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A collicular map for touch-guided tongue control

Nature volume 637, pages 1143–1151 (2025)Cite this article

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Abstract

Accurate goal-directed behaviour requires the sense of touch to be integrated with information about body position and ongoing motion1,2. Behaviours such as chewing, swallowing and speech critically depend on precise tactile events on a rapidly moving tongue3, but neural circuits for dynamic touch-guided tongue control are unknown. Here, using high-speed videography, we examined three-dimensional lingual kinematics as mice drank from a water spout that unexpectedly changed position during licking, requiring re-aiming in response to subtle contact events on the left, centre or right surface of the tongue. Mice integrated information about both precise touch events and tongue position to re-aim ensuing licks. Touch-guided re-aiming was unaffected by photoinactivation of tongue sensory, premotor and motor cortices, but was impaired by photoinactivation of the lateral superior colliculus (latSC). Electrophysiological recordings identified latSC neurons with mechanosensory receptive fields for precise touch events that were anchored in tongue-centred, head-centred or conjunctive reference frames. Notably, latSC neurons also encoded tongue position before contact, information that is important for tongue-to-head-based coordinate transformations underlying accurate touch-guided aiming. Viral tracing revealed tongue sensory inputs to the latSC from the lingual trigeminal nucleus, and optical microstimulation in the latSC revealed a topographic map for aiming licks. These findings demonstrate that touch-guided tongue control relies on a collicular mechanosensorimotor map, analogous to collicular visuomotor maps associated with visually guided orienting across many species.

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Fig. 1: Lingual cortical areas are not required for touch-guided re-aiming.
Fig. 2: Photoinactivation of the latSC impairs touch-guided re-aiming.
Fig. 3: latSC neural activity encodes the location of contact events on the tongue surface.
Fig. 4: latSC neurons encode contact location in tongue-centric, head-centric and conjunctive coordinate frames.
Fig. 5: latSC photostimulation reveals a topographic map for tongue aiming.

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Data availability

Source data have been deposited at an Open-Science Framework (OSF) repository (https://doi.org/10.17605/OSF.IO/FY7J5). Source data are provided with this paper.

Code availability

Custom MATLAB and Python code used for analysis is available at GitHub (https://github.com/GoldbergLab/Ito-Gao-et-al-2024).

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Acknowledgements

We thank C. Rodgers for advice on GLMs; M. Warden for use of the Zeiss LSM 710 confocal microscope; T. Bollu, J. Fetcho, A. Pruszynski, M. Sheehan, M. Warden and the members of the J.H.G. laboratory for discussions; and T. Bollu, A. Fernadez-Ruiz, J. Fetcho, G. Maimon, A. Oliva, M. Sedigh-Sarvestani and M. Zipple for comments on the manuscript. This work was supported by the NIH Director’s New Innovator Award (1DP2HD087952-01), an NIH NINDS R01 (1R01NS138093-01) and Jean Sheng and the Sheng Family Foundation. B.S.I. was supported by an NSF Graduate Research Fellowship.

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  1. These authors contributed equally: Brendan S. Ito, Yongjie Gao

Authors and Affiliations

  1. Department of Neurobiology and Behavior, Cornell University, Ithaca, NY, USA

    Brendan S. Ito, Yongjie Gao, Brian Kardon & Jesse H. Goldberg

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  1. Brendan S. Ito
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  2. Yongjie Gao
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Contributions

B.S.I., Y.G. and J.H.G. designed the experiments. B.S.I. and Y.G. trained all of the animals, conducted all experiments and analysed all data. B.S.I. and B.K. developed the contact location tracking algorithms. B.S.I., B.K. and Y.G. built the hardware and software necessary for data acquisition. B.S.I. and J.H.G. wrote the manuscript.

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Correspondence to Brendan S. Ito or Jesse H. Goldberg.

