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Bilateral integration in somatosensory cortex is controlled by behavioral relevance

Nature Neuroscience volume 28, pages 1300–1310 (2025)Cite this article

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Abstract

Sensory perception requires the processing of stimuli from both sides of the body. Yet, how neurons bind stimulus information across the hemispheres to create a unified percept remains unknown. Here we perform large-scale recordings from neurons in the left and right primary somatosensory cortex (S1) in mice performing a task requiring active whisker touch to coordinate stimulus features across hemispheres. When mice touched reward-associated stimuli, their whiskers moved with greater bilateral symmetry, and synchronous spiking and enhanced spike–field coupling emerged between the hemispheres. This coordinated activity was absent in stimulus-matched naive animals, indicating that interhemispheric coupling involves a goal-directed, internal process. In S1 neurons, the addition of ipsilateral touch primarily facilitated the contralateral principal whisker response. This facilitation primarily emerged for reward-associated stimuli and was lost on trials where mice failed to respond. Silencing of callosal S1 signaling reduced bilateral facilitation and interhemispheric synchrony. These results reveal a state-dependent logic that augments the flow of tactile information through the corpus callosum.

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Fig. 1: BWS reflects task engagement and reward expectation.
Fig. 2: Bilateral integration in S1 neurons emerges during reward-associated active touch.
Fig. 3: IH spike synchrony is augmented by behavioral relevance.
Fig. 4: IH spike–field phase-locking is focally enhanced in the superficial cortical layers.
Fig. 5: Bilateral integration in S1 neurons is correlated with task performance.
Fig. 6: The corpus callosum drives bilateral integration and IH spike synchrony.

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There are no access restrictions. All data presented in this article are publicly available69. Source data are provided with this paper.

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Acknowledgements

We acknowledge the members of the Pluta Lab, D. Butts, J. Veit and H. Adesnik for providing valuable feedback on the paper. This work was supported by the Whitehall Foundation (to S.R.P.), Showalter Trust (to S.R.P.) and Air Force Office of Scientific Research (FA9550-23-1-0701 to S.R.P.). Any opinions, findings and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the United States Air Force. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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  1. These authors contributed equally: Hyein Park, Hayagreev V. S. Keri.

Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, IN, USA

    Hyein Park, Hayagreev V. S. Keri, Chaeyoung Yoo, Chengyu Bi & Scott R. Pluta

  2. Department of Biomedical Engineering, Purdue University, West Lafayette, IN, USA

    Hayagreev V. S. Keri

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  1. Hyein Park
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Contributions

S.R.P. conceived and supervised the project, wrote the paper and performed a few experiments. H.P. and H.V.S.K. performed nearly all the experiments and data analysis and wrote the paper. C.Y. and C.B. performed animal training.

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Correspondence to Scott R. Pluta.

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Extended data

Extended Data Fig. 1 Task performance and behavioral dynamics during bilateral discrimination.

