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Representation of egomotion in rat's trident and E-row whisker cortices

Nature Neuroscience volume 19, pages 1367–1373 (2016)Cite this article

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Abstract

The whisker trident, a three-whisker array on the rat's chin, has been implicated in egomotion sensing and might function as a tactile speedometer. Here we study the cortical representation of trident whiskers and E-row whiskers in barrel cortex. Neurons identified in trident cortex of anesthetized animals showed sustained velocity-sensitive responses to ground motion. In freely moving animals, about two-thirds of the units in the trident and E-row whisker cortices were tuned to locomotion speed, a larger fraction of speed-tuned cells than in the somatosensory dysgranular zone. Similarly, more units were tuned to acceleration and showed sensitivity to turning in trident and E-row whisker cortices than in the dysgranular zone. Microstimulation in locomoting animals evoked small but significant speed changes, and such changes were larger in the trident and E-row whisker representations than in the dysgranular zone. Thus, activity in trident and E-row cortices represents egomotion information and influences locomotion behavior.

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Figure 1: Trident units can signal ground movements.
Figure 2: Midline trident unit firing in relation to locomotion speed.
Figure 3: Speed selectivity is more frequent in trident and E-row barrels than in the DGZ.
Figure 4: Tuning to acceleration is more common in trident and E-row barrels than in the DGZ.
Figure 5: Turn-tuned units in the trident, DGZ and E-row cortices.
Figure 6: Microstimulation in the trident and E-row whisker barrels evokes running speed changes.

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  • 05 September 2016

    In the version of this article initially published online, Patricia Preston-Ferrer's name was misspelled as “Patricia Preston Ferrer,” without the hyphen. The error has been corrected in the print, PDF and HTML versions of this article.

References

  1. Thé, L., Wallace, M.L., Chen, C.H., Chorev, E. & Brecht, M. Structure, function, and cortical representation of the rat submandibular whisker trident. J. Neurosci. 33, 4815–4824 (2013).

    Article  Google Scholar 

  2. Nishiike, S., Guldin, W.O. & Bäurle, J. Corticofugal connections between the cerebral cortex and the vestibular nuclei in the rat. J. Comp. Neurol. 420, 363–372 (2000).

    Article  CAS  Google Scholar 

  3. Reep, R.L., Chandler, H.C., King, V. & Corwin, J.V. Rat posterior parietal cortex: topography of corticocortical and thalamic connections. Exp. Brain Res. 100, 67–84 (1994).

    Article  CAS  Google Scholar 

  4. Parron, C. & Save, E. Evidence for entorhinal and parietal cortices involvement in path integration in the rat. Exp. Brain Res. 159, 349–359 (2004).

    Article  Google Scholar 

  5. Welker, W., Sanderson, K.J. & Shambes, G.M. Patterns of afferent projections to transitional zones in the somatic sensorimotor cerebral cortex of albino rats. Brain Res. 292, 261–267 (1984).

    Article  CAS  Google Scholar 

  6. Chapin, J.K. & Lin, C.-S. Mapping the body representation in the SI cortex of anesthetized and awake rats. J. Comp. Neurol. 229, 199–213 (1984).

    Article  CAS  Google Scholar 

  7. Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003).

    Article  CAS  Google Scholar 

  8. Kropff, E., Carmichael, J.E., Moser, M.-B. & Moser, E.I. Speed cells in the medial entorhinal cortex. Nature 523, 419–424 (2015).

    Article  CAS  Google Scholar 

  9. Sargolini, F. et al. Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312, 758–762 (2006).

    Article  CAS  Google Scholar 

  10. Gu, Y., Angelaki, D.E. & Deangelis, G.C. Neural correlates of multisensory cue integration in macaque MSTd. Nat. Neurosci. 11, 1201–1210 (2008).

    Article  CAS  Google Scholar 

  11. Fetsch, C.R., Turner, A.H., DeAngelis, G.C. & Angelaki, D.E. Dynamic reweighting of visual and vestibular cues during self-motion perception. J. Neurosci. 29, 15601–15612 (2009).

    Article  CAS  Google Scholar 

  12. Longuet-Higgins, H.C. & Prazdny, K. The interpretation of a moving retinal image. Proc. R. Soc. Lond. B Biol. Sci. 208, 385–397 (1980).

    Article  CAS  Google Scholar 

  13. Saleem, A.B., Ayaz, A., Jeffery, K.J., Harris, K.D. & Carandini, M. Integration of visual motion and locomotion in mouse visual cortex. Nat. Neurosci. 16, 1864–1869 (2013).

    Article  CAS  Google Scholar 

  14. Elliott, D. The influence of walking speed and prior practice on locomotor distance estimation. J. Mot. Behav. 19, 476–485 (1987).

    Article  CAS  Google Scholar 

  15. Cardin, V. & Smith, A.T. Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. Cereb. Cortex 20, 1964–1973 (2010).

    Article  Google Scholar 

  16. Dokka, K., MacNeilage, P.R., DeAngelis, G.C. & Angelaki, D.E. Estimating distance during self-motion: a role for visual-vestibular interactions. J. Vis. 11, 11.13.2 (2011).

    Article  Google Scholar 

  17. Jacob, P.-Y., Poucet, B., Liberge, M., Save, E. & Sargolini, F. Vestibular control of entorhinal cortex activity in spatial navigation. Front. Integr. Neurosci. 8, 38 (2014).

    Article  Google Scholar 

  18. Arkley, K., Grant, R.A., Mitchinson, B. & Prescott, T.J. Strategy change in vibrissal active sensing during rat locomotion. Curr. Biol. 24, 1507–1512 (2014).