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Extended data figures and tables

Extended Data Fig. 1 Touch-guided re-aiming does not depend on water dispensation.

a, Trial structure was the same as in Fig. 1a, except water was dispensed at L3 contact instead of L2 contact. b, Bottom view still frames at L1-L3 contact onset across trial types for dispense on L3 trials. Tip site and vector, blue dot and dashed line. Contact site and vector, red dot and dashed line. Contact angle and protrusion angle, red and white values. c, L1-L3 protrusion angle distributions during left (gold), centre (black) and right (purple) trials from a session where water was dispensed on L2 (top) or L3 (bottom). d, L3 protrusion angles for dispense on L2 (black, n = 7 mice) and dispense on L3 trials (dark grey, n = 7 mice). Grey dots are medians of individual mice. Data in d are median ± IQR. **corrected p < 0.01, two-sided hierarchical bootstrap test; n.s., not significant. Exact statistics are in Supplementary Table 2.

Source Data

Extended Data Fig. 2 Bilateral photoinactivation of ALM and TJM1, but not TJS1, reduces lick pathlength and duration.

a, Rhythm of lick bouts are unaffected by spout displacement on L2. Inter-lick intervals (ILI) for L2 to L3 (dark grey) do not significantly differ by condition. ILI for L1 to L2 (light grey), where no spout displacements occurred, provided for comparison. b-d, Left, Cumulative probability of L3 protrusion relative to L2 contact onset for ALM (blue, b), TJM1 (green, c) and TJS1 (brown, d) inactivated trials, relative to no laser trials for the same mice (black). Right, L3 protrusion probability for inactivation and no laser trials. e-j, Effect of bilateral ALM, TJM1 or TJS1 inactivation on L3 lick kinematics. L3 contact probability (e), corrective submovement (CSM) probability (f), lick duration (g), lick pathlength (h), lick peak speed (i) and number of acceleration peaks (j) for left, centre and right trials. Colours for each panel are the same as in b-d. Note that ALM and TJM1, but not TJS1, inactivation impair lick duration and pathlength. Data in e-j are median ± IQR. *corrected p < 0.05, **corrected p < 0.01, two-sided hierarchical bootstrap test; n.s., not significant. Exact statistics are in Supplementary Tables 1, 3 and 4.

Source Data

Extended Data Fig. 3 Electrophysiological validation of photoinhibition of the cortex and latSC.

a, Spike rasters (top row) and rate histograms (bottom row) for an example putative interneuron (left) and pyramidal neuron (right) recorded in the superficial layers of ALM during photovalidation experiments in VGAT-CHR2-EYFP mice. Data are aligned to trial onset and sorted by laser on (dark blue) or off (black) trials. Cyan bar above the raster indicates when the laser was on. Laser power, waveform and duration were the same as in behavioural experiments. b, Left, Normalized mean ± IQR firing rates of superficial layer ALM neurons (300–800 μm below dura surface, Methods) recorded during photoinactivation. Dark grey and light grey indicate putative pyramidal and interneurons, respectively. Right, Mean ± IQR normalized firing rate of putative ALM pyramidal neurons during no laser (black) and laser on (dark grey) trials. c-d, Same as a-b, but for an example putative interneuron (left) and pyramidal neuron (right) recorded in the deep layers of ALM (800–1200 μm below dura surface, Methods). e-f, Same as a-b, but for two example neurons recorded in latSC during axonal stimulation of the SNr-SC pathway in Vgat-cre mice (orange). For all rate histograms, shading represents the bootstrapped s.e.m. across trials.

Extended Data Fig. 4 Lesions of all three lingual cortical areas at once impair lick kinematics while preserving touch-guided re-aiming.

a, Example histological images from a mouse with ALM, TJM1 and TJS1 lesioned. Slices were stained with anti-NeuN (gold). Scale bar, 1 mm. b-h, L3 protrusion angles (b), protrusion probability (c), reaction time (d), first lick duration (e), first lick pathlength (f), first lick peak speed (g), and first lick number of acceleration peaks (h) across mice prior to lesion (black) and post-lesion (brown). Data in b-h are median ± IQR, n = 5 mice. *corrected p < 0.05, **corrected p < 0.01, two-sided hierarchical bootstrap test; n.s., not significant. Exact statistics are in Supplementary Tables 5 and 6.

