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Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex

Nature volume 499, pages 336–340 (2013)Cite this article

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Abstract

In the mammalian neocortex, segregated processing streams are thought to be important for forming sensory representations of the environment1,2, but how local information in primary sensory cortex is transmitted to other distant cortical areas during behaviour is unclear. Here we show task-dependent activation of distinct, largely non-overlapping long-range projection neurons in the whisker region of primary somatosensory cortex (S1) in awake, behaving mice. Using two-photon calcium imaging, we monitored neuronal activity in anatomically identified S1 neurons projecting to secondary somatosensory (S2) or primary motor (M1) cortex in mice using their whiskers to perform a texture-discrimination task or a task that required them to detect the presence of an object at a certain location. Whisking-related cells were found among S2-projecting (S2P) but not M1-projecting (M1P) neurons. A higher fraction of S2P than M1P neurons showed touch-related responses during texture discrimination, whereas a higher fraction of M1P than S2P neurons showed touch-related responses during the detection task. In both tasks, S2P and M1P neurons could discriminate similarly between trials producing different behavioural decisions. However, in trials producing the same decision, S2P neurons performed better at discriminating texture, whereas M1P neurons were better at discriminating location. Sensory stimulus features alone were not sufficient to elicit these differences, suggesting that selective transmission of S1 information to S2 and M1 is driven by behaviour.

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Figure 1: In vivo calcium imaging of long-range projection neurons in S1 during texture discrimination.
Figure 2: Single-neuron discrimination analysis of decision or texture in S1 projection neurons.
Figure 3: Activity of S1 projection neurons during object localization.
Figure 4: Sensory stimuli are not sufficient to produce task-related differences.

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References

  1. Diamond, M. E., von Heimendahl, M., Knutsen, P. M., Kleinfeld, D. & Ahissar, E. 'Where' and 'what' in the whisker sensorimotor system. Nature Rev. Neurosci. 9, 601–612 (2008)

    Article  CAS  Google Scholar 

  2. Felleman, D. J. & Van Essen, D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991)

    Article  CAS  Google Scholar 

  3. Aronoff, R. et al. Long-range connectivity of mouse primary somatosensory barrel cortex. Eur. J. Neurosci. 31, 2221–2233 (2010)

    Article  Google Scholar 

  4. Mao, T. et al. Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72, 111–123 (2011)

    Article  CAS  Google Scholar 

  5. Sato, T. R. & Svoboda, K. The functional properties of barrel cortex neurons projecting to the primary motor cortex. J. Neurosci. 30, 4256–4260 (2010)

    Article  CAS  Google Scholar 

  6. Chakrabarti, S. & Alloway, K. D. Differential origin of projections from SI barrel cortex to the whisker representations in SII and MI. J. Comp. Neurol. 498, 624–636 (2006)

    Article  Google Scholar 

  7. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neurosci. 13, 133–140 (2010)

    Article  CAS  Google Scholar 

  8. Horikawa, K. et al. Spontaneous network activity visualized by ultrasensitive Ca2+ indicators, yellow Cameleon-Nano. Nature Methods 7, 729–732 (2010)

    Article  CAS  Google Scholar 

  9. Carvell, G. E. & Simons, D. J. Biometric analyses of vibrissal tactile discrimination in the rat. J. Neurosci. 10, 2638–2648 (1990)

    Article  CAS  Google Scholar 

  10. Guic-Robles, E., Jenkins, W. M. & Bravo, H. Vibrissal roughness discrimination is barrel cortex-dependent. Behav. Brain Res. 48, 145–152 (1992)

    Article  CAS  Google Scholar 

  11. Jadhav, S. P., Wolfe, J. & Feldman, D. E. Sparse temporal coding of elementary tactile features during active whisker sensation. Nature Neurosci. 12, 792–800 (2009)

    Article  CAS  Google Scholar 

  12. von Heimendahl, M., Itskov, P. M., Arabzadeh, E. & Diamond, M. E. Neuronal activity in rat barrel cortex underlying texture discrimination. PLoS Biol. 5, e305 (2007)

    Article  Google Scholar 

  13. Crochet, S. & Petersen, C. C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nature Neurosci. 9, 608–610 (2006)

    Article  CAS  Google Scholar 

  14. Fee, M. S., Mitra, P. P. & Kleinfeld, D. Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J. Neurophysiol. 78, 1144–1149 (1997)

