Visualizing mammalian brain area interactions by dual-axis two-photon calcium imaging

Fluorescence Ca2+ imaging enables large-scale recordings of neural activity, but collective dynamics across mammalian brain regions are generally inaccessible within single fields of view. Here we introduce a two-photon microscope possessing two articulated arms that can simultaneously image two brain areas (∼0.38 mm2 each), either nearby or distal, using microendoscopes. Concurrent Ca2+ imaging of ∼100–300 neurons in primary visual cortex (V1) and lateromedial (LM) visual area in behaving mice revealed that the variability in LM neurons' visual responses was strongly dependent on that in V1, suggesting that fluctuations in sensory responses propagate through extended cortical networks.

[1]  Michael Unser,et al.  A pyramid approach to subpixel registration based on intensity , 1998, IEEE Trans. Image Process..

[2]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[3]  A. Mehta,et al.  Multiphoton endoscopy: optical design and application to in vivo imaging of mammalian hippocampal neurons , 2003, Conference on Lasers and Electro-Optics, 2003. CLEO '03..

[4]  Karel Svoboda,et al.  ScanImage: Flexible software for operating laser scanning microscopes , 2003, Biomedical engineering online.

[5]  Bert Sakmann,et al.  Supralinear Ca2+ Influx into Dendritic Tufts of Layer 2/3 Neocortical Pyramidal Neurons In Vitro and In Vivo , 2003, The Journal of Neuroscience.

[6]  A. Mehta,et al.  In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy. , 2004, Journal of neurophysiology.

[7]  R. Tsien,et al.  Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein , 2004, Nature Biotechnology.

[8]  Bartlett W. Mel,et al.  Computational subunits in thin dendrites of pyramidal cells , 2004, Nature Neuroscience.

[9]  S. Arber,et al.  A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling , 2005, PLoS biology.

[10]  E. Cocker,et al.  In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. , 2005, Optics letters.

[11]  A. Zvyagin.  Multiphoton endoscopy , 2007 .

[12]  D. Tank,et al.  Imaging Large-Scale Neural Activity with Cellular Resolution in Awake, Mobile Mice , 2007, Neuron.

[13]  David S. Greenberg,et al.  Visually evoked activity in cortical cells imaged in freely moving animals , 2009, Proceedings of the National Academy of Sciences.

[14]  Mark J. Schnitzer,et al.  Automated Analysis of Cellular Signals from Large-Scale Calcium Imaging Data , 2009, Neuron.

[15]  A. Nimmerjahn,et al.  Motor Behavior Activates Bergmann Glial Networks , 2009, Neuron.

[16]  Olav Solgaard,et al.  In vivo brain imaging using a portable 2.9 g two-photon microscope based on a microelectromechanical systems scanning mirror. , 2009, Optics letters.

[17]  Rafael Yuste,et al.  Fast nonnegative deconvolution for spike train inference from population calcium imaging. , 2009, Journal of neurophysiology.

[18]  R. Reid,et al.  Frontiers in Cellular Neuroscience Cellular Neuroscience Methods Article , 2022 .

[19]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

[20]  Lin Tian,et al.  Functional imaging of hippocampal place cells at cellular resolution during virtual navigation , 2010, Nature Neuroscience.

[21]  T. M. Esdaille,et al.  Dark Light, Rod Saturation, and the Absolute and Incremental Sensitivity of Mouse Cone Vision , 2010, The Journal of Neuroscience.

[22]  Allan R. Jones,et al.  A robust and high-throughput Cre reporting and characterization system for the whole mouse brain , 2009, Nature Neuroscience.

[23]  Yaniv Ziv,et al.  Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy , 2011, Nature Medicine.

[24]  A. Gamal,et al.  Miniaturized integration of a fluorescence microscope , 2011, Nature Methods.

[25]  James H. Marshel,et al.  Functional Specialization of Seven Mouse Visual Cortical Areas , 2011, Neuron.

[26]  Demetris K. Roumis,et al.  Functional Specialization of Mouse Higher Visual Cortical Areas , 2011, Neuron.

[27]  Georg B. Keller,et al.  Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse , 2012, Neuron.

[28]  Olaf Sporns,et al.  Network Analysis of Corticocortical Connections Reveals Ventral and Dorsal Processing Streams in Mouse Visual Cortex , 2012, The Journal of Neuroscience.

[29]  Winfried Denk,et al.  Miniaturization of two-photon microscopy for imaging in freely moving animals. , 2013, Cold Spring Harbor protocols.

[30]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[31]  Lacey J. Kitch,et al.  Long-term dynamics of CA1 hippocampal place codes , 2013, Nature Neuroscience.

[32]  Lindsey L. Glickfeld,et al.  Cortico-cortical projections in mouse visual cortex are functionally target specific , 2013, Nature Neuroscience.