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Sensory and decision-related activity propagate in a cortical feedback loop during touch perception

Abstract

The brain transforms physical sensory stimuli into meaningful perceptions. In animals making choices about sensory stimuli, neuronal activity in successive cortical stages reflects a progression from sensation to decision. Feedforward and feedback pathways connecting cortical areas are critical for this transformation. However, the computational functions of these pathways are poorly understood because pathway-specific activity has rarely been monitored during a perceptual task. Using cellular-resolution, pathway-specific imaging, we measured neuronal activity across primary (S1) and secondary (S2) somatosensory cortices of mice performing a tactile detection task. S1 encoded the stimulus better than S2, while S2 activity more strongly reflected perceptual choice. S1 neurons projecting to S2 fed forward activity that predicted choice. Activity encoding touch and choice propagated in an S1–S2 loop along feedforward and feedback axons. Our results suggest that sensory inputs converge into a perceptual outcome as feedforward computations are reinforced in a feedback loop.

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Figure 1: Cellular resolution imaging of population activity in S1 and S2 during tactile detection.
Figure 2: Coding of stimulus and choice in S1 and S2.
Figure 3: Feedforward propagation of activity from S1 to S2 predicts choice.
Figure 4: Activity in a feedback loop between S2 and S1.

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Acknowledgements

We thank V. Jayaraman, R. Kerr, D. Kim, L. Looger, K. Svoboda and the HHMI Janelia Farm GENIE Project for GCaMP6. We thank S. Peron for MATLAB software, T. Shelley for instrument fabrication, and K. Severson and E. Finkel for mouse husbandry. We thank E. Finkel, D. Xu, K. Severson, B. Bari, M. Chevee, K. Svoboda, S. Brown, J. Cohen and S. Mysore for comments on the manuscript. This work was supported by the Whitehall Foundation, Klingenstein Fund, the Johns Hopkins Science of Learning Institute, NIH grant R01NS089652 (D.H.O.) and NIH core grant P30NS050274. G.M. was supported by a JSPS Postdoctoral Fellowship for Research Abroad.

Author information

Authors and Affiliations

Authors

Contributions

S.E.K. and D.H.O. planned the project. S.E.K. performed imaging, behavioral, and optogenetics experiments. H.Y. performed electrophysiology and optogenetics experiments. S.E.K. and D.H.O. analyzed data. G.M. established S2 targeting methods. S.E.K. and D.H.O. wrote the paper with comments from H.Y. and G.M.

Corresponding author

Correspondence to Daniel H O'Connor.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Behavioral task.

(a) Example session showing trials sorted by type. Ticks show lick times and are colored by trial type. Dashed line indicates auditory cue onset. Pink shading shows time window in which a single whisker was deflected on Hit and Miss trials. (b) Summary of mouse task performance across sessions used in imaging experiments (mean ± SEM). Each grey dot indicates a session. (c) Cumulative histogram of first-lick times from Hit trials (excluding those with premature licks; Online Methods) from trained mice during S1 (brown) and S2 (orange) imaging sessions. Thin lines represent pooled data from individual mice. Thick lines show mean histograms across mice. There was no significant difference in first-lick times between S1 and S2 sessions (D = 0.060, P = 0.436; 338 S1 and 502 S2 trials; Kolmogorov-Smirnov test). Dashed lines indicate median at 0.52 s.

Supplementary Figure 2 Fraction of responsive neurons encoding stimulus condition and/or choice.

Neurons (mean ± SEM across mice, from 12 sessions in S1, 10 sessions in S2) were tabulated into four categories based on DP and SP. “DP neurons” and “SP neurons” are those with 95% confidence intervals not including 0.5. Includes 274 ± 72 (mean ± SEM across mice) neurons per mouse for S1, 103 ± 26 for S2.

Supplementary Figure 3 Simultaneous imaging of S1 and S2.

