3D directional tuning in the orofacial sensorimotor cortex during natural feeding and drinking
- Department of Oral Health Sciences, School of Dentistry, University of Washington, United States
- Division of Neuroscience, Washington National Primate Research Center, University of Washington, United States
- Graduate Program in Neuroscience, University of Washington, United States
Figures
Figure 1
Direction of tongue motion in each behavioral task.
(A) Schematic of the location of three spouts, left (L), middle (M), and right (R), for the drinking task. Tongue direction was categorized based on spout location. (B) Calculation of 3D tongue direction during feeding. θ is the instantaneous 3D direction of the tongue tip over a 100 ms interval between its positions at t1 and t2, where t1=0 and t2=t1+100. The dotted line shows the actual trajectory during this interval.
Figure 2 with 2 supplements
Examples of single neuron activity in relation to tongue direction.
(A) Each peri-event time histogram (PETH and ±1 SE, smoothed by a 25 ms Gaussian kernel) corresponds to spiking activity for a specific range of tongue direction for feeding trials. Dashed lines indicate 100 ms interval used for calculating the tongue direction. (B) PETHs for drinking trials with the same spout, centered at the point of minimum protrusion of the tongue (0 s). Percent tongue displacement along the anterior-posterior axis is shown in gray, with shaded area representing ±1 SD. Vertical lines indicate 500 ms interval used for tuning analysis.
Figure 2—figure supplement 1
Directional neural responses across trials.
Raster plots corresponding to the same neurons represented in Figure 2. All trials in the respective dataset are included, grouped by direction.
Figure 2—figure supplement 2
Microelectrode array locations.
Squares represent Utah arrays and rectangles represent floating microelectrode arrays. Drawing is to scale and array locations were taken from surgical photographs. Adapted from Supplementary Figure 8 of ‘Robust cortical encoding of 3D tongue shape during feeding in macaques’ (Laurence-Chasen et al., 2023).
Figure 3 with 2 supplements
Directional tuning of neurons during control tasks.
(A) 3D firing rate map of a neuron in MIo during feeding. Smaller inset plots are 1D tuning curves across each axis. (B) Percentage of neurons tuned to direction, combined for both subjects. Recordings were taken from four areas of the orofacial sensorimotor cortex (OSMCx): rMIo - rostral M1 (n = 57, 54), cMIo - caudal M1 (n = 201, 289), SIo(3a/3b) - area 3a/3b (n = 27, 39), and SIo(1/2) - area 1/2 (n = 66, 117). Error bars represent ±1 SE.
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Figure 3—source data 1
Figure 3B: Percentage of directionally tuned neurons.
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Figure 3—figure supplement 1
Proportion of feeding trials in each group of directions.
Error bars represent ±1 standard deviation across datasets (n = 4).
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Figure 3—figure supplement 1—source data 1
Number of feeding trials in each group of directions.
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Figure 3—figure supplement 2
Proportion of neurons directionally modulated during chews vs. swallows in both monkeys.
Recordings were taken from four areas of the orofacial sensorimotor cortex (OSMCx): rMIo - rostral M1 (n = 29, 28), cMIo - caudal M1 (n = 125, 76), SIo(3a/3b) - area 3a/3b (n = 9, 18), and SIo(1/2) - area 1/2 (n = 29, 37). Error bars represent ±1 SE.
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Figure 3—figure supplement 2—source data 1
Directionally modulated neurons during chews versus swallows.
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Figure 4
Directional tuning to yaw and pitch during feeding.
(A) Firing rate maps of a neuron in MIo and in SIo across yaw and pitch angles. Firing rates were averaged across all 100 ms feeding intervals within a 10° range. (B) Proportion of neurons tuned to yaw and pitch, combined for both subjects. Recordings were taken from four areas of the orofacial sensorimotor cortex (OSMCx): rMIo - rostral M1 (n = 57, 54), cMIo - caudal M1 (n = 201, 289), SIo(3a/3b) - area 3a/3b (n = 27, 39), and SIo(1/2) - area 1/2 (n = 66, 117). Error bars represent ±1 SE.
