Synchronized neural rhythms in rat hippocampal CA1 region and orbitofrontal cortex are involved in learning and memory consolidation in spatial goal-directed tasks

doi:10.12122/j.issn.1673-4254.2025.03.05

Abstract

Abstract:

Objective To investigate the neural mechanisms of rhythmic activity in the hippocampal CA1 region and orbitofrontal cortex (OFC) during a spatial goal-directed task. Methods Four long-Evans rats were trained to perform a spatial goal-directed task in a land-based water maze (Cheese-board maze). The task was divided into 5 periods: Pre-test, Pre-sleep, Learning, Post-sleep, and Post-test. During the Learning phase, the task was split into two goal navigation and two reward acquisition processes with a total of 8 learning stages. Local field potentials (LFP) from the CA1 and the OFC were recorded, and power spectral density analysis was performed on Theta (6-12 Hz), Beta (15-30 Hz), Low gamma (30-60 Hz), and High gamma (60-90 Hz) bands. Coherence, phase-locking value (PLV), and phase-amplitude cross coupling (PAC) were used to assess the interactions between the CA1 and the OFC during learning and memory. Results During the task training, the rats showed consistent rhythms of OFC neural activity across the task states (P>0.05) while exhibiting significant changes in Beta and High gamma rhythms in the CA1 region (P<0.05). Coherence and PLV between the CA1 and the OFC were higher during goal navigation, especially in the stable learning phase (Stage 8 vs Stage 1, P<0.01). The rats showed stronger cross-frequency coupling between CA1-Theta and OFC-Low gamma in the Post-test phase than in the Pre-test phase (P<0.05). Conclusion Learning and memory consolidation in goal-directed tasks involve synchronized activity between the CA1 region and the OFC, and cross-frequency coupling plays a key role in maintaining short-term memory of reward locations in rats.

Key words: goal-directed task, hippocampal CA1, orbitofrontal cortex, neural rhythms

Lingwei TANG, Jiasong LI, Haibing XU. Synchronized neural rhythms in rat hippocampal CA1 region and orbitofrontal cortex are involved in learning and memory consolidation in spatial goal-directed tasks[J]. Journal of Southern Medical University, 2025, 45(3): 479-487.

Figures/Tables 6

Fig.1 Performance of the rats in the spatial goal-directed task. A: Trajectory in the task. This task was divided into 5 periods, and the learning period was further divided into 8 stages. The two orange dots represent two novel reward positions; the two gray dots represent two old reward positions. B: Learning performance was assessed based on the distance of each stage (Stage 1 vs Stage 8, ***P<0.005). C: Memory performance was evaluated based on the number of times that the rats entered the old and novel reward positions during the Pre-test and Post-test, respectively (**P<0.01, ***P<0.005).

Fig.2 Hippocampal CA1 and OFC tetrodes placement. A: An example of tetrode trajectories from lw016. The arrowhead indicates the end of tetrodes. B: Tetrode positions in the 4 rats. Orange dot: lw016; green dot: lw015; blue dot: js001; red dot: lw014. Numbers represent the distance from the bregma.

Fig.3 Differences in neural rhythm responses between the hippocampal CA1 and OFC in different task states. A: The task state was divided into goal navigation process (S-P1 and P1-P1) and reward acquisition process (P1 and P2). B: Distribution of power across 1-100 Hz. C: Differences in power strength of different rhythms across different processes. D: Comparison of power between reward (average of two novel positions) and non-reward (average of two old positions). *P<0.05, ***P<0.005.

Fig.4 Coherence of hippocampal CA1 region and the OFC. A: Distribution of coherence across 1-100 Hz. B: Coherence in two goal navigation processes, two reward acquisition processes, and non-reward processes. C: The distribution of coherence across learning phases. D: Comparison of coherence differences in Theta and Beta rhythms during Stage 1 and Stage 8 in two goal navigation processes (**P<0.01, ***P<0.005).

Fig.5 Phase locking of hippocampal CA1 and the OFC. A: Distribution of phase locking across the learning phases. B: Comparison of phase locking differences in Theta and Beta rhythms during Stage 1 and Stage 8 in the two goal navigation processes (***P<0.005).

Fig.6 Neural activity in the hippocampal CA1 region and the OFC during long-term memory and short-term memory. A: Distribution of power across 1-100 Hz. Dashed line represents Pre-test; solid line represents Post-test. B: Distribution of power across 1-100 Hz. C: Phase-amplitude coupling in Pre-test and Post-test. Y-axis represents the data of OFC in the 15-90 Hz range; X-axis represents the data of CA1 in the Theta rhythm. The color map indicates the phase-amplitude coupling value. The area between the two dashed lines represents the Low gamma rhythm. D: Hippocampal CA1 Theta phase-OFC Low gamma amplitude cross-coupling in the Post-test was greater than in the Pre-test (*P<0.05).

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