Exploring Memory-related Network Via Dorsal Hippocampus Suppression

Overview

Journal Netw Neurosci

Publisher MIT Press

Specialty Neurology

Date 2024 Dec 30

PMID 39735497

Authors

Xu Han

Samuel R Cramer

Dennis C Y Chan

Nanyin Zhang

Affiliations

Soon will be listed here.

Abstract

Memory is a complex brain process that requires coordinated activities in a large-scale brain network. However, the relationship between coordinated brain network activities and memory-related behavior is not well understood. In this study, we investigated this issue by suppressing the activity in the dorsal hippocampus (dHP) using chemogenetics and measuring the corresponding changes in brain-wide resting-state functional connectivity (RSFC) and memory behavior in awake rats. We identified an extended brain network contributing to the performance in a spatial memory related task. Our results were cross-validated using two different chemogenetic actuators, clozapine (CLZ) and clozapine-N-oxide (CNO). This study provides a brain network interpretation of memory performance, indicating that memory is associated with coordinated brain-wide neural activities.

References

Shimizu M, Yoshimura M, Baba K, Ikeda N, Nonaka Y, Maruyama T . Deschloroclozapine exhibits an exquisite agonistic effect at lower concentration compared to clozapine-N-oxide in hM3Dq expressing chemogenetically modified rats. Front Neurosci. 2023; 17:1301515. PMC: 10720889. DOI: 10.3389/fnins.2023.1301515. View

Euston D, Gruber A, McNaughton B . The role of medial prefrontal cortex in memory and decision making. Neuron. 2012; 76(6):1057-70. PMC: 3562704. DOI: 10.1016/j.neuron.2012.12.002. View

Zou Q, Zhu C, Yang Y, Zuo X, Long X, Cao Q . An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods. 2008; 172(1):137-41. PMC: 3902859. DOI: 10.1016/j.jneumeth.2008.04.012. View

Ma Z, Zhang N . Temporal transitions of spontaneous brain activity. Elife. 2018; 7. PMC: 5843406. DOI: 10.7554/eLife.33562. View

Oldham S, Fornito A . The development of brain network hubs. Dev Cogn Neurosci. 2018; 36:100607. PMC: 6969262. DOI: 10.1016/j.dcn.2018.12.005. View

Park S, Kramer E, Mercaldo V, Rashid A, Insel N, Frankland P . Neuronal Allocation to a Hippocampal Engram. Neuropsychopharmacology. 2016; 41(13):2987-2993. PMC: 5101572. DOI: 10.1038/npp.2016.73. View

Vann S . Gudden's ventral tegmental nucleus is vital for memory: re-evaluating diencephalic inputs for amnesia. Brain. 2009; 132(Pt 9):2372-84. DOI: 10.1093/brain/awp175. View

Jendryka M, Palchaudhuri M, Ursu D, van der Veen B, Liss B, Katzel D . Pharmacokinetic and pharmacodynamic actions of clozapine-N-oxide, clozapine, and compound 21 in DREADD-based chemogenetics in mice. Sci Rep. 2019; 9(1):4522. PMC: 6418145. DOI: 10.1038/s41598-019-41088-2. View

Aggleton J, Nelson A, OMara S . Time to retire the serial Papez circuit: Implications for space, memory, and attention. Neurosci Biobehav Rev. 2022; 140:104813. PMC: 10804970. DOI: 10.1016/j.neubiorev.2022.104813. View

10.

Lopez J, Wolff M, Lecourtier L, Cosquer B, Bontempi B, Dalrymple-Alford J . The intralaminar thalamic nuclei contribute to remote spatial memory. J Neurosci. 2009; 29(10):3302-6. PMC: 6666443. DOI: 10.1523/JNEUROSCI.5576-08.2009. View

11.

Liu Y, Perez P, Ma Z, Ma Z, Dopfel D, Cramer S . An open database of resting-state fMRI in awake rats. Neuroimage. 2020; 220:117094. PMC: 7605641. DOI: 10.1016/j.neuroimage.2020.117094. View

12.

Yu Y, Qiu Y, Li G, Zhang K, Bo B, Pei M . Sleep fMRI with simultaneous electrophysiology at 9.4 T in male mice. Nat Commun. 2023; 14(1):1651. PMC: 10039056. DOI: 10.1038/s41467-023-37352-9. View

13.

Han X, Cramer S, Zhang N . Deriving causal relationships in resting-state functional connectivity using SSFO-based optogenetic fMRI. J Neural Eng. 2022; 19(6). PMC: 9681600. DOI: 10.1088/1741-2552/ac9d66. View

14.

Sewards T, Sewards M . Input and output stations of the entorhinal cortex: superficial vs. deep layers or lateral vs. medial divisions?. Brain Res Brain Res Rev. 2003; 42(3):243-51. DOI: 10.1016/s0165-0173(03)00175-9. View

15.

Conrad C, Galea L, Kuroda Y, McEwen B . Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav Neurosci. 1996; 110(6):1321-34. DOI: 10.1037//0735-7044.110.6.1321. View

16.

Gomez J, Bonaventura J, Lesniak W, Mathews W, Sysa-Shah P, Rodriguez L . Chemogenetics revealed: DREADD occupancy and activation via converted clozapine. Science. 2017; 357(6350):503-507. PMC: 7309169. DOI: 10.1126/science.aan2475. View

17.

Amaral D, Scharfman H, Lavenex P . The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res. 2007; 163:3-22. PMC: 2492885. DOI: 10.1016/S0079-6123(07)63001-5. View

18.

Beloate L, Zhang N . Connecting the dots between cell populations, whole-brain activity, and behavior. Neurophotonics. 2022; 9(3):032208. PMC: 8957372. DOI: 10.1117/1.NPh.9.3.032208. View

19.

Hindy N, Ng F, Turk-Browne N . Linking pattern completion in the hippocampus to predictive coding in visual cortex. Nat Neurosci. 2016; 19(5):665-667. PMC: 4948994. DOI: 10.1038/nn.4284. View

20.

Restivo L, Niibori Y, Mercaldo V, Josselyn S, Frankland P . Development of Adult-Generated Cell Connectivity with Excitatory and Inhibitory Cell Populations in the Hippocampus. J Neurosci. 2015; 35(29):10600-12. PMC: 6605118. DOI: 10.1523/JNEUROSCI.3238-14.2015. View