Characterization of exploratory patterns and hippocampal–prefrontal network oscillations during the emergence of free exploration

Dong, Wen-Xiu; Chen, Hongbiao; Sit, Timothy; Han, Yechao; Song, Fei; Vyssotski, Alexei L.; Gross, Cornelius; Si, Bailu; Zhan, Yang

doi:10.1016/j.scib.2021.05.018

Cited by 14 publications

(8 citation statements)

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“…Recent studies have suggested that animals with epilepsy have impaired RA (Kubova et al, 2004;O'Loughlin et al, 2014), and we found that the impaired RA led to epileptic mice preferentially approaching potential threats. Previous studies have shown that the hippocampus and its broad of downstream participate in regulating behavior in EPM (Lee et al, 2019;Besnard et al, 2020;Xia and Kheirbek, 2020;Botterill et al, 2021;Dong et al, 2021;Wang et al, 2021), in which RA behavior plays a key role in future outcomes (Jacinto et al, 2016;Motta et al, 2017;Blanchard, 2018;McNaughton and Corr, 2018). In this study, we confirmed that dDG/CA3 neurons are involved in RA behavior.…”

Section: Discussionsupporting

confidence: 85%

“…It is generally considered that the ventral hippocampal neurons participate in the modulation of anxiety behaviors, while the dorsal hippocampal neurons play an important role in coding spatial information (Fanselow and Dong, 2010). Recent studies have revealed that the dorsal hippocampus also regulates mild anxiogenic contextual exploration (Dong et al, 2021) and ambiguous threat context (Besnard et al, 2020). As the HPC and its downstream region represent diverging patterns of coding Abbreviations: TLE, temporal lobe epilepsy; WT, wild type; RA, risk assessment; dHPC, dorsal hippocampus; HPC, hippocampus; EPM, elevated plus maze; E/I, excitation and inhibition; SOM+, somatostatin-positive; CCK+, cholecystokininpositive; PV+, parvalbumin-positive; VIP+, vasoactive intestinal polypeptide positive; LS, lateral septum; HPC-LS, hippocampal-lateral section; dDG/CA3, dorsal dentate gyrus and CA3; ns, no significant; N.R., no response.…”

Section: Introductionmentioning

confidence: 99%

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Dysfunction of the Hippocampal-Lateral Septal Circuit Impairs Risk Assessment in Epileptic Mice

Cao

Sun²,

Huang

et al. 2022

Front. Mol. Neurosci.

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Temporal lobe epilepsy, a chronic disease of the brain characterized by degeneration of the hippocampus, has impaired risk assessment. Risk assessment is vital for survival in complex environments with potential threats. However, the underlying mechanisms remain largely unknown. The intricate balance of gene regulation and expression across different brain regions is related to the structure and function of specific neuron subtypes. In particular, excitation/inhibition imbalance caused by hyperexcitability of glutamatergic neurons and/or dysfunction of GABAergic neurons, have been implicated in epilepsy. First, we estimated the risk assessment (RA) by evaluating the behavior of mice in the center of the elevated plus maze, and found that the kainic acid-induced temporal lobe epilepsy mice were specifically impaired their RA. This experiment evaluated approach-RA, with a forthcoming approach to the open arm, and avoid-RA, with forthcoming avoidance of the open arm. Next, results from free-moving electrophysiological recordings showed that in the hippocampus, ∼7% of putative glutamatergic neurons and ∼15% of putative GABAergic neurons were preferentially responsive to either approach-risk assessment or avoid-risk assessment, respectively. In addition, ∼12% and ∼8% of dorsal lateral septum GABAergic neurons were preferentially responsive to approach-risk assessment and avoid-risk assessment, respectively. Notably, during the impaired approach-risk assessment, the favorably activated dorsal dentate gyrus and CA3 glutamatergic neurons increased (∼9%) and dorsal dentate gyrus and CA3 GABAergic neurons decreased (∼7%) in the temporal lobe epilepsy mice. Then, we used RNA sequencing and immunohistochemical staining to investigate which subtype of GABAergic neuron loss may contribute to excitation/inhibition imbalance. The results show that temporal lobe epilepsy mice exhibit significant neuronal loss and reorganization of neural networks. In particular, the dorsal dentate gyrus and CA3 somatostatin-positive neurons and dorsal lateral septum cholecystokinin-positive neurons are selectively vulnerable to damage after temporal lobe epilepsy. Optogenetic activation of the hippocampal glutamatergic neurons or chemogenetic inhibition of the hippocampal somatostatin neurons directly disrupts RA, suggesting that an excitation/inhibition imbalance in the dHPC dorsal lateral septum circuit results in the impairment of RA behavior. Taken together, this study provides insight into epilepsy and its comorbidity at different levels, including molecular, cell, neural circuit, and behavior, which are expected to decrease injury and premature mortality in patients with epilepsy.

