Active information maintenance in working memory by a sensory cortex

  1. Xiaoxing Zhang
  2. Wenjun Yan
  3. Wenliang Wang
  4. Hongmei Fan
  5. Ruiqing Hou
  6. Yulei Chen
  7. Zhaoqin Chen
  8. Chaofan Ge
  9. Shumin Duan
  10. Albert Compte
  11. Chengyu T Li  Is a corresponding author
  1. Chinese Academy of Sciences, China
  2. University of Chinese Academy of Sciences, China
  3. Zhejiang University School of Medicine, China
  4. Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Spain
7 figures, 2 videos, 1 table and 1 additional file

Figures

Figure 1 with 6 supplements
The APC activity is important for the DNMS performance.

(a) Diagram of the experimental setup. (b) Design of the DNMS task. (c) Averaged licking rate of mice well-trained for the DNMS task in hit (left) and correct rejection (right) trials. Shadow, 95% …

https://doi.org/10.7554/eLife.43191.002
Figure 1—source data 1

Performance in the DNMS task.

https://doi.org/10.7554/eLife.43191.009
Figure 1—source data 2

Effect size and ANOVA statistics for optogenetics.

https://doi.org/10.7554/eLife.43191.010
Figure 1—figure supplement 1
Odor residual of the odor-delivery system.

Odor residual of the odor-delivery system, as measured by a photo-ionization detector (PID). The odor identity is labeled below each plot. Time zero marks odor onset. Odor-delivery duration was 1 s. …

https://doi.org/10.7554/eLife.43191.003
Figure 1—figure supplement 2
Location for optical fibers and range of optogenetic stimulation.

(a) Location for optical fibers, as shown by the histological images. Arrowheads indicate the tips of optical fibers. The IDs of the mice are displayed on the bottom left of each panel, for the …

https://doi.org/10.7554/eLife.43191.004
Figure 1—figure supplement 3
Single-unit spike-sorting quality.

(a) Autocorrelation of spikes from 30 example neurons. Note the clear refractory periods in all neurons. (b) All neurons that we sorted exhibited large signal-noise ratio and small false alarm rate, …

https://doi.org/10.7554/eLife.43191.005
Figure 1—figure supplement 4
Optogenetic effects on APC neurons.

(a) Four neurons with enhanced activity during laser delivery. Arrowheads in the top two panels indicate the clear peaks. The complex patterns may be due to the recurrent excitatory and inhibitory …

https://doi.org/10.7554/eLife.43191.006
Figure 1—figure supplement 5
The APC activity is important for the DNMS performance.

(a–d) Miss rate, false-alarm rate, lick efficiency and sensitivity index (d′) following the APC delay-period suppression in DNMS task with 5 s delay. *, p=0.019; ***, p<0.001; …

https://doi.org/10.7554/eLife.43191.007
Figure 1—figure supplement 6
Lick rate in the DNMS tasks.

(a–e) Lick rates of VGAT-ChR2 mice through the entire trail in laser-on and laser-off trials, for DNMS tasks with delay duration of 20 s (a), 12 s (b, c), 8 s (d) and 5 s (e). A small increase in …

https://doi.org/10.7554/eLife.43191.008
Figure 2 with 2 supplements
Varied delay and optogenetic suppression effects.

(a) Designs of the fixed delay, varied optogenetic suppression task. (b, c) Correct rates (b) and false alarm rates (c) in the fixed delay, varied optogenetic suppression task with 12 s delay. (d, e)…

https://doi.org/10.7554/eLife.43191.013
Figure 2—source data 1

Fixed delay, varied optogenetic suppression.

https://doi.org/10.7554/eLife.43191.016
Figure 2—source data 2

Fixed optogenetic suppression, varied delay duration.

https://doi.org/10.7554/eLife.43191.017
Figure 2—source data 3

Effect size and ANOVA statistics for optogenetics.

https://doi.org/10.7554/eLife.43191.018
Figure 2—figure supplement 1
Varied delay and optogenetic suppression effects.

(a, b) Miss rates in the fixed delay, varied optogenetic suppression task with 12 s delay (a) and 20 s delay duration (b). (c, d) False alarm rate (c) and miss rate (d) in the fixed optogenetic …

https://doi.org/10.7554/eLife.43191.014
Figure 2—figure supplement 2
Optogenetic suppression effect size.

(a–c) Optogenetic effect size, as measured by Cohen’s d, for the correct rate (a), miss rate (b), false alarm rate (c), for the fixed 12s-delay varied optogenetic stimulation task. (d–f) As (a–c), …

https://doi.org/10.7554/eLife.43191.015
Figure 3 with 1 supplement
The optogenetic suppression effects were not due to impaired sensory perception.

(a) Designs of the DNMS-baseline optogenetic control task. (b, c) Correct rates in the DNMS-baseline perturbation control task with 3 s perturbation and 5 s delay (b) and with 6 s and 10 s …

https://doi.org/10.7554/eLife.43191.019
Figure 3—source data 1

The optogenetic suppression effects were not due to impaired sensory perception.

https://doi.org/10.7554/eLife.43191.021
Figure 3—source data 2

Effect size and ANOVA statistics for optogenetics.

https://doi.org/10.7554/eLife.43191.022
Figure 3—source data 3

General linear model coefficients.

https://doi.org/10.7554/eLife.43191.023
Figure 3—source data 4

Task parameter combinations and general linear model fit.

https://doi.org/10.7554/eLife.43191.024
Figure 3—figure supplement 1
Learning curve for the GNG and NMS-WOD tasks.

