Long-range population dynamics of anatomically defined neocortical networks

  1. Jerry L Chen  Is a corresponding author
  2. Fabian F Voigt
  3. Mitra Javadzadeh
  4. Roland Krueppel
  5. Fritjof Helmchen  Is a corresponding author
  1. University of Zurich, Switzerland
  2. University of Zurich, ETH Zurich, Switzerland
7 figures, 2 videos and 1 table

Figures

Figure 1 with 2 supplements
Multi-area two-photon microscope for flexible simultaneous imaging of sub-areas within a large field-of-view.

(A) Schematic of multi-area two-photon microscope. Light from a Ti:sapphire laser is split into two beams and one beam sent to a delay line. Each beam then enters a focal plane unit (FPU), which …

https://doi.org/10.7554/eLife.14679.003
Figure 1—figure supplement 1
Variation of the point-spread function over field-of-view position and ETL tuning range.

The point-spread function (PSF) was measured using 200 nm beads (Fluoresbrite Plain YG Microspheres, Polysciences Inc) at 840 nm excitation. Off-axis positions were accessed by translating a focal …

https://doi.org/10.7554/eLife.14679.004
Figure 1—figure supplement 2
Crosstalk between both sub-areas observed in vivo.

Neurons expressing YC-Nano140 were imaged with a single beam exciting fluorescence either in sub-area 1 or 2 (Average of n = 49 frames with motion correction). The detected signal in the …

https://doi.org/10.7554/eLife.14679.005
Figure 2 with 1 supplement
Simultaneous calcium imaging of identified feedforward and feedback neurons in S1 and S2 of mouse neocortex during behavior.

(A) Viral injection scheme for simultaneous labeling of feedforward and feedback neurons and YC-Nano140 expression. (B) Functional mapping of S1 and S2 through optical intrinsic signal imaging. …

https://doi.org/10.7554/eLife.14679.007
Figure 2—source data 1

Optimized low tensor rank across animals.

Table of optimum column size of each factor matrices related to neurons (N’ + N’offset), time points (T’), and trial conditions (C’) determined after cross-validation and cost function procedures for each animal used for denoising. Total possible column sizes are also indicated along with number of active neurons.

https://doi.org/10.7554/eLife.14679.008
Figure 2—figure supplement 1
Denoising with tensor decomposition.

(A) Calcium responses from one animal across multiple sessions are organized into a data tensor. The tensor is decomposed and a low-rank tensor representing denoised calcium responses is generated. …

https://doi.org/10.7554/eLife.14679.009
Figure 3 with 1 supplement
Feedback neurons in S2 exhibit behavior-related responses.

(A) General linear model (GLM) of behavior-related responses. Example of GLM fit for one neuron of calcium responses against touch, licking, and whisking as behavior events. Single-trial calcium …

https://doi.org/10.7554/eLife.14679.011
Figure 3—figure supplement 1
General linear model of whisking- and licking-related calcium responses.

(AB) Example of GLM fit for neurons showing prominent whisking [A] and licking [B] related calcium responses against touch, licking, and whisking behavior events. Single-trial calcium responses are …

https://doi.org/10.7554/eLife.14679.012
Illustration of extracting population response time courses by linear discriminant analysis.

(A) While LDA is performed on multiple simultaneously imaged neurons, for demonstration purposes, here calcium transients of two simultaneously imaged neurons within an imaging plane are plotted and …

https://doi.org/10.7554/eLife.14679.014
Figure 5 with 2 supplements
Motor behavior is associated with coordinated population activity across S1 and S2.

(A) Analysis of coordinated activity across S1 and S2. Left panel shows example of single-trial population responses for Hit trials projected along Hit vs. CR axis for simultaneously imaged S1 (LDS1)…

https://doi.org/10.7554/eLife.14679.015
Figure 5—figure supplement 1
Linear discriminant analysis across different sensory or behavior axes.

Average S1 or S2 population responses across the first second prior to and following whisker touch onset for: (A) FA vs. CR trials; (C) high- vs. low-amplitude whisking CR trials; (E) target vs. …

https://doi.org/10.7554/eLife.14679.016
Figure 5—figure supplement 2
Coordinated actitvity across S1 and S2 is not stimulus-specific.

(A) LDCCS1:S2 for target vs. non-target textures under non-task condition trials. (B) LDCCS1:S2 for P280 vs. P1200 textures for CR trials. We observed no increased or different LDCCS1:S2 between …

https://doi.org/10.7554/eLife.14679.017
Figure 6 with 3 supplements
Projection neurons contribute to coordinated S1 and S2 activity.

(A) The contribution of specific cell types to coordinated activity across S1 and S2 is measured by trial-shuffling responses for those cell types prior to calculating the LDCCS1:S2. The resulting …

https://doi.org/10.7554/eLife.14679.018
Figure 6—figure supplement 1
Measuring the contribution of specific cell types to coordinated population activity.

(A), An example of population response after trial shuffling. Trial responses of neuronal subpopulations were shuffled in order to determine their contribution to the population response. For the …

https://doi.org/10.7554/eLife.14679.019
Figure 6—figure supplement 2
Projection of shuffled trials does not alter average population response.

(A) Cumulative distribution of average peak calcium responses for each cell type. (B) Average S1 (top) or S2 (bottom) population responses projected along the Hit vs. CR axis across the first second …

https://doi.org/10.7554/eLife.14679.020
Figure 6—figure supplement 3
Contribution of S1S2 and S2S1 neurons to Hit and CR trials relative to whisker-touch onset.

(A) Contribution of S1S2 and S2S1 neurons or S1ND and S2ND neurons to coordinated S1 and S2 activity for Hit trials along the Hit vs. CR axis after aligning to whisker-touch onset (dotted line). (B) …

https://doi.org/10.7554/eLife.14679.021
Model of coordinated activity across S1 and S2.

Our results identify coordinated activity patterns across S1 and S2 that are related to motor behaviors, which could arise from common input from M1 or POm or indirect cortico-thalamocortical (CTC) …

https://doi.org/10.7554/eLife.14679.022

Videos

Video 1
In vivo z-stack of YC-Nano140 expressing neurons.

Single area images from the multi-area two-photon microscope of L2/3 neurons were taken from 70-210 µm below the pial surface at 1 µm z-step resolution. Sub-area excitation beam was delivered …

https://doi.org/10.7554/eLife.14679.006
Video 2
Simultaneous calcium imaging across S1 and S2.

Single trial video of calcium responses during texture discrimination acquired at 7 Hz with the multi-area two-photon microscope (1x playback speed). YFP (green) and CFP (blue) fluorescence from …

https://doi.org/10.7554/eLife.14679.010

Tables

Table 1

Axes used for linear discriminant analysis. Summary of trial conditions compared and used for linear discriminant analysis. For each axes, noted are potential differences in texture, licking, and …

https://doi.org/10.7554/eLife.14679.013
Axes for LDATextureLickingWhiskingUtility in analysis
Hit vs. CRDifferentDifferent (Hit)SameCannot isolate sensory, decision, or action-related responses
FA vs. CRSameDifferent (FA)SameIsolate decision and action-related responses
Pre- vs. post-touch licking (FA trials)SameDifferentSameIsolate licking-related responses
High vs. Low Whisking (CR trials)SameNoneDifferentIsolate whisking-related responses
P280 vs. P1200
(CR trials)
DifferentNoneSameIsolate sensory-related responses
Target vs. Non-target (Non-task)DifferentNoneNoneIsolate sensory-related responses

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