Source Data

Extended Data Fig. 5 Unilateral photoinactivation of ALM, TJM1 and latSC minimally impairs L3 kinematics.

a-f, Effect of unilateral ALM, TJM1 or latSC inactivation on L3 lick kinematics for left, centre and right trials. a, L3 contact probability. b, Corrective submovement (CSM) probability. c, Lick duration. d, Lick pathlength. e, Lick peak speed. f, Number of acceleration peaks. Data in a-f are median ± IQR. Colours in a-f correspond to the photoinactivated brain region. g. Effect of unilateral inactivation of latSC on L3 protrusion angles in VGAT-ChR2-eYFP mice (n = 2). Note that, like unilateral latSC photoinactivation in Vgat-cre mice targeting the SNr-SC pathway, unilateral latSC inactivation in VGAT-ChR2-eYFP mice impaired contralateral re-aiming. Black dots are no laser trials from the same session. Grey dots are medians of individual mice. *p < 0.05, **p < 0.01, two-sided hierarchical bootstrap test; n.s., not significant. Exact statistics are in Supplementary Table 7.

Source Data

Extended Data Fig. 6 latSC neurons exhibit diverse tuning in response to contact events.

a, Spike rasters (top row), rate histograms (middle row) and relationship between mean firing rate and L2 contact angle (bottom row) for contralateral + centre (left), ipsilateral + centre (middle). Data are sorted by condition, then by L2 contact angle within each condition. Shading represents the bootstrapped s.e.m. across trials. b, Normalized mean firing rates of L2-contact modulated neurons with significant selectivity for contralateral + centre (left, n = 81/279) and ipsilateral + centre (right, n = 23/279) contacts on L2.

Extended Data Fig. 7 Location of contact events on the tongue predicts next lick re-aiming.

a, Example still frames of L2 and L3. Contact angle for each lick was defined as the angle between the tip vector (pointing from fiducial to tongue tip) and the contact vector (pointing from fiducial to contact centroid). Protrusion angle change was defined as the angle between the tip vectors at time of spout contact for one lick and the next. b, Example data from a single session showing that L1 contact angle (which varied slightly even though the spout was always centred) was significantly correlated with the change in protrusion angle from L1 to L2 across trial types (left). Pearson’s R and p-value for example data shown in inset. Grey line indicates the line of best fit from linear regression. Right, median correlation coefficient (Pearson’s R, black) compared to shuffled data (grey, n = 6 mice). Left, centre and right displacement trials are yellow, black and purple, respectively. Pearson’s R and p-value for example data shown in inset. c, Same as b, but for correlation between L2 contact angle and the change in protrusion angle from L2 to L3 across trial types. Colours as in b. d-f, Same data as c but analysed separately for each condition: left (d), centre (e), and right (f). Top, example data. Bottom, median correlation coefficient compared to shuffled data. **p < 0.01, two-sided shuffle test. Exact statistics are in Supplementary Table 11.

Source Data

Extended Data Fig. 8 latSC neuronal activity can be selectively tuned to contact events on some licks, but not others.

a-b, Example latSC neurons tuned to contacts on specific licks. a, A neuron tuned to certain contact locations during L2, but not L4. b, A neuron tuned to certain contact locations during L4, but not L2. c, Left, Percentage of L2- and L4-modulated neurons tuned to contacts on L2 only (dark green), L4 only (light green), both L2 and L4 (green), or neither L2 or L4 (grey). Right, Pearson’s R between L2 contact angle and mean firing rate following L2 contact plotted against Pearson’s R for L4 contact angle and mean firing rates following L4 contact. Positive and negative correlation coefficients indicate right or left preference, respectively. Note that the activity of many latSC neurons exhibited similar correlations between firing rate and contact location on L2 and L4. d, Example latSC neuron selective for L2 centre contacts that was re-tuned to non-centre responses on L4 during recentring trials. e, Example L4 modulated neuron that was activated by both left and right recentring trials. f, Left, Percentage of neurons selective for L2 centre contacts that were re-tuned to a non-centre contact on L4 (blue). Blue and grey, re-tuned and not re-tuned, respectively. Right, Percentage of L4 modulated neurons that were activated by both left and right recentring trials (orange). g, Left, Illustration of a hypothetical conjunctively-tuned neuron. Right, Spike rasters and rate histograms for an example conjunctively-tuned latSC neuron aligned to L2 (left) and L4 contact (right). Colours as in Fig. 1a. h, Median ± IQR of single neuron divergence latencies between left, centre and right conditions for tongue-, head-, and conjunctively-tuned neurons, as well as neurons that were not correlated with any reference frame. Note that tactile responses in neurons with a head-centric reference frame diverged significantly later than those with tongue-centric (p = 0.003) or conjunctive (p = 0.007) reference frames, as well as neurons that were modulated, but not correlated (p = 0.006), with contact site. Grey dots are individual neuron divergence latencies. *corrected p < 0.05, **corrected p < 0.01, one-sided hierarchical bootstrap test. For all rate histograms, shading represents the bootstrapped s.e.m. across trials. g was adapted from ref. 8 (Springer Nature Limited).

