Abstract
How the somatosensory cortex (S1) encodes complex patterns of touch, such as those that occur during tactile exploration, is poorly understood. In the mouse whisker S1, temporally dense stimulation of local whisker pairs revealed that most neurons are not classical single-whisker feature detectors, but instead are strongly tuned to two-whisker sequences that involve the columnar whisker (CW) and one specific surround whisker (SW), usually in a SW-leading-CW order. Tuning was spatiotemporally precise and diverse across cells, generating a rate code for local motion vectors defined by SW–CW combinations. Spatially asymmetric, sublinear suppression for suboptimal combinations and near-linearity for preferred combinations sharpened combination tuning relative to linearly predicted tuning. This resembles computation of motion direction selectivity in vision. SW-tuned neurons, misplaced in the classical whisker map, had the strongest combination tuning. Thus, each S1 column contains a rate code for local motion sequences involving the CW, thus providing a basis for higher-order feature extraction.
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Data availability
Data are available in the Collaborative Research in Computational Neuroscience repository at https://crcns.org.
Code availability
The Matlab code for performing the statistical and data analyses are available upon request to the corresponding author.
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Acknowledgements
This work was supported by NIH 1R37 NS092367 (to D.E.F.), a NSF Graduate Research Fellowship (to K.J.L.-J.) and a NIH F99/K00 award (to K.J.L.-J.). The authors thank the members of the Feldman Lab for insightful comments and suggestions to the manuscript. They also thank J. Benson and C. Shi for performing behavioral training, and H.-C. Wang for developing behavioral methods, for experiment 3.
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K.J.L.-J. designed, performed and analyzed the results of the experiments. T.L. performed the awake recordings. S.A. performed the spike sorting. D.E.F. supervised the project. K.J.L.-J. and D.E.F. wrote the paper.
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Peer review information: Nature Neuroscience thanks Sylvain Crochet and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Integrated supplementary information
Supplementary Figure 1 Diverse single-whisker tuning in within the S1 column.
(a) Average PSTH response to single whisker deflections across all units (n = 142). (b) Top, single-whisker tuning curves of 6 example units that were recorded in the same penetration of the D1 column. Bottom, multiunit activity across layers, multiunit activity was the number of voltage transients that exceeded 3 standard deviations of baseline. Shaded regions are SEM. (c) Fraction of units that had their peak single-whisker response to CW deflections (CW-tuned units, n = 89) across layers. Error bars are SE of sample proportion. (d) Average single-whisker receptive fields of CW (n = 89) and SW-tuned (n = 53) units. Responses were normalized to each unit’s maximum spiking response and surround whiskers were ranked by response strength. Tuning was broader for SW-tuned units (1-factor ANOVA on ranked tuning curves, p=.0003). bSW is the best surround whisker.
Supplementary Figure 2 SW-tuned units have the sharpest CW-SW sequence tuning.
Tuning sharpness, quantified as lifetime sparseness, among different sets of pairwise whisker sequences. Within each set, sequences were ranked from strongest to weakest spiking response, and lifetime sparseness was calculated for increasing number of sequences ranked. Thus, tuning sharpness can be compared between the N best CW-SW sequences and the N best SW-SW sequences (at X=N on the x-axis). Shaded regions are SEM.
Supplementary Figure 3 Diversity of combination tuning in S1.
Combination tuning curves of 30 combination-selective units, chosen to be representative of the population. Asterisks denote peak responses. Best Δt’s are shown in the top left of each unit.
Supplementary Figure 4 Relationship between firing rate and combination selectivity (CSI).
(a) Mean relationship between CSI and evoked firing rate to the best combination stimulus (large circles: mean, bars: SEM), for all combination-selective (n = 187) and non-selective (n = 264) units in Experiment 2. For stimuli at best Δt. Small circles are individual units. (b) Distribution of mean evoked firing rate for best CW-SW combinations at best Δt. Each histogram bar corresponds to a firing rate bin from (a). (c) Mean peak-aligned combination-tuning curves for combination-selective units with low firing rate (<0.81 spikes/stim, corresponding to the first two bins in (a) and (b). N = 95 units. Left, tuning calculated from total spiking. Right, tuning calculated after subtraction of mean spontaneous firing rate of each unit. Grey, tuning observed after shuffling spike counts across stimuli and trials. (d), Same as (c), but for combination-selective high firing rate units (>= 0.81 spikes/stim, corresponding to bins 3–10 in (a) and (b). N = 92 units. (e), Same as (d), but for non-selective high firing rate units. N = 91 units. Shaded regions are SEM. Asterisks in c–e indicate best combination.
Supplementary Figure 5 Somatotopic bias of combination tuning in S1.
(a) Average, rate normalized, combination tuning curves for combination-selective (n = 187) and non-selective units (n = 264). (b) Average combination selectivity across combination-selective units that prefer a specific CW-SW combination. Each point at each angle is the average CSI of units that prefer the corresponding CW-SW combination. Error bars are SEM. D, V, R and C indicate dorsal, ventral, rostral and caudal neighboring whiskers on the whisker pad.
Supplementary Figure 6 Properties of combination tuning across layers.
Data are for all whisker-responsive cells in each layer, not just for combination-selective units (L2/3: 108 units; L4: 157 units; L5: 141 units; L6: 45 units. (a) Log10 CSI across layers for combination-selective units. Open circles are individual units, red line is the mean and shaded region is the 95% confidence interval. Asterisks denote statistically significant differences (1-factor ANOVA, p=.0025). (b) Fraction of combination-selective units across layers. Error bars are SE of sample proportion. (c) Average polar tuning curves aligned to the best stimulus for each layer. Axes are in spikes per stimulus and are the same across all plots. Shaded regions are SEM.
Supplementary Figure 7 Full data distributions for linear and nonlinear components of combination tuning.
Left and right columns are combination-selective (n = 187) and non-selective units (n = 264). These are the individual data points underlying the analysis of linear and nonlinear components of combination tuning in Fig. 6. Each dot is one unit. (a) Combination-specific enhancement (positive) or suppression (negative), relative to the global 0.64x-sublinearity, as a function of CW-SW combination rank. Open circles are individual units, red line is mean and shaded region is 95% confidence intervals. (b) and (c) Same as (a) but for measured combination-evoked response (b) and linear predicted response (c). (d) Combination-specific enhancement or suppression for CW-SW combinations as a function of the rank of single-whisker SW stimulus.
Supplementary Figure 8 Rate coding for CW-SW sequence order in S1.
(a) Average performance of a neural population decoder that predicts sequence order (inbound -Δt vs. outbound +Δt) based on single-trial spiking activity. The decoder was constructed as in Fig. 3 and 4. For this analysis, –Δt was defined as the [−50 ms, −10 ms] range, and +Δt was defined as the [+10 ms, +50 ms] range. Only responses to best whisker combinations were used in this analysis. Performance of the order decoder was ~65% correct on hold-out trials for N=100 units, relative to chance performance of 50%. Shaded region is SD across 2500 bootstrap trials. (b) Decoding performance across different combination identities. The order of each CW-SW combination was decoded from units that had that combination as their best combination. S1 units tuned to different spatial CW-SW combinations provided equally accurate order decoding.
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Laboy-Juárez, K.J., Langberg, T., Ahn, S. et al. Elementary motion sequence detectors in whisker somatosensory cortex. Nat Neurosci 22, 1438–1449 (2019). https://doi.org/10.1038/s41593-019-0448-6
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DOI: https://doi.org/10.1038/s41593-019-0448-6
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