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Motor modulation of afferent somatosensory circuits

Abstract

A prominent feature of thalamocortical circuitry in sensory systems is the extensive and highly organized feedback projection from the cortex to the thalamic neurons that provide stimulus-specific input to the cortex. In lightly sedated rats, we found that focal enhancement of motor cortex activity facilitated sensory-evoked responses of topographically aligned neurons in primary somatosensory cortex, including antidromically identified corticothalamic cells; similar effects were observed in ventral posterior medial thalamus (VPm). In behaving rats, thalamic responses were normally smaller during whisking but larger when signal transmission in brainstem trigeminal nuclei was bypassed or altered. During voluntary movement, sensory activity may be globally suppressed in the brainstem, whereas signaling by cortically facilitated VPm neurons is simultaneously enhanced relative to other VPm neurons receiving no such facilitation.

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Figure 1: The