(a) Left, View through a cranial imaging window implanted over S1 and S2 of a transgenic mouse (GP 4.3) expressing GCaMP6s under the Thy1 promoter. Middle, Intrinsic signal image resulting from deflection of a single whisker (B3), showing locations of S1 and S2 (brown and orange arrows, respectively). Right, Wide-field imaging of GCaMP6s shows evoked fluorescence signal in areas that overlap with those identified by ISI, confirming the locations of S1 and S2. (b) Example field of view used for simultaneous imaging of S1 and S2. (c) Example fluorescence traces concatenated across trials from S1 and S2 within the same mouse. Conventions as in Fig. 1f. (d) Example traces showing responses of an S1 neuron (top of each pair) and an S2 neuron (bottom). Traces are grouped by trial type. Dashed lines: onset of whisker stimulus. (e) Activity (mean ± SEM ΔF/F0 across 4 mice, 11 sessions total) averaged across each trial type from S1 (left, 57 ± 13 neurons per mouse, 226 total), or S2 (right, 54 ± 16 neurons per mouse, 214 total). S1 and S2 data were acquired simultaneously. Conventions as in Fig. 2a. In both S1 and S2, evoked ΔF/F0 responses on Hits were larger than on Misses (Hit – Miss mean ± [95% CI]: S1: 0.046 ± [0.035, 0.058] ΔF/F0; S2: 0.053 ± [0.035, 0.074] ΔF/F0; 11 sessions total from 4 mice; S1: t(225) = 10.60, P = 1.53 × 10−21; S2: t(213) = 7.76, P = 3.50 × 10−13; paired t-tests). (f) Mean evoked ΔF/F0 responses normalized to Hits across individual neurons in S1 and S2 (mean ± SEM across mice; circles show individual mice). The Miss/Hit response ratio was smaller in S2 compared to S1 (0.41 ± 0.06 vs 0.62 ± 0.07; z = 2.72, **P = 0.006; 226 neurons in S1; 214 neurons in S2; Wilcoxon rank sum test). (g) Cumulative histograms of noise correlations for individual pairs of S1 and S2 neurons (one neuron in each area) in Hit trials and in Miss trials. (Hit median: 0.11, Miss median: 0.09; Hit – Miss mean ± [95% CI]: 0.025 ± [0.017, 0.033]. (h) Mean noise correlations across pairs comprising an S1 neuron and an S2 neuron were slightly higher on Hits compared with Misses (0.12 ± 0.02 vs 0.10 ± 0.02, mean ± SEM across sessions; **P < 2 × 10−5; 4,910 pairs; permutation test; Hit – Miss mean ± [95% CI]: 0.025 ± [0.017, 0.033]). (i) Left, SP was higher in S1 (medians: 0.67 vs 0.65; **P = 0.003; permutation test). Middle, DP was similar in S1 and S2 (S1 median: 0.64; S2 median: 0.64; P = 0.392; permutation test). Right, The DP/SP ratio was higher in S2 (the effect was mainly due to distribution tails; S1 3rd quartile: 1.02; S2 3rd quartile: 1.04; S1 median: 0.97; S2 median: 0.98; *P = 0.023; permutation test on 3rd quartile). (j) Performance of a classifier (mean ± SEM across mice) in decoding the stimulus condition (present vs absent) from population activity at each time point. Decoding was done with each area separately (brown or orange) or with the two areas combined (black). Performance diverged for S1 & S2 combined decoder (74 ± 2%) vs individual decoders for S1 (69 ± 2%; R = 7, P = 0.037) or S2 (67 ± 6%; R = 2, P = 0.005; one-tailed Wilcoxon sign rank tests) at 0.05 s after stimulus onset. Conventions as in Fig. 2k. (k) Same as in j for decoding choice (lick vs no-lick). Decoding of choice was slightly better in S2 compared with S1 (76 ± 0.3% vs 67 ± 2% at 0.15 s; R = 41, P = 0.014; one-tailed Wilcoxon sign rank test). Performance diverged for S1 & S2 combined decoder (79 ± 1%) vs individual decoders for S1 (74 ± 1%; R = 7, P = 0.037) or S2 (76 ± 1%; R = 3, P = 0.010; one-tailed Wilcoxon sign rank tests) at 0.32 s. (i-j) Includes 9 sessions total from 3 mice (2 sessions from 1 mouse were excluded because we obtained < 3 responsive neurons in the S2 field of view).

Supplementary Figure 4 Axon clustering.