a, Example bilateral whisker kinematics. Top, whisker position. Middle, whisker phase. Bottom, whisker bend. Blue shadows indicate touches. b, Example high-speed video frames capturing homotopic C1 touch (top) and homotopic D1 touch (bottom) during a recording session. Blue traces represent C1 whiskers and red traces represent D1 whiskers. Yellow dots represent contact points. c, Example images from intrinsic imaging on wS1 (top and middle) to locate barrel columns corresponding to whiskers used in the task. The locations of intrinsic signals were registered with images of the superficial vasculature to guide electrode placement (bottom). d, Left, d′ of all recorded mice over training sessions (10 mice). Right, average hit and false alarm rates of the mice over training sessions. e, Average hit and false alarm rates (left) and d′ (right) of five expert mice over days of operant conditioning, followed by a control session with all whiskers trimmed. f, d′ of expert mice on the recording day (10 mice). g, Average run speed during hit and correct rejection (CR) trials (10 mice). h, Number of expert mice that showed decrease (blue), increase (red) or no significant change in BWS during the stimulus period compared to the prestimulus period for hit and CR trials. i, Percent decrease in BWS during the stimulus period compared to the prestimulus period in mice with significant BWS decrease for hit trials (4 mice) and CR trials (7 mice). j, Bilateral whisking symmetry (BWS) for all expert mice during hit trials in black and unilateral discrimination mice in gray (p = 6.3e−18, two-sample t test; 920 samples for hit trials in expert mice (20 whisker pairs in 10 mice) and 552 samples for unilateral mice (12 whisker pairs in five mice)). k, BWS of all expert mice (black, ten mice) and unilateral mice (gray) during the prestimulus period (p = 5.3e−9, two-sided Wilcoxon rank-sum test; 340 samples from 10 expert mice; 204 samples from 6 trained control mice). l, Example whisking trace during a hit trial. Top, whisker position (black) and phase (gray). Bottom, amplitude of whisking. m, Example whisking trace during a CR trial. Top, whisker position (black) and phase (gray). Bottom, amplitude of whisking. n, Whisking amplitude as a function of whisking frequency during hit trials (black) and CR trials (red) in all expert mice (10 mice—2,116 hit trials and 2,307 CR trials). o, Distribution of whisking frequencies in all expert mice (ten mice) for hit trials (black—2,116 trials) and CR trials (red—2,307 trials). p, Whisker kinematics during hit and CR trials (10 mice—2,134 hit trials and 2,296 CR trials). From top left to bottom right, box plot of whisking frequency, touch rate, standard deviation of interhemispheric touch intervals and interhemispheric touch intervals. Centerlines and bounds of boxes represent median and 25th–75th percentiles. Dots represent outliers. All error bars represent the mean ± s.e.m. All statistical tests used are two-sided.

Extended Data Fig. 2 Context-dependent bilateral facilitation is maintained across different touch dynamics.

a, Average bilateral integration indices of neurons depending on interhemispheric touch intervals (ITI). Hit and CR are shown for expert mice (10 mice, 914 neurons) and HM and HT for naive mice (7 mice, 609 neurons). ITI was calculated as difference in time between PW and ipsilateral touch. b, Distributions of bilateral integration indices for hit and CR conditions in expert mice after controlling for numbers of touches included in the calculation (p = 5.7e−16, paired-sample t test; 10 mice, 914 neurons). Index was calculated using the same number of touches within each trial (equal to the mean number of touches in hit trials). Touches that occurred later in the trial, exceeding the mean touch number, were excluded. c, Distributions of bilateral integration indices for hit and CR conditions in expert mice after removing CR trials adjacent to three consecutive miss trials (p = 1.3e−25, paired-sample t test; 10 mice, 914 neurons). CR population distribution was not significantly different from zero (p = 0.1, one-sample t test). d, Left, bilateral integration indices in mice expecting reward but not performing bilateral discrimination during HM (p = 0.4, one-sample t test; 3 mice, 99 neurons) and HT touch (p = 0.1, one-sample t test; 3 mice, 99 neurons). Right, bilateral stimulus (HT vs. HM) preference in mice expecting reward but not performing bilateral discrimination (p = 0.31, one-sample t test; 3 mice, 99 neurons). e, Left, histograms of spiking aligned to the onset of unilateral touch with the ipsilateral whisker in two example neurons. Right, box plot comparing percentage of neurons showing significant response to ipsilateral touches in expert and naive mice (p = 8.6e−4, Fisher’s exact test; expert—10 mice, 914 neurons; naive—7 mice, 609 neurons). Centerlines and bounds of boxes represent median and 25th–75th percentiles. f, Scatter plots comparing unilateral responses to ipsilateral and contralateral touch in neurons with a significant ipsilateral response. Left, expert mice (91 neurons; 10 mice). Right, naive mice (29 neurons; 7 mice). g, Percentage of neurons with significant spike facilitation or suppression during ipsilateral touch. Percentages in trained mice and naive mice are shown. All error bars represent the mean ± s.e.m. All statistical tests used are two-sided.

Extended Data Fig. 3 Bilateral stimulus preference increases with cortical depth.

a, Distribution of all recorded neurons across cortical depth in expert mice (10 mice, 914 neurons; black) and in naive mice (7 mice, 609 neurons; gray). b, Average stimulus preference of neurons in all expert mice across cortical depth (10 mice, 914 neurons). c, Best stimulus of neurons in expert mice across cortical depth (10 mice, 914 neurons).

Extended Data Fig. 4 Bilateral integration is similar between regular and fast-spiking neurons.

