimulation. Among them, at 80 Hz, pigeons showed passive turning behavior. Each asterisk indicates significant and highly significant differences (* p < 0.05, ** p < 0.01, and *** p < 0.001) in the mean power spectrum between different stimuli.

Figure 6

Absolute power spectra in the formatio reticularis medialis mesencephali (FRM) nuclei regions of the left and right hemispheres for different stimulus conditions: (a–e) the five different characteristic bands. The least-significant difference test (LSD) was employed for conducting pairwise comparisons between these different stimulus conditions. Abbreviation: AI: pigeons’ awake immobile state; AT: pigeons actively turning. The values 40 Hz, 60 Hz, and 80 Hz represent the different frequencies of electrical stimulation. Asterisks denote significant and highly significant differences (* p < 0.05, ** p < 0.01, and *** p < 0.001).