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Section: Discussionsupporting

confidence: 85%

Section: Introductionmentioning

confidence: 99%

Dysfunction of the Hippocampal-Lateral Septal Circuit Impairs Risk Assessment in Epileptic Mice

Cao

Sun²,

Huang

et al. 2022

Front. Mol. Neurosci.

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“…However, in our experimental paradigm, this behavior may have been promoted by the vestibule-reward association rather than anxiety. Finally, the random strategy might be related to exploratory behaviors and engage an ensemble of brain regions important for sensory integration, decision-making and reinforcement learning such as the hippocampus, prefrontal cortex, and basal ganglia 9,[55][56][57][58][59][60][61][62] .…”

Section: Discussionmentioning

confidence: 99%

Stochastic characterization of navigation strategies in an automated variant of the Barnes maze

Lee

Jung

Royer

2023

Preprint

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Animals can use a repertoire of strategies to navigate in an environment, and it remains an intriguing question how these strategies are selected based on the nature and familiarity of environments. To investigate this question, we developed a fully automated variant of the Barnes maze, characterized by 24 vestibules distributed along the periphery of a circular arena, and monitored the trajectories of mice over 15 days as they learned to navigate from a random start vestibule to a goal vestibule. We show that the patterns of vestibule visits can be reproduced by the combination of three stochastic processes reminiscent of random, serial and spatial strategies. The processes randomly selected vestibules based on either uniform (random) or biased (serial and spatial) probability distributions; closely matched experimental data across a range of statistical distributions characterizing the length, distribution, step size, direction, and stereotypy of vestibule sequences; and revealed a shift from random to spatial and serial strategies over time, with a strategy switch occurring approximately every 6 vestibule visits. Our study provides a novel apparatus and analysis toolset for tracking the repertoire of navigation strategies and demonstrates that a set of stochastic processes can largely account for exploration patterns in the Barnes maze.

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“…The setup of the robot experiment mimics the initial exploration patterns of mice in environments near their ecological habitants. In free exploration, mice often repeat familiar paths to the frontiers of exploration and start to acquaint unknow territory ( Dong et al, 2021 ). After sufficient exploration, the trajectories of the agent cover the whole environment.…”

Section: Discussionmentioning

confidence: 99%

Entorhinal-hippocampal interactions lead to globally coherent representations of space

Zeng

Si²,

Li³

2022

Current Research in Neurobiology

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Characterization of exploratory patterns and hippocampal–prefrontal network oscillations during the emergence of free exploration

Cited by 14 publications

References 34 publications

Dysfunction of the Hippocampal-Lateral Septal Circuit Impairs Risk Assessment in Epileptic Mice

Dysfunction of the Hippocampal-Lateral Septal Circuit Impairs Risk Assessment in Epileptic Mice

Stochastic characterization of navigation strategies in an automated variant of the Barnes maze

Entorhinal-hippocampal interactions lead to globally coherent representations of space

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