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Activity in motor–sensory projections reveals distributed coding in somatosensation

Abstract

Cortical-feedback projections to primary sensory areas terminate most heavily in layer 1 (L1) of the neocortex 1,2, where they make synapses with tuft dendrites of pyramidal neurons. L1 input is thought to provide ‘contextual’ information3, but the signals transmitted by L1 feedback remain uncharacterized. In the rodent somatosensory system, the spatially diffuse4 feedback projection from vibrissal motor cortex (vM1) to vibrissal somatosensory cortex (vS1, also known as the barrel cortex) may allow whisker touch to be interpreted in the context of whisker position to compute object location5,6. When mice palpate objects with their whiskers to localize object features7,8, whisker touch excites vS19 and later vM1 in a somatotopic manner10,11,12,13. Here we use axonal calcium imaging to track activity in vM1→vS1 afferents in L1 of the barrel cortex while mice performed whisker-dependent object localization. Spatially intermingled individual axons represent whisker movements, touch and other behavioural features. In a subpopulation of axons, activity depends on object location and persists for seconds after touch. Neurons in the barrel cortex thus have information to integrate movements and touches of multiple whiskers over time, key components of object identification and navigation by active touch.

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Figure 1: Imaging activity in vM1→vS1 axons during whisker-based object localization.
Figure 2: Motor and sensory signals in vM1→vS1 axons.
Figure 3: Decoding behavioural variables on the basis of axonal activity.
Figure 4: Persistent object-location-dependent activity.

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Acknowledgements

We thank M. Hooks, N. Li, Z. Guo, J. Magee and J. Dudman for comments on the manuscript, N. Clack, V. Iyer and J. Vogelstein for help with software and D. Flickinger for help with microscope design.

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Authors

Contributions

L.P. and K.S. conceived the study. L.P. performed the experiments. L.P., D.A.G. and K.S. analysed the data. D.A.G. and D.H.O. contributed software. D.H. and D.H.O. helped with behavioural and imaging experiments. N.-l.X. performed key pilot studies. L.T. and L.L. provided reagents. L.P., D.A.G. and K.S. wrote the paper with comments from all authors.

Corresponding author

Correspondence to Karel Svoboda.

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The authors declare no competing financial interests.

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Petreanu, L., Gutnisky, D., Huber, D. et al. Activity in motor–sensory projections reveals distributed coding in somatosensation. Nature 489, 299–303 (2012). https://doi.org/10.1038/nature11321

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