    Article  CAS  Google Scholar 

  19. Kim, U. & Lee, T. Intra-areal and corticocortical circuits arising in the dysgranular zone of rat primary somatosensory cortex that processes deep somatic input. J. Comp. Neurol. 521, 2585–2601 (2013).

    Article  CAS  Google Scholar 

  20. Lee, T. & Kim, U. Descending projections from the dysgranular zone of rat primary somatosensory cortex processing deep somatic input. J. Comp. Neurol. 520, 1021–1046 (2012).

    Article  Google Scholar 

  21. Keller, G.B., Bonhoeffer, T. & Hübener, M. Sensorimotor mismatch signals in primary visual cortex of the behaving mouse. Neuron 74, 809–815 (2012).

    Article  CAS  Google Scholar 

  22. Houweling, A.R., Doron, G., Voigt, B.C., Herfst, L.J. & Brecht, M. Nanostimulation: manipulation of single neuron activity by juxtacellular current injection. J. Neurophysiol. 103, 1696–1704 (2010).

    Article  Google Scholar 

  23. Schmitzer-Torbert, N., Jackson, J., Henze, D., Harris, K. & Redish, A.D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131, 1–11 (2005).

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank C. Ebbesen, P. Bennett, S. Ray and R. Rao for comments on the manuscript. We also thank all members of the Brecht laboratory for discussions throughout the study. This work was supported by the Bernstein Center for Computational Neuroscience Berlin, the German Federal Ministry of Education and Research (BMBF, Förderkennzeichen 01GQ1001A (M.B.)), NeuroCure and the Gottfried Wilhelm Leibniz prize of the DFG (M.B.).

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Author notes

  1. Patricia Preston-Ferrer

    Present address: Present address: Werner Reichardt Centre for Integrative Neuroscience, Tübingen, Germany.,

Authors and Affiliations

  1. Department of Systems Neurobiology and Neural Computation, Humboldt Universität zu Berlin, Berlin, Germany

    Edith Chorev, Patricia Preston-Ferrer & Michael Brecht

  2. Bernstein Center for Computational Neuroscience, Berlin, Germany

    Edith Chorev, Patricia Preston-Ferrer & Michael Brecht

Authors
  1. Edith Chorev
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  3. Michael Brecht
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Contributions

E.C., P.P.F. and M.B. designed experiments. P.P.F. performed juxtacellular experiments. E.C. performed tetrode experiment. E.C. analyzed the data. E.C. and M.B. wrote the manuscript.

Corresponding author

Correspondence to Edith Chorev.

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Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Speed tuning in an anesthetized animal.

An example of a speed-tuned unit. Each one of the three panels shows a raster plot and PSTH for different backward ground speeds. This unit shows a clear preference for the medium speed.

Supplementary Figure 2 Changes in trident whisker position during ground movement stimulation.

(a) Two frames from periods were the treadmill was moving in the forward and backward directions (right and left, respectively). Arrows mark the midline whisker. Notice that during forward motion of the treadmill the trident whisker is bent toward the rat’s nose as in the no contact situation (compare to picture in Fig. 1a), while during backward motion of the treadmill the whisker is bent towards the trunk. (b) Overlaid traced trajectories of the midline whisker from 50 consecutive frames (2 seconds) during periods of forward and backward treadmill motion (red & black, respectively); the x-axis was stretched to twice the size as appears in the photos to magnify the differences. Note the very different positions of the whisker under the two conditions. Also not that the red traces are more dispersed as compared to the black ones due to the increase in micro-motions under this condition. (c) Four frames of the midline trident whiskers taken at different speeds of the treadmill. Arrows mark the midline whisker. (d) Traced whiskers from the frames in c overlaid and stretched on the x-axis to twice the size of the photos. Colors correspond to the different speeds. As the speed is increased the midline trident whisker is more bend towards the trunk.

Supplementary Figure 3 An anticorrelated speed-tuned unit from the trident area.

(a) Z-scores of speed and firing rate from one trident unit (light and dark gray, respectively). (b) Distribution of Pearson Product-Moment correlation coefficients for shuffled data (black bars), green bar marks the value of the coefficient of the unshuffled data.

Supplementary Figure 4 An example of a microstimulation experiment at an E-row barrel site.

An accelerating effect of microstimulation at an E-row cortex site. Left, average running speed (blue line) of a rat before and after the onset of stimulation (gray area marks time of stimulation). Light blue area around blue line marks the standard error. Right, statistics for running speed before and after onset of stimulation, which were significantly different (mean speed before stimulation onset was 7.45±0.19 cm/s, mean speed after stimulation onset was 10.29±0.29 cm/s, these differences were significant (two sided student t-test p=3.93e-20). Red lines are for medians and the edges of the boxes mark the 25 and 75 percentiles.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 394 kb)

Supplementary Methods Checklist (PDF 420 kb)

Trident whiskers during free foraging

The video (slowed down by a factor of 8) shows multiple snippets of the rat foraging. Red arrows show the location of the trident at the beginning of each snippet. The trident whiskers are bent backwards towards the animal's trunk, similarly to their position on the treadmill during backward movement of the treadmill. (MP4 2596 kb)

Facial whiskers during free foraging

The video (slowed down by a factor of 8) shows multiple snippets of the rat foraging. The lower rows of whiskers are contacting the ground; some seem to be dragged while others are being tapped onto the ground. (MP4 4622 kb)

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Chorev, E., Preston-Ferrer, P. & Brecht, M. Representation of egomotion in rat's trident and E-row whisker cortices. Nat Neurosci 19, 1367–1373 (2016). https://doi.org/10.1038/nn.4363

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