Characterizing neural activity comparing RS and FS neurons. a, Left, example waveforms of RS and FS neurons, showing two of the criteria used for classification. Right, scatter plot showing normalized end slope and spike width of individual FS and RS neurons (10 mice, 914 neurons; FS neurons—228, RS neurons—593 and unclassified neurons—93). Gray dots indicate unclassified neurons. b, Percentage of RS and FS cells in the population of recorded neurons (10 mice, 914 neurons). c, Percentage of RS and FS neurons across cortical depth (10 mice, 914 neurons; for FS neurons, n = 25, 73, 106 and 24 neurons for ≤400 μm, 400–600 μm, 600–900 μm and ≥900 μm; for RS neurons, n = 53, 146, 291 and 103 neurons for ≤400 μm, 400–600 μm, 600–900 μm and ≥900 μm). d, Box plot of bilateral integration indices for RS and FS neurons during hit and CR conditions (10 mice, 914 neurons; FS neurons—228 and RS neurons—593). Centerlines and bounds of boxes represent mean and 25th–75th percentiles. Dots represent outliers. e, Percentage of RS and FS cells among significantly ipsilateral neurons (10 mice, 91 neurons) in expert mice. f, Average stimulus preference index for RS and FS neurons comparing hit and CR conditions (10 mice, 914 neurons) in expert mice. Centerlines and bounds of boxes represent mean and 25th–75th percentiles. Dots represent outliers.

Extended Data Fig. 5 Bottom–up signaling cannot explain the enhanced interhemispheric synchrony in expert mice.

a, Interhemispheric touch rate as a function of touch lags for expert (n = 10 mice) and naive mice (7 mice). b, Box plot of IH touch rates for hit and correct reject trials in expert mice (p = 5.2e−4, 2-sample t test, n = 10 mice) and naive mice (p = 0.76, 2-sample t test, n = 7 mice). c, Population-averaged interhemispheric firing rates as a function of temporal lag between pairs of neurons during the baseline period in an expert mouse. Pairs of neurons with their individual firing rates during prestimulus period (Blf) greater than 4, 6, 8 and 10 Hz. d, Prestimulus IH spike rates of stimulus-responsive neurons with comparison of their baseline firing rates (Blf) >4 Hz (n = 8 mice and m = 367 cells), >6 Hz (n = 8 mice and m = 292 cells), >8 Hz (n = 8 mice and m = 238 cells) and >10 Hz (n = 8 mice and m = 194) in expert mice. e, Prestimulus IH spike rates comparing expert mice (n = 8 mice and m = 367 cells) and naive mice (n = 4 mice and m = 201 cells). Cells with Blf >4 were used for IH spike rate calculation. f, Relationship between IH touch interval (ITI) and spike coincidence (jPSTH) in expert and naive mice. g, Schematic illustrating the generation of predicted spike coincidence from the unilateral touch-triggered PSTHs. The real bilateral ITIs were used to match the temporal relationship of the unilateral touches to the actual bilateral stimulus. h, Average spike coincidence across the conditions (real vs. predicted) in expert (n = 8 mice, m = 783 cells) and naive mice (n = 4 mice, m = 409 cells). All box plots are defined with median (center), 25th percentile, 75th percentile as bounds, whiskers extending up to 1.5× interquartile range and outliers beyond this range. All error bars represent the mean ± s.e.m. All statistical tests are two-sided.

Source data

Extended Data Fig. 6 Regular-spiking cells are more strongly coupled to the opposite hemisphere.

a, Schematic illustrating the spike–field pairwise phase consistency analysis. b, Interhemispheric (IH) spike–field PPC for fast and regular-spiking cells in expert mice (FS cells: 138, RS cells: 455, 7 mice, p = 8.9e−9, one-way ANOVA) and naive mice (FS cells: 78, RS cells: 287, 4 mice, p = 0.33 one-way ANOVA). c, Percent decrease in PPC between supragranular and infragranular field potentials in expert mice (FS cells: 138, RS cells: 455, 7 mice, p = 0.73, one-way ANOVA) and naive mice (FS cells: 78, RS cells: 287, 4 mice, p = 0.95, one-way ANOVA). d, IH spike–field PPC according to laminar ___location of neuron and using the infragranular field potential. Expert mice—41 neurons in layer 2/3, 103 in layer 4, 205 in layer 5 and 106 in layer 6. Naive mice—55 neurons in layer 2/3, 84 in layer 4, 118 in layer 5 and 30 in layer 6. e, Left, histogram of spike–field phase relationships in an example neuron for hit and CR trials. Right, change in phase preference between hits and CR in population of RS cells of expert mice shown in degrees (p = 2.7e−7, signed-rank test, n = 323, 7 mice). All error bars represent the mean ± s.e.m. All statistical tests were two-sided.