Source Data

Extended Data Fig. 9 latSC neuronal activity prior to spout contact encodes tongue position.

a, Example lick cycle correlated latSC neuron. Black bar indicates window used for cross-correlation analysis. b, Top, Mean-subtracted firing rate of the neuron in a. Middle, Mean-subtracted tongue volume. Data in a and b are aligned to L4 protrusion onset. Bottom, Normalized cross-correlation coefficient histogram. Black horizontal line, correlation coefficient from shuffled data. c, Percentage of neurons correlated with lick cycle across all combinations of trial types. Note that the circles are not proportional to the actual percentages. d, Top, Distribution of maximum cross-correlation coefficient across all lick cycle correlated neurons (n = 242). Bottom, Distribution of lags for lick cycle correlated neurons. Lag was taken at the time which maximized the cross-correlation coefficient for each neuron. e, Two example latSC neurons that are modulated prior to L4. Data are aligned to L4 protrusion onset, and sorted by condition. Within each condition, data are sorted by tip position in the ML plane at L4 protrusion offset. Black bar, analysis window used for GLMs. f, GLM schematic. We sought to test whether tongue position was encoded in pre-contact L4 latSC neuronal activity. Given the close temporal proximity (~120 ms) between past (L3) contact and L4 re-aiming, any relationship we might observe between tongue position and latSC neuronal activity may be confounded by past L3 contact location. We included both variables to test whether L4 tongue position and/or past L3 contact location was encoded in latSC neural activity. Note that, we are using GLMs to examine encoding of tongue position, not as a model of the latSC. g, Mean ± IQR McFadden’s pseudo-R2 across all latSC neurons (n = 320 neurons). pseudo-R2 is a measure of goodness-of-fit for GLMs, with higher values indicating better model fits. Note that pseudo-R2 values of 0.2-0.4 represent excellent model fits. h, Relative contribution of each predictor across all latSC neurons (n = 320 neurons). Tip and contact position are separated into their ML, AP or DV components. Error bars represent the bootstrapped IQR. i, Percentage of neurons encoding L4 tip position (left) and previous (L3) contact position. Tip and contact position are broken down into neurons encoding only ML, AP or DV components of position, two of these components, or all three.

Source Data

Extended Data Fig. 10 latSC photostimulation reveals the same topographic map when conducted in a cued lick task.

