Integration of Gene Expression and Brain-wide Connectivity Reveals the Multiscale Organization of Mouse Hippocampal Networks

Overview

Journal Nat Neurosci

Date 2018 Oct 10

PMID 30297807

Citations 96

Authors

Michael S Bienkowski

Ian Bowman

Monica Y Song

Lin Gou

Tyler Ard

Kaelan Cotter

Muye Zhu

Nora L Benavidez

Seita Yamashita

Jaspar Abu-Jaber

Sana Azam

Darrick Lo

Nicholas N Foster

Houri Hintiryan

Hong-Wei Dong

Affiliations

Soon will be listed here.

Abstract

Understanding the organization of the hippocampus is fundamental to understanding brain function related to learning, memory, emotions, and diseases such as Alzheimer's disease. Physiological studies in humans and rodents have suggested that there is both structural and functional heterogeneity along the longitudinal axis of the hippocampus. However, the recent discovery of discrete gene expression domains in the mouse hippocampus has provided the opportunity to re-evaluate hippocampal connectivity. To integrate mouse hippocampal gene expression and connectivity, we mapped the distribution of distinct gene expression patterns in mouse hippocampus and subiculum to create the Hippocampus Gene Expression Atlas (HGEA). Notably, previously unknown subiculum gene expression patterns revealed a hidden laminar organization. Guided by the HGEA, we constructed the most detailed hippocampal connectome available using Mouse Connectome Project ( http://www.mouseconnectome.org ) tract tracing data. Our results define the hippocampus' multiscale network organization and elucidate each subnetwork's unique brain-wide connectivity patterns.

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References

Dong H, Swanson L, Chen L, Fanselow M, Toga A . Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc Natl Acad Sci U S A. 2009; 106(28):11794-9. PMC: 2710698. DOI: 10.1073/pnas.0812608106. View

Vann S, Aggleton J, Maguire E . What does the retrosplenial cortex do?. Nat Rev Neurosci. 2009; 10(11):792-802. DOI: 10.1038/nrn2733. View

Zeisel A, Munoz-Manchado A, Codeluppi S, Lonnerberg P, La Manno G, Jureus A . Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science. 2015; 347(6226):1138-42. DOI: 10.1126/science.aaa1934. View

Sik A, Penttonen M, Ylinen A, Buzsaki G . Hippocampal CA1 interneurons: an in vivo intracellular labeling study. J Neurosci. 1995; 15(10):6651-65. PMC: 6577981. View

Tovote P, Fadok J, Luthi A . Neuronal circuits for fear and anxiety. Nat Rev Neurosci. 2015; 16(6):317-31. DOI: 10.1038/nrn3945. View

Cembrowski M, Spruston N . Integrating Results across Methodologies Is Essential for Producing Robust Neuronal Taxonomies. Neuron. 2017; 94(4):747-751.e1. DOI: 10.1016/j.neuron.2017.04.023. View

Biag J, Huang Y, Gou L, Hintiryan H, Askarinam A, Hahn J . Cyto- and chemoarchitecture of the hypothalamic paraventricular nucleus in the C57BL/6J male mouse: a study of immunostaining and multiple fluorescent tract tracing. J Comp Neurol. 2011; 520(1):6-33. PMC: 4104804. DOI: 10.1002/cne.22698. View

Swanson L . Cerebral hemisphere regulation of motivated behavior. Brain Res. 2000; 886(1-2):113-164. DOI: 10.1016/s0006-8993(00)02905-x. View

Shah S, Lubeck E, Zhou W, Cai L . seqFISH Accurately Detects Transcripts in Single Cells and Reveals Robust Spatial Organization in the Hippocampus. Neuron. 2017; 94(4):752-758.e1. DOI: 10.1016/j.neuron.2017.05.008. View

10.

Weible A . Remembering to attend: the anterior cingulate cortex and remote memory. Behav Brain Res. 2013; 245:63-75. DOI: 10.1016/j.bbr.2013.02.010. View

11.

Amaral D . Emerging principles of intrinsic hippocampal organization. Curr Opin Neurobiol. 1993; 3(2):225-9. DOI: 10.1016/0959-4388(93)90214-j. View

12.

de Lima M, Baldo M, Canteras N . A role for the anteromedial thalamic nucleus in the acquisition of contextual fear memory to predatory threats. Brain Struct Funct. 2016; 222(1):113-129. DOI: 10.1007/s00429-016-1204-2. View

13.

Ding S . Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. J Comp Neurol. 2013; 521(18):4145-62. DOI: 10.1002/cne.23416. View

14.

Thompson R, Swanson L . Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Brain Res Rev. 2003; 41(2-3):153-202. DOI: 10.1016/s0165-0173(02)00232-1. View

15.

Gauthier J, Tank D . A Dedicated Population for Reward Coding in the Hippocampus. Neuron. 2018; 99(1):179-193.e7. PMC: 7023678. DOI: 10.1016/j.neuron.2018.06.008. View

16.

Scharfman H . The enigmatic mossy cell of the dentate gyrus. Nat Rev Neurosci. 2016; 17(9):562-75. PMC: 5369357. DOI: 10.1038/nrn.2016.87. View

17.

Fanselow M, Dong H . Are the dorsal and ventral hippocampus functionally distinct structures?. Neuron. 2010; 65(1):7-19. PMC: 2822727. DOI: 10.1016/j.neuron.2009.11.031. View

18.

Swanson L, Cowan W . An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol. 1977; 172(1):49-84. DOI: 10.1002/cne.901720104. View

19.

Taube J . The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci. 2007; 30:181-207. DOI: 10.1146/annurev.neuro.29.051605.112854. View

20.

Gross C, Canteras N . The many paths to fear. Nat Rev Neurosci. 2012; 13(9):651-8. DOI: 10.1038/nrn3301. View