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Figure 4—source data 1
Figure 4B: Proportion of neurons tuned to yaw and pitch.
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Figure 5
Cosine tuning of MIo and SIo neurons.
(A) Distribution of 3D preferred directions in unit sphere for neurons that fit the tuning function during feeding, combined for both subjects. The origin represents the start of a movement. Color bar represents posterior-anterior axis. (B) Distribution of the index for the depth of directional tuning, combined for both subjects (n = 170, 34).
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Figure 5—source data 1
Figure 5A: Distribution of 3D preferred directions.
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Figure 5—source data 2
Figure 5B: Distribution of directional index.
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Figure 6
Distribution of preferred directions (PDs) in MIo (yellow) and SIo (purple) neurons during control feeding (A) and drinking (B).
For the feeding task, polar plots are split into 10° bins with thick colored lines representing the mean PD. For the drinking task, error bars represent ±1 SE. Neuron counts are included in Appendix 1—table 1.
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Figure 6—source data 1
Figure 6A: Distribution of preferred directions (PDs) during control feeding.
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Figure 6—source data 2
Figure 6B: Distribution of preferred directions (PDs) during control drinking.
- https://cdn.elifesciences.org/articles/101325/elife-101325-fig6-data2-v1.xlsx
Figure 7 with 7 supplements
Neural population trajectories vary across directions.
Trial-averaged trajectories of MIo and SIo population activity along the first three latent factors for Monkey R, grouped by direction. Axes for SIo are 1/4 scale of MIo. Arrows indicate the end of the trajectory. Percentages denote the sum of the variance explained by the first three factors. Inset plots show the difference between the normalized inter-trajectory distances of MIo and SIo over time for both feeding and drinking.
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Figure 7—source data 1
Neural population trajectories.
- https://cdn.elifesciences.org/articles/101325/elife-101325-fig7-data1-v1.xlsx
Figure 7—figure supplement 1
Comparison of cumulative explained variance between feeding and drinking behaviors with an equal number of neurons (N = 24) for both subjects.
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Figure 7—figure supplement 1—source data 1
Cumulative explained variance for feeding and drinking with equal neurons.
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Figure 7—figure supplement 2
Population trajectories of stable neurons.
Comparison between stable MIo (N = 20) neural population trajectories in feeding and drinking behaviors for (A) all trials 200 ms around minimum gape and (B) a subset of trials (feeding: N = 40, drinking: N = 175) with similar kinematics 100 ms after minimum tongue protrusion. Dots represent each 10 ms time bin, and the arrow represents the end of the trajectory. Data from Monkey R.
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Figure 7—figure supplement 2—source data 1
Comparison between stable MIo neural population trajectories.
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Figure 7—figure supplement 3
Effect of subsampling (A) equal number of trials per direction (N = 80) from MIo and (B) equivalent neuron counts from MIo and SIo populations (N = 24) on the cumulative variance explained by latent factors.
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Figure 7—figure supplement 3—source data 1
Effect of subsampling on cumulative explained variance.
- https://cdn.elifesciences.org/articles/101325/elife-101325-fig7-figsupp3-data1-v1.xlsx
Figure 7—video 1
First three latent variables for trial-averaged neural population trajectories of MIo neurons of Monkey R during control feeding task, grouped by direction.
Figure 7—video 2
First three latent variables for trial-averaged neural population trajectories of MIo neurons of Monkey R during control drinking task, grouped by direction.
Figure 7—video 3
First three latent variables for trial-averaged neural population trajectories of SIo neurons of Monkey R during nerve-blocked feeding task, grouped by direction.
Figure 7—video 4
First three latent variables for trial-averaged neural population trajectories of SIo neurons of Monkey R during nerve-blocked drinking task, grouped by direction.
Figure 8
Effect of nerve block on direction of tongue movement.
