Simultaneous Cellular-resolution Optical Perturbation and Imaging of Place Cell Firing Fields

Overview

Journal Nat Neurosci

Date 2014 Nov 18

PMID 25402854

Citations 187

Authors

John Peter Rickgauer

Karl Deisseroth

David W Tank

Affiliations

Soon will be listed here.

Abstract

Linking neural microcircuit function to emergent properties of the mammalian brain requires fine-scale manipulation and measurement of neural activity during behavior, where each neuron's coding and dynamics can be characterized. We developed an optical method for simultaneous cellular-resolution stimulation and large-scale recording of neuronal activity in behaving mice. Dual-wavelength two-photon excitation allowed largely independent functional imaging with a green fluorescent calcium sensor (GCaMP3, λ = 920 ± 6 nm) and single-neuron photostimulation with a red-shifted optogenetic probe (C1V1, λ = 1,064 ± 6 nm) in neurons coexpressing the two proteins. We manipulated task-modulated activity in individual hippocampal CA1 place cells during spatial navigation in a virtual reality environment, mimicking natural place-field activity, or 'biasing', to reveal subthreshold dynamics. Notably, manipulating single place-cell activity also affected activity in small groups of other place cells that were active around the same time in the task, suggesting a functional role for local place cell interactions in shaping firing fields.

Citing Articles

Theoretical analysis of low-power deep synergistic sono-optogenetic excitation of neurons by co-expressing light-sensitive and mechano-sensitive ion-channels.

Roy S, Pyari G, Bansal H Commun Biol. 2025; 8(1):379.

PMID: 40050670 PMC: 11885482. DOI: 10.1038/s42003-025-07792-8.

TWINKLE: An open-source two-photon microscope for teaching and research.

Schottdorf M, Rich P, Diamanti E, Lin A, Tafazoli S, Nieh E PLoS One. 2025; 20(2):e0318924.

PMID: 39946384 PMC: 11824991. DOI: 10.1371/journal.pone.0318924.

TWINKLE: An open-source two-photon microscope for teaching and research.

Schottdorf M, Rich P, Diamanti E, Lin A, Tafazoli S, Nieh E bioRxiv. 2024; .

PMID: 39386506 PMC: 11463478. DOI: 10.1101/2024.09.23.612766.

Two-photon all-optical neurophysiology for the dissection of larval zebrafish brain functional and effective connectivity.

Turrini L, Ricci P, Sorelli M, De Vito G, Marchetti M, Vanzi F Commun Biol. 2024; 7(1):1261.

PMID: 39367042 PMC: 11452506. DOI: 10.1038/s42003-024-06731-3.

NeuroART: Real-Time Analysis and Targeting of Neuronal Population Activity during Calcium Imaging for Informed Closed-Loop Experiments.

Bowen Z, De Zoysa D, Shilling-Scrivo K, Aghayee S, Di Salvo G, Smirnov A eNeuro. 2024; 11(10).

PMID: 39266327 PMC: 11485737. DOI: 10.1523/ENEURO.0079-24.2024.

References

Galarreta M, HESTRIN S . Spike transmission and synchrony detection in networks of GABAergic interneurons. Science. 2001; 292(5525):2295-9. DOI: 10.1126/science.1061395. View

Zhang F, Wang L, Brauner M, Liewald J, Kay K, Watzke N . Multimodal fast optical interrogation of neural circuitry. Nature. 2007; 446(7136):633-9. DOI: 10.1038/nature05744. View

Greenberg D, Houweling A, Kerr J . Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat Neurosci. 2008; 11(7):749-51. DOI: 10.1038/nn.2140. View

Ziv Y, Burns L, Cocker E, Hamel E, Ghosh K, Kitch L . Long-term dynamics of CA1 hippocampal place codes. Nat Neurosci. 2013; 16(3):264-6. PMC: 3784308. DOI: 10.1038/nn.3329. View

Packer A, Peterka D, Hirtz J, Prakash R, Deisseroth K, Yuste R . Two-photon optogenetics of dendritic spines and neural circuits. Nat Methods. 2012; 9(12):1202-5. PMC: 3518588. DOI: 10.1038/nmeth.2249. View

Harvey C, Collman F, Dombeck D, Tank D . Intracellular dynamics of hippocampal place cells during virtual navigation. Nature. 2009; 461(7266):941-6. PMC: 2771429. DOI: 10.1038/nature08499. View

Denk W, Strickler J, Webb W . Two-photon laser scanning fluorescence microscopy. Science. 1990; 248(4951):73-6. DOI: 10.1126/science.2321027. View

Dana H, Chen T, Hu A, Shields B, Guo C, Looger L . Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo. PLoS One. 2014; 9(9):e108697. PMC: 4177405. DOI: 10.1371/journal.pone.0108697. View

Guo Z, Hart A, Ramanathan S . Optical interrogation of neural circuits in Caenorhabditis elegans. Nat Methods. 2009; 6(12):891-6. PMC: 3108858. DOI: 10.1038/nmeth.1397. View

10.

St-Pierre F, Marshall J, Yang Y, Gong Y, Schnitzer M, Lin M . High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci. 2014; 17(6):884-9. PMC: 4494739. DOI: 10.1038/nn.3709. View

11.

Yizhar O, Fenno L, Prigge M, Schneider F, Davidson T, OShea D . Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature. 2011; 477(7363):171-8. PMC: 4155501. DOI: 10.1038/nature10360. View

12.

Yaroslavsky A, Schulze P, Yaroslavsky I, SCHOBER R, Ulrich F, Schwarzmaier H . Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range. Phys Med Biol. 2002; 47(12):2059-73. DOI: 10.1088/0031-9155/47/12/305. View

13.

Andrasfalvy B, Zemelman B, Tang J, Vaziri A . Two-photon single-cell optogenetic control of neuronal activity by sculpted light. Proc Natl Acad Sci U S A. 2010; 107(26):11981-6. PMC: 2900666. DOI: 10.1073/pnas.1006620107. View

14.

Petreanu L, Gutnisky D, Huber D, Xu N, OConnor D, Tian L . Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature. 2012; 489(7415):299-303. PMC: 3443316. DOI: 10.1038/nature11321. View

15.

Akerboom J, Carreras Calderon N, Tian L, Wabnig S, Prigge M, Tolo J . Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci. 2013; 6:2. PMC: 3586699. DOI: 10.3389/fnmol.2013.00002. View

16.

Petreanu L, Huber D, Sobczyk A, Svoboda K . Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci. 2007; 10(5):663-8. DOI: 10.1038/nn1891. View

17.

Mattis J, Tye K, Ferenczi E, Ramakrishnan C, OShea D, Prakash R . Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat Methods. 2011; 9(2):159-72. PMC: 4165888. DOI: 10.1038/nmeth.1808. View

18.

Prakash R, Yizhar O, Grewe B, Ramakrishnan C, Wang N, Goshen I . Two-photon optogenetic toolbox for fast inhibition, excitation and bistable modulation. Nat Methods. 2012; 9(12):1171-9. PMC: 5734860. DOI: 10.1038/nmeth.2215. View

19.

Adamantidis A, Zhang F, Aravanis A, Deisseroth K, De Lecea L . Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature. 2007; 450(7168):420-4. PMC: 6744371. DOI: 10.1038/nature06310. View

20.

Kaifosh P, Lovett-Barron M, Turi G, Reardon T, Losonczy A . Septo-hippocampal GABAergic signaling across multiple modalities in awake mice. Nat Neurosci. 2013; 16(9):1182-4. DOI: 10.1038/nn.3482. View