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Extended Data Fig. 7 Intrahemispheric synchrony is enhanced by goal-directed processing.

a, Left, inter-neuronal firing rates between neurons in the same hemisphere in an example expert mouse. Right, mean area of inter-neuronal synchrony for all expert mice (p = 3.7e−23, signed-rank test, 867 neurons, 9 mice). b, Same as in a, but for naive mice (p = 0.87, signed-rank test, 744 neurons, 6 mice). c, Left, joint-PSTHs between neurons in same hemisphere of an example expert mouse. Right, all responsive neurons in expert mice (p = 2.3e−36, signed-rank test, 867 neurons, 9 mice). d, Same as in c, except in naive mice (p = 0.87, signed-rank test, 744 neurons, 6 mice). e, Left, within hemisphere spike–field PPC for RS cells in an example expert mouse (n = 134), Right, all stimuli responsive RS cells (p = 2.3e−11, signed-rank test, 810 neurons, 9 mice). f, Same as in e, except in naive mice (p = 0.004, signed-rank test, 743 neurons, 6 mice). g, Left, within hemisphere spike–field PPC according to horizontal ___location of field potential in an expert mouse (98 neurons). Right, all stimulus-responsive cells during hit stimulus (p = 1e−11, two-sample t test, 566 neurons, 9 mice). h, Same as in g, except in naive mice during HM stimulus (p = 4.7e−8, two-sample t test, 499 neurons, 6 mice). All error bars represent the mean ± s.e.m. All statistical tests were two-sided.

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Extended Data Fig. 8 EOPN3-mediated ipsilateral response suppression and unchanged whisker kinematics.

a, Histogram of firing rate of an example neuron aligned to the onset of ipsilateral touch during the control and light conditions. b, Scatter plot comparing ipsilateral firing rates between the control and light conditions for all neurons with a significant ipsilateral touch-evoked response (eOPN3—26 neurons in 5 mice, p = 0.01; tdTomato—15 neurons in 3 mice, p = 0.81, Wilcoxon signed-rank test). c, Rasters and histograms of trial-averaged firing rates in two example neurons aligned to the onset of ipsilateral touch during control (black) and light (magenta) trials in mice expressing eOPN3. d, Ipsilateral touch rate aligned to the onset of ipsilateral touch during control and light trials in a mouse expressing eOPN3. e, Scatter plot of the mean normalized (divided by baseline rate) firing rate of neurons during control and light trials in mice expressing eOPN3 (41 neurons in 5 mice, p = 3.7e−8, signed-rank test). f, Left, whisker curvature aligned to the onset of touch during the control and light conditions. Right, scatter plot of mean whisker curvature calculated during the control and light conditions. All error bars represent the s.e.m. All statistical tests were two-sided.

Supplementary information

Reporting Summary

Supplementary Video

Synchronized high-speed (500 fps) video from each whisker pad during tactile discrimination of bilateral space. One object on each side of the face was extended into the anterior region of the whisking fields. Mice used active touch to determine if the objects were matching or nonmatching whisker pairs. The mouse reported the presence of the Go stimulus by licking a water port. Video playback has been slowed down to 6% (30 fps) of its recorded frame rate.

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Datapoints in Fig. 3.

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Datapoints in Fig. 4.

Source Data Extended Data Fig. 5

Datapoints in Extended Data Fig. 5.

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Datapoints in Extended Data Fig. 6.

Source Data Extended Data Fig. 7

Datapoints in Extended Data Fig. 7.

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Park, H., Keri, H.V.S., Yoo, C. et al. Bilateral integration in somatosensory cortex is controlled by behavioral relevance. Nat Neurosci 28, 1300–1310 (2025). https://doi.org/10.1038/s41593-025-01960-z

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