(A) Distribution of tongue directions during feeding. (B) Variance in 3D trajectory endpoints during drinking (posterior-anterior, inferior-superior, left-right) for each direction: left (L), middle (M), and right (R). (C) Variation in the distance of drinking endpoint positions from the mean endpoint. Left halves of hemi-violins (black) are control and right halves (red) are nerve block for an individual. Horizontal black lines represent the mean and horizontal red lines the median. Results of two-tailed t-test and F-test are indicated by asterisks and crosses, respectively: *,†p<0.05; **,††p<0.01; ***,†††p<0.001. Smaller inset plots show that there was no effect in the sham nerve block condition, for reference. The sham procedure was identical to the nerve block, except the anesthetic was substituted with saline solution.
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Figure 8—source data 1
Figure 8A: Distribution of directions during feeding.
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Figure 8—source data 2
Figure 8B: Variance in 3D position of drinking trajectory endpoints.
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Figure 8—source data 3
Figure 8C: Variation in the distance of drinking endpoints from mean.
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Figure 9
Effect of nerve block on drinking kinematics in Monkey R.
(A) Tongue tip trajectories from starting position to one of three drinking spouts in the control and nerve block conditions. (B) Drinking trajectory endpoints, where the black dot represents the mean endpoint position.
Figure 10 with 2 supplements
Effects of nerve block on directional tuning of orofacial sensorimotor cortex (OSMCx) neurons during feeding and drinking tasks.
(A) Percentage of directionally tuned neurons in four areas: rMIo - rostral M1, cMIo - caudal M1, SIo(3a/3b) - area 3a/3b, and SIo(1/2) - area 1/2. Filled-in bars represent control while empty bars represent nerve block. Error bars represent ±1 SE. Neuron counts are included in Appendix 1—table 1. (B) Percentage of MIo and SIo neurons which gained or lost directionality with the addition of nerve block.
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Figure 10—source data 1
Figure 10A: Percentage of directionally tuned neurons.
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Figure 10—source data 2
Figure 10B: Percentage of neurons that gained or lost directionality with the addition of nerve block.
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Figure 10—figure supplement 1
Effect of subsampling drinking trials with similar kinematic profiles on the change in proportion of directionally tuned neurons in control vs. nerve block conditions for both subjects.
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Figure 10—figure supplement 1—source data 1
Effect of subsampling drinking trials with similar kinematics.
- https://cdn.elifesciences.org/articles/101325/elife-101325-fig10-figsupp1-data1-v1.xlsx
Figure 10—figure supplement 2
Change in firing rates of cortical somatosensory neurons.
A decrease in firing rate in over 50% of SIo neurons was the criterion for a successful nerve block. Red bars indicate a relative decrease in firing rate for a given electrode, while blue bars indicate an increase. Only electrodes for which the control baseline firing rate was greater than 3 spikes/s are shown. Adapted from Supplementary Figure 6 of ‘Loss of oral sensation impairs feeding performance and consistency of tongue-jaw coordination’ (Laurence-Chasen et al., 2022).
Figure 11
Effects of nerve block on the distribution of preferred directions (PDs) of MIo (yellow) and SIo (purple) neurons.
(A) For the feeding task, polar plots are split into 10° bins with thick colored lines representing the mean PD. Significant circular concentration test (k-test) comparing control and nerve block are indicated by asterisks: *p<0.05; **p<0.01; ***p<0.001. (B) For the drinking task, error bars represent ±1 SE. Filled-in bars represent control while empty bars represent nerve block. Neuron counts are included in Appendix 1—table 1.
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Figure 11—source data 1
Figure 11A: Comparison of preferred left-right directions in control and nerve block during feeding.
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Figure 11—source data 2
Figure 11B: Comparison of preferred directions in control and nerve block during drinking.
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Figure 12
Effect of nerve block on population trajectories.