(a) Learning curve for the correct rate in the Go/No-go (GNG) and non-match-to-sample without delay (NMS-WOD) task. (b) Optogenetic effect size, as measured by Cohen’s d, for the correct rate in the …

https://doi.org/10.7554/eLife.43191.020
Figure 4 with 2 supplements
Active memory maintenance by the APC delay activity.

(a) Design of the delayed paired association (DPA) task. (b) Correct rates following APC delay-period optogenetic suppression in the DPA task. *, p=0.038, as determined by a …

https://doi.org/10.7554/eLife.43191.025
Figure 4—source data 1

Active memory maintenance by the APC delay activity.

https://doi.org/10.7554/eLife.43191.028
Figure 4—source data 2

Effect size and ANOVA statistics for optogenetics.

https://doi.org/10.7554/eLife.43191.029
Figure 4—figure supplement 1
Active memory maintenance by the APC delay activity.

(a–d) Miss rate (a), false alarm rate (b), lick efficiency (c) and sensitivity index (d′) (d) following the APC delay-period suppression in the DPA task. *, p=0.018, from the mixed-between-within-ANO…

https://doi.org/10.7554/eLife.43191.026
Figure 4—figure supplement 2
Optogenetic suppression effect size.

(a–e) Optogenetic effect size, as measured by Cohen’s d, for the correct rate (a), miss rate (b), false alarm rate (c), lick efficiency (d) and sensitivity index (d′) (e) in the single DPA, …

https://doi.org/10.7554/eLife.43191.027
Figure 5 with 4 supplements
Neural correlates of the APC activity in the DNMS task.

(a, b) Spike raster (top) and peristimulus time histogram (PSTH, bottom) of two example neurons recorded during the DNMS task. Shadow for PSTH shows the 95% confidence intervals. Top inset: spike …

https://doi.org/10.7554/eLife.43191.030
Figure 5—figure supplement 1
Design and implementation of the op-tetrodes.

(a–c) Microdrive, tetrode and recording sites. Images of the microdrive (a), tetrode (b) (electron microscopy scale bar, 20 μm) and examples of recording sites (c) (indicated by arrows).

https://doi.org/10.7554/eLife.43191.031
Figure 5—figure supplement 2
Neural correlates of the APC activity in the DNMS task.

(a–i) As in Figure 5a,c,d), for three more example neurons. (j) Distribution of the auROC for all the recorded neurons during the 4s-delay in DNMS tasks in the correct trials. (k) As in (I), but in …

https://doi.org/10.7554/eLife.43191.032
Figure 5—figure supplement 3
Neural correlates of the APC activity in the DNMS task.

(a) Activity of neurons in the DNMS task with odor S1 (left) and S2 (right) as sample. Color: firing rates (FR) in Z-scores. Neurons were aligned according to the FRS1–FRS2 values during the delay …

https://doi.org/10.7554/eLife.43191.033
Figure 5—figure supplement 4
Selective neurons randomly distributed in different mice.

(a–d) Number of single units recorded for different mice, for sample delivery (a–b) or for the last second of the delay period (c–d). Note that selective neurons are randomly distributed in …

https://doi.org/10.7554/eLife.43191.034
Neural correlates of APC activity in the multiple-sample DPA task.

(a) Design of the multiple-sample DPA (MS-DPA) task. (b) Averaged daily performance of well-trained mice in the MS-DPA task. (c) Mutual information of the APC neurons for the sample odors in the …

https://doi.org/10.7554/eLife.43191.035
Neural correlates of the APC activity in dual-task experiments.

(a) Example neuron with mixed DPA-sample and GNG-task odor-cue information in the dual-task. Bottom bars, p<0.001 for DPA sample (red) and GNG cue (blue), two-tailed permutation test of 1000 …

https://doi.org/10.7554/eLife.43191.036

Videos

Video 1
Performance of a delayed non-match to sample task in mice.
https://doi.org/10.7554/eLife.43191.011
Video 2
Continuous video recording of mice performing a DNMS task with 20s-delay.
https://doi.org/10.7554/eLife.43191.012

Tables

Key resources table
Reagent type
(species) or
resource
DesignationSource or referenceIdentifiersAdditional
information
Strain, strain background
(Mus musculus)
VGAT-CHR2:B6.Cg-Tg(Slc32a1-COP4*H134R/EYFP)8Gfng/JDr. Guoping Feng (Zhao et al., 2011)VGAT-ChR2-EYFP line 8
Antibodygoat polyclonal anti-GFP (FITC)AbcamRRID: AB_305635(1:200)
Antibodyrabbit polyclonal anti-c-FosSynaptic SystemsRRID: AB_2231974(1:1000)
AntibodyCy5 goat polyclonal anti-rabbitJacksonRRID: AB_2338013(1:2000)
Chemical compound, drugDAPIBeyotimecatalog number: C1002
Chemical compound, drugpropyl formateSigma-Aldrichcatalog number: 245852
Chemical compound, drugbutyl formateSigma-Aldrichcatalog number: 261521
Chemical compound, drugmethyl butyrateSigma-Aldrichcatalog number: 246093
Chemical compound, drug3-methyl-2-buten-1-olSigma-Aldrichcatalog number: W364703
Chemical compound, drug1-butanolSigma-Aldrichcatalog number: B7906
Chemical compound, drug1-pentanolSigma-Aldrichcatalog number: 398268
Chemical compound, drugethyl propionateSigma-Aldrichcatalog number: 112305
Chemical compound, drugpropyl acetateSigma-Aldrichcatalog number: 133108
Software, algorithmMATLABMathWorksRRID: SCR_001622
Software, algorithmLIBSVMhttps://www.csie.ntu.edu.tw/~cjlin/libsvm/RRID: SCR_010243

Additional files

Download links