a, Example histological confirmation of latSC photoactivation sites (−3.1, −3.4, −3.7 and −3.9 mm AP) and AAV2-hSyn-ChR2 expression (green). DiI and DiD tracts corresponding to a single fibre implant site are orange and purple, respectively. Sites were excluded if fibre tracts were outside of the latSC or in regions with little viral expression (white, in contrast to yellow). b, Schematic of experimental timeline. Two latSC photostimulation sites were probed per session, with two trial blocks each. In block 1, mice performed ~120 trials of a cued lick task, where no laser trials (Cue only) were interleaved with latSC photostimulation trials (Stim w/cue, Methods). In block 2, mice were photostimulated (Stim only) with no task structure (40 trials). This was repeated for each site on each day. c, Trial structure for Stim w/cue (top) and Stim only (bottom) conditions. Red and cyan dashed lines are cue and laser onset, respectively. Cyan bar indicates photostimulation duration. Black pulse trains indicate lick duration for each lick. d, Polar plots of L1 protrusion endpoints for an example left (left) and right latSC (right) photostimulation session in the ‘Stim w/cue’ condition. Colours as in a. e, latSC-evoked L1 protrusion angles similarly depended on latSC photostimulation site in a cued lick task (n = 8 mice, left). Black line and coloured dots are median ± IQR across mice for each stimulation site. Grey lines are individual mice. Right, R2 for the observed correlation between photostimulation site and L1 protrusion angle (black) compared to shuffled data (grey) for the ‘Stim w/cue’ condition. **p < 0.01, two-sided shuffle test. f-g, L1 protrusion probability (f) and protrusion latency (g) did not significantly differ in post-hoc tests between latSC stimulation sites for the ‘Stim w/cue’ and ‘Cue only’ conditions. Kruskal–Wallis test. h-m, Lick kinematics during latSC photostimulation for each condition. L1 protrusion latency (h), L1 duration (i), the L1 - L2 ILI (j), L1 pathlength (k), peak L1 speed (l) and the number of acceleration peaks in L1 (m) are shown for all trial types. Note that protrusion latencies were briefer and licks were slightly slower following latSC stimulation than with a cue alone. *corrected p < 0.05, **corrected p < 0.01, two-sided hierarchical bootstrap test; n.s., not significant. Exact statistics are in Supplementary Tables 14, 15.

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Supplementary information

Supplementary Tables

Supplementary Tables 1–15, which include statistics for each figure panel.

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Supplementary Video 1

Mice use tactile feedback to re-aim licks. Side and bottom views of the mouse tongue for L1–L5 at full speed and slowed 1/40×, for left, centre and right spout displacement trials. Left to right, raw video, video with tongue labelled by a convolutional neural network (pink; yellow, tongue tip; red, contact centroid) and the estimated tongue tip trajectory and nick location for L1–L5. Lick phases are protrusion (green), corrective sub-movement (orange), spout contact sub-movement (yellow) and retraction (purple).

Supplementary Video 2

Bilateral ALM, TJM1 or TJS1 inactivation does not impair touch-guided re-aiming. Example trial in the touch-guided lick task with bilateral ALM, TJM1 or TJS1 photoinactivation from L2 contact onset for 250 ms. Note that L3 re-aiming is not impaired by inactivation of lingual cortical areas.

Supplementary Video 3

Lesions of all three lingual cortical areas at once impair lick kinematics while preserving touch-guided re-aiming. Example pre-lesion and post-lesion trial in the touch-guided lick task from a mouse with ALM, TJM1 and TJS1 lesioned. Note that L3 re-aiming is not impaired by inactivation of lingual cortical areas.

Supplementary Video 4

Bilateral latSC inactivation halts ongoing licking. Example trial in the touch-guided lick task with bilateral latSC photoinactivation from L2 contact onset for 250 ms. Note that very few, if any, licks are produced with latSC photoinactivation.

Supplementary Video 5

Unilateral ALM or TJM1 inactivation biases licks ipsilaterally, but preserves touch-guided re-aiming. Example trial in the touch-guided lick task with unilateral ALM or TJM1 photoinactivation from L2 contact onset for 250 ms. Note that while all L3s are biased ipsilaterally, L3s are still re-aimed depending on L2 contact site.

Supplementary Video 6

Unilateral latSC inactivation impairs contralateral touch-guided re-aiming. Example trial in the touch-guided lick task with unilateral latSC photoinactivation. Note that re-aiming to the contralateral side is largely impaired with latSC inactivation, while re-aiming to the ipsilateral side is intact.

Supplementary Video 7

Recentring task decouples contact site from spout position. Example trial from a recentring session. In addition to left or right displacements between L1 and L2, which evoke left/right nicks at left/right spout positions, the spout is also moved back to the centre position between L3 and L4, evoking right/left nicks at centre spout positions.

Supplementary Video 8

latSC photostimulation reveals a topographic map for lick aiming. Example trials with unilateral latSC photostimulation at 4 sites along the AP axis in latSC. Note that more posterior stimulations in the latSC evoked more lateral protrusions. The ‘x’ in each trajectory marks the moment of maximum lateral displacement.

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Ito, B.S., Gao, Y., Kardon, B. et al. A collicular map for touch-guided tongue control. Nature 637, 1143–1151 (2025). https://doi.org/10.1038/s41586-024-08339-3

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