    Article  CAS  Google Scholar 

  15. Curtis, J. C. & Kleinfeld, D. Phase-to-rate transformations encode touch in cortical neurons of a scanning sensorimotor system. Nature Neurosci. 12, 492–501 (2009)

    Article  CAS  Google Scholar 

  16. O'Connor, D. H., Peron, S. P., Huber, D. & Svoboda, K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 67, 1048–1061 (2010)

    Article  CAS  Google Scholar 

  17. de Kock, C. P., Bruno, R. M., Spors, H. & Sakmann, B. Layer- and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J. Physiol. (Lond.) 581, 139–154 (2007)

    Article  CAS  Google Scholar 

  18. Petreanu, L. et al. Activity in motor-sensory projections reveals distributed coding in somatosensation. Nature 489, 299–303 (2012)

    Article  ADS  CAS  Google Scholar 

  19. Xu, N. L. et al. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492, 247–251 (2012)

    Article  ADS  CAS  Google Scholar 

  20. Hill, D. N., Curtis, J. C., Moore, J. D. & Kleinfeld, D. Primary motor cortex reports efferent control of vibrissa motion on multiple timescales. Neuron 72, 344–356 (2011)

    Article  CAS  Google Scholar 

  21. Green, D. M. & Swets, J. A. Signal Detection Theory and Psychophysics (Wiley, 1966)

    Google Scholar 

  22. O'Connor, D. H. et al. Vibrissa-based object localization in head-fixed mice. J. Neurosci. 30, 1947–1967 (2010)

    Article  CAS  Google Scholar 

  23. Huber, D. et al. Multiple dynamic representations in the motor cortex during sensorimotor learning. Nature 484, 473–478 (2012)

    Article  ADS  CAS  Google Scholar 

  24. Mehta, S. B., Whitmer, D., Figueroa, R., Williams, B. A. & Kleinfeld, D. Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol. 5, e15 (2007)

    Article  Google Scholar 

  25. Melzer, P., Champney, G. C., Maguire, M. J. & Ebner, F. F. Rate code and temporal code for frequency of whisker stimulation in rat primary and secondary somatic sensory cortex. Exp. Brain Res. 172, 370–386 (2006)

    Article  Google Scholar 

  26. Alloway, K. D. Information processing streams in rodent barrel cortex: the differential functions of barrel and septal circuits. Cereb. Cortex 18, 979–989 (2008)

    Article  Google Scholar 

  27. Guic, E., Carrasco, X., Rodriguez, E., Robles, I. & Merzenich, M. M. Plasticity in primary somatosensory cortex resulting from environmentally enriched stimulation and sensory discrimination training. Biol. Res. 41, 425–437 (2008)

    PubMed  Google Scholar 

  28. Wiest, M. C., Thomson, E., Pantoja, J. & Nicolelis, M. A. Changes in S1 neural responses during tactile discrimination learning. J. Neurophysiol. 104, 300–312 (2010)

    Article  Google Scholar 

  29. Krupa, D. J., Wiest, M. C., Shuler, M. G., Laubach, M. & Nicolelis, M. A. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 304, 1989–1992 (2004)

    Article  ADS  CAS  Google Scholar 

  30. Gilbert, C. D. & Sigman, M. Brain states: top-down influences in sensory processing. Neuron 54, 677–696 (2007)

    Article  CAS  Google Scholar 

  31. Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154–165 (2010)

    Article  CAS  Google Scholar 

  32. Lütcke, H. et al. Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice. Front Neural Circuits 4, 9 (2010)

    PubMed  PubMed Central  Google Scholar 

  33. Margolis, D. J. et al. Reorganization of cortical population activity imaged throughout long-term sensory deprivation. Nature Neurosci. 15, 1539–1546 (2012)

    Article  CAS  Google Scholar 

  34. Langer, D. et al. HelioScan: A software framework for controlling in vivo microscopy setups with high hardware flexibility, functional diversity and extendibility. J. Neurosci. Methods 215, 38–52 (2013)

    Article  Google Scholar 

  35. Knutsen, P. M., Derdikman, D. & Ahissar, E. Tracking whisker and head movements in unrestrained behaving rodents. J. Neurophysiol. 93, 2294–2301 (2004)

