Molecular Tools to Capture Active Neural Circuits

Overview

Journal Front Neural Circuits

Date 2024 Aug 5

PMID 39100199

Authors

Taichi Onishi

Kenzo Hirose

Takeshi Sakaba

Affiliations

Soon will be listed here.

Abstract

To understand how neurons and neural circuits function during behaviors, it is essential to record neuronal activity in the brain . Among the various technologies developed for recording neuronal activity, molecular tools that induce gene expression in an activity-dependent manner have attracted particular attention for their ability to clarify the causal relationships between neuronal activity and behavior. In this review, we summarize recently developed activity-dependent gene expression tools and their potential contributions to the study of neural circuits.

References

Sakurai K, Zhao S, Takatoh J, Rodriguez E, Lu J, Leavitt A . Capturing and Manipulating Activated Neuronal Ensembles with CANE Delineates a Hypothalamic Social-Fear Circuit. Neuron. 2016; 92(4):739-753. PMC: 5172402. DOI: 10.1016/j.neuron.2016.10.015. View

Tasaka G, Guenthner C, Shalev A, Gilday O, Luo L, Mizrahi A . Genetic tagging of active neurons in auditory cortex reveals maternal plasticity of coding ultrasonic vocalizations. Nat Commun. 2018; 9(1):871. PMC: 5830453. DOI: 10.1038/s41467-018-03183-2. View

Tschida K, Michael V, Takatoh J, Han B, Zhao S, Sakurai K . A Specialized Neural Circuit Gates Social Vocalizations in the Mouse. Neuron. 2019; 103(3):459-472.e4. PMC: 6687542. DOI: 10.1016/j.neuron.2019.05.025. View

Mayford M . The search for a hippocampal engram. Philos Trans R Soc Lond B Biol Sci. 2013; 369(1633):20130161. PMC: 3843892. DOI: 10.1098/rstb.2013.0161. View

Fosque B, Sun Y, Dana H, Yang C, Ohyama T, Tadross M . Neural circuits. Labeling of active neural circuits in vivo with designed calcium integrators. Science. 2015; 347(6223):755-60. DOI: 10.1126/science.1260922. View

Groves A, Kihara Y, Jonnalagadda D, Rivera R, Kennedy G, Mayford M . A Functionally Defined Astrocyte Population Identified by c-Fos Activation in a Mouse Model of Multiple Sclerosis Modulated by S1P Signaling: Immediate-Early Astrocytes (). eNeuro. 2018; 5(5). PMC: 6153337. DOI: 10.1523/ENEURO.0239-18.2018. View

Wang W, Wildes C, Pattarabanjird T, Sanchez M, Glober G, Matthews G . A light- and calcium-gated transcription factor for imaging and manipulating activated neurons. Nat Biotechnol. 2017; 35(9):864-871. PMC: 5595644. DOI: 10.1038/nbt.3909. View

Okuyama T, Kitamura T, Roy D, Itohara S, Tonegawa S . Ventral CA1 neurons store social memory. Science. 2016; 353(6307):1536-1541. PMC: 5493325. DOI: 10.1126/science.aaf7003. View

Stegemann A, Liu S, Retana Romero O, Oswald M, Han Y, Beretta C . Prefrontal engrams of long-term fear memory perpetuate pain perception. Nat Neurosci. 2023; 26(5):820-829. PMC: 10166861. DOI: 10.1038/s41593-023-01291-x. View

10.

Tanaka K, Pevzner A, Hamidi A, Nakazawa Y, Graham J, Wiltgen B . Cortical representations are reinstated by the hippocampus during memory retrieval. Neuron. 2014; 84(2):347-54. DOI: 10.1016/j.neuron.2014.09.037. View

11.

Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura M . Synaptic activity-responsive element in the Arc/Arg3.1 promoter essential for synapse-to-nucleus signaling in activated neurons. Proc Natl Acad Sci U S A. 2009; 106(1):316-21. PMC: 2629236. DOI: 10.1073/pnas.0806518106. View

12.

Roy D, Park Y, Kim M, Zhang Y, Ogawa S, DiNapoli N . Brain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions. Nat Commun. 2022; 13(1):1799. PMC: 8980018. DOI: 10.1038/s41467-022-29384-4. View

13.

Shemesh O, Tanese D, Zampini V, Linghu C, Piatkevich K, Ronzitti E . Temporally precise single-cell-resolution optogenetics. Nat Neurosci. 2017; 20(12):1796-1806. PMC: 5726564. DOI: 10.1038/s41593-017-0018-8. View

14.

Kawashima T, Kitamura K, Suzuki K, Nonaka M, Kamijo S, Takemoto-Kimura S . Functional labeling of neurons and their projections using the synthetic activity-dependent promoter E-SARE. Nat Methods. 2013; 10(9):889-95. DOI: 10.1038/nmeth.2559. View

15.

Hyun J, Nagahama K, Namkung H, Mignocchi N, Roh S, Hannan P . Tagging active neurons by soma-targeted Cal-Light. Nat Commun. 2022; 13(1):7692. PMC: 9744738. DOI: 10.1038/s41467-022-35406-y. View

16.

Hwang F, Roth R, Wu Y, Sun Y, Kwon D, Liu Y . Motor learning selectively strengthens cortical and striatal synapses of motor engram neurons. Neuron. 2022; 110(17):2790-2801.e5. PMC: 9464700. DOI: 10.1016/j.neuron.2022.06.006. View

17.

Lecoq J, Orlova N, Grewe B . Wide. Fast. Deep: Recent Advances in Multiphoton Microscopy of Neuronal Activity. J Neurosci. 2019; 39(46):9042-9052. PMC: 6855689. DOI: 10.1523/JNEUROSCI.1527-18.2019. View

18.

Lee D, Hyun J, Jung K, Hannan P, Kwon H . A calcium- and light-gated switch to induce gene expression in activated neurons. Nat Biotechnol. 2017; 35(9):858-863. DOI: 10.1038/nbt.3902. View

19.

Grewe B, Helmchen F . Optical probing of neuronal ensemble activity. Curr Opin Neurobiol. 2009; 19(5):520-9. DOI: 10.1016/j.conb.2009.09.003. View

20.

Sorensen A, Cooper Y, Baratta M, Weng F, Zhang Y, Ramamoorthi K . A robust activity marking system for exploring active neuronal ensembles. Elife. 2016; 5. PMC: 5035142. DOI: 10.7554/eLife.13918. View