(a) Example distribution of correlation coefficients among ΔF/F0 traces from all varicosities from a session. Inset: Zoomed region showing highly correlated varicosities. Red dashed line: threshold used for clustering. (b) High correlation coefficients were exhibited by a subset of varicosities that could be identified with visual inspection as belonging to the same axon. (c) Example traces from varicosities assigned to the same cluster. (d) Fractions of varicosities that were successfully assigned to a cluster for each session.

Supplementary Figure 5 Optogenetic silencing of S1 or S2.

Behavioral task performance in the absence (black) or presence (blue) of photostimulation. Plot symbol type shows photostimulation target area (S1, circles; S2, squares; control area, diamonds). Faint symbols indicate individual mice (n = 4). Bold symbols with error bars indicate mean ± SEM across mice. Data for each mouse are means over 2–4 behavioral sessions.

Supplementary Figure 6 Assignment of mice to experimental conditions and figures.

Supplementary Figure 7 Pre-stimulus activity.

To examine pre-stimulus activity, ΔF/F0 was calculated as (FF0)/F0 where F0 was the mean over 5 baseline frames immediately preceding the auditory cue onset (frames 17:21 with auditory cue onset at frame 22). Evoked ΔF/F0 was calculated as the mean ΔF/F0 over 6 frames preceding the stimulus onset (frames 45:50 with stimulus onset between frames 52 and 53). Gray plot symbols show individual mice. Bars show means across mice. Mean ± 95% CI on Hit – Miss ΔF/F0: S1: −0.005 ± [−0.011, 3.33 × 10−4]; S2: 5.33 × 10−4 ± [−0.008, 0.009].

Supplementary Figure 8 High-speed video recording of whisking and licking.

(a) Example images acquired by high-speed video (250 Hz, 1000 frames per trial) in parallel with calcium imaging. Video allowed monitoring whisker and tongue movements. (b) To examine the effect of whisking/licking on neural activity, videos were manually inspected (51 total Go trials), and those trials that showed negligible movement prior to the median reaction time (0.5 s) were selected (24 trials). Example fluorescence traces are shown for three Hit trials (blue) and three Miss trials (black) that met our criterion. First dashed line indicates stimulus onset. Second dashed line indicates median reaction time (0.52 s after the stimulus onset). (c) Data from one session showing activity (mean ± SEM ΔF/F0 across neurons) for all Hit (blue) and all Miss (black) trials. (d) Activity (mean ± SEM ΔF/F0 across neurons) for all Hit and Miss trials with negligible movement. Green shading indicates time window devoid of whisking/licking.

Supplementary Figure 9 SP and DP values are similar when calculated using different choices of post-stimulus frames.

(a) Each row of cumulative histograms (means across mice) shows SP (left panel), DP (middle) and DP/SP ratio (right) calculated based on an evoked ΔF/F0 response measured in different 5-frame windows. The frames defining each window, and the corresponding times from stimulus onset, are indicated to the left of each row. The measurement window begins immediately after that used in Fig. 2d, and extends until approximately 917 ms following stimulus onset. Aside from choice of window, calculation of SP and DP was identical to that used in Fig. 2d (Methods). S1: 12 sessions, 5 mice, 498 ± 74 neurons per mouse; S2: 11 sessions, 5 mice, 294 ± 47 neurons per mouse. The pattern of responses is similar to that shown in Fig. 2d for all windows. P values with D statistics in parentheses: row 1: P = 2.20 × 10−4 (0.070), P = 0.060 (0.044), P = 0.002 (0.060); row 2: P = 5.14 × 10−7 (0.090), P = 0.060 (0.044), P = 0.002 (0.060), row 3: P = 9.76 × 10−6 (0.081), P = 0.041 (0.046), P = 7.15 × 10−5 (0.074), row 4: P = 8.17 × 10−8 (0.096), P = 0.051 (0.045), P = 1.76 × 10−4 (0.071). *P < 0.05; **P < 0.005; Kolmogorov–Smirnov tests. (b) Time series of SP, DP and their ratio calculated frame-by-frame (mean ± SEM across mice). Conventions as in Fig. 2.

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Kwon, S., Yang, H., Minamisawa, G. et al. Sensory and decision-related activity propagate in a cortical feedback loop during touch perception. Nat Neurosci 19, 1243–1249 (2016). https://doi.org/10.1038/nn.4356

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