    Article  Google Scholar 

  36. Conte, W. L., Kamishina, H. & Reep, R. L. Multiple neuroanatomical tract-tracing using fluorescent Alexa Fluor conjugates of cholera toxin subunit B in rats. Nature Protocols 4, 1157–1166 (2009)

    Article  CAS  Google Scholar 

  37. Dombeck, D. A., Khabbaz, A. N., Collman, F., Adelman, T. L. & Tank, D. W. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron 56, 43–57 (2007)

    Article  CAS  Google Scholar 

  38. de Kock, C. P. & Sakmann, B. Spiking in primary somatosensory cortex during natural whisking in awake head-restrained rats is cell-type specific. Proc. Natl Acad. Sci. USA 106, 16446–16450 (2009)

    Article  ADS  CAS  Google Scholar 

  39. Birdwell, J. A. et al. Biomechanical models for radial distance determination by the rat vibrissal system. J. Neurophysiol. 98, 2439–2455 (2007)

    Article  Google Scholar 

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Acknowledgements

We thank S. Soldado-Magraner and L. Sumanovski for assistance with data analysis, H. Kasper, M. Wieckhorst, S. Giger and F. Voigt for technical assistance, A. Miyawaki for plasmid reagents, and D. Margolis, H. Lütcke and K. Schulz for help with initial experiments, helpful discussions and comments on the manuscript and V. Padrun and F. Pidoux for virus production. This work was supported by grants from the Swiss National Science Foundation (310030-127091 to F.H.), the EU-FP7 program (PLASTICISE project 223524 to F.H. and B.L.S.; and the BRAIN-I-NETS project 243914 to F.H.), the Swiss SystemsX.ch initiative (project 2008/2011-Neurochoice to F.H. and B.L.S.), the National Center of Competence in Research ‘Neural Plasticity and Repair’ (F.H.), Forschungskredit of the University of Zurich (grant 541541808 to J.L.C.) and a fellowship from the US National Science Foundation, International Research Fellowship Program (grant 1158914 to J.L.C.).

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Authors and Affiliations

  1. Brain Research Institute, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland,

    Jerry L. Chen, Stefano Carta, Joana Soldado-Magraner & Fritjof Helmchen

  2. Neuroscience Center Zurich, University of Zurich/ETH Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland,

    Stefano Carta & Fritjof Helmchen

  3. Institute of Neuroinformatics, University of Zurich/ETH Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland,

    Joana Soldado-Magraner

  4. Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), EPFL SV BMI LEN, Station 19, CH-1015 Lausanne, Switzerland,

    Bernard L. Schneider

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Contributions

J.L.C. and F.H. designed the study. J.L.C. carried out experiments. J.L.C., S.C., J.S.M and F.H. performed data analysis. S.C. carried out experiments and data analysis characterizing YC-Nano140. B.L.S. contributed viral reagents. J.L.C. and F.H. wrote the paper.

Corresponding author

Correspondence to Fritjof Helmchen.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-14, Supplementary Methods and Supplementary Table 1. (PDF 3374 kb)

'Hit trial' during texture discrimination

Realtime video of hit trial from head-fixed mouse performing texture discrimination task during two-photon imaging. Video was acquired using an infrared CCD camera under infrared LED illumination (for high-speed whisker tracking) with additional illumination provided by two-photon excitation laser source. (MOV 1160 kb)

'Correct rejection' trial during texture discrimination

Realtime video of correct rejection trial from head-fixed mouse performing texture discrimination task during two-photon imaging. Video was acquired using an infrared CCD camera under infrared LED illumination (for high-speed whisker tracking) with additional illumination provided by two-photon excitation laser source. (MOV 1256 kb)

Neuronal activity and whisking behavior during texture discrimination

Realtime playback of high-speed video of whisking and touch (top left panel) along with two-photon imaging of calcium activity in S1 (bottom panel) from a “correct rejection” trial. Top right panel shows measured whisker angle, whisking amplitude, and period of texture touch (orange region) along with calcium traces of active cells. Indicated cells 1-5 were behaviorally classified as touch cells with cells 1, 3-5 identified as S2P neurons and cell 2 identified as an UNL neuron. (MOV 796 kb)

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Chen, J., Carta, S., Soldado-Magraner, J. et al. Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex. Nature 499, 336–340 (2013). https://doi.org/10.1038/nature12236

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