Trial-averaged trajectories of MIo and SIo population activity for Monkey R’s feeding and drinking sessions, grouped by direction. Two factors with the highest explained variance are plotted for visualization only. Axes represent the latent factors from control data, with the x-axis chosen as the factor with the highest degree of separation between directions. Lighter, dotted lines represent superimposed population trajectories in the nerve block condition. Insets show the difference between the average inter-trajectory distances for control and nerve block conditions.
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Figure 12—source data 1
Effect of nerve block on population trajectories.
- https://cdn.elifesciences.org/articles/101325/elife-101325-fig12-data1-v1.xlsx
Figure 13 with 2 supplements
Accuracies of two different decoding algorithms from MIo and SIo populations of equal size (N=28).
(A) Comparison between average decoding accuracy of k-nearest neighbor (KNN) classifier. Chance level is 33.33%. (B) Comparison between average decoding accuracy by long short-term memory (LSTM) network. Data are shown separately for each subject, behavioral task, and condition. The dashed line signifies equal decoding performance for MIo and SIo. Decoding accuracies from full populations are included in Figure 13—figure supplement 2.
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Figure 13—source data 1
Figure 13A: k-Nearest neighbor (KNN) decoding performance.
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Figure 13—source data 2
Figure 13B: Long short-term memory (LSTM) decoding performance.
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Figure 13—figure supplement 1
Correlation between population size and decoding accuracy.
Each cross represents one iteration of k-nearest neighbor (KNN) classification, and the trendline is the linear fit: R2 = 0.6.
Figure 13—figure supplement 2
Decoding accuracies from neuronal populations of various sizes.
(A) Comparison between average decoding accuracy of k-nearest neighbor (KNN) classifier. Chance level is 33.33%. (B) Comparison between average decoding accuracy by long short-term memory (LSTM) network. Data shown separately for each subject, behavioral task, and condition. The dashed line signifies equal decoding performance for MIo and SIo.
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Figure 13—figure supplement 2—source data 1
k-Nearest neighbor (KNN) decoding accuracies from neuronal populations of various sizes.
- https://cdn.elifesciences.org/articles/101325/elife-101325-fig13-figsupp2-data1-v1.xlsx
Author response image 1
Author response image 2
Comparison of mean-matched Fano Factor between Sio neurons during feeding and drinking control tasks across both subjects (Wilcoxon rank sum test, p < 0. 001).
Author response image 3
Comparison of Fano Factor across directions for MIo and SIo Feeding Control (Kruskal-Wallis, p > 0. 7).
Author response image 4
Tongue tip position (mm) and jaw pitch(degree) during feeding (left) and drinking (right) behaviors.
Most protruded tongue position coincides with minimum gape (jaw pitch at 0°) during feeding but with maximum gape during drinking.
Author response image 5
Proportion of feeding trials in each group of directions.
Error bars represent ±1 standard deviation across datasets (n = 4).
Author response image 6
Left halves of hemi-violins (black) are control and right halves (red) are nerve block for an individual.
Horizontal black lines represent the mean and horizontal red lines the median. Results of two-tailed t-test and f-test are indicated by asterisks and crosses, respectively: *,† p < 0.05; **,†† p < 0.01; ***,††† p < 0.001.
Tables
Appendix 1—table 1
Numbers of individual neurons recorded from each array location during each data collection session.
| Control | rMIo | cMIo | SIo(3a/3b) | SIo(1/2) |
|---|---|---|---|---|
| R Feeding | 29 | 125 | 9 | 29 |
| Y Feeding | 28 | 76 | 18 | 37 |
| R Drinking | 31 | 185 | 23 | 54 |
| Y Drinking | 23 | 104 | 16 | 63 |
| Nerve block | ||||
| R Feeding | 27 | 126 | 1 | 27 |
| Y Feeding | 29 | 64 | 17 | 21 |
| R Drinking | 36 | 182 | 26 | 56 |
| Y Drinking | 22 | 55 | 14 | 55 |
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3D directional tuning in the orofacial sensorimotor cortex during natural feeding and drinking
eLife 13:RP101325.
https://doi.org/10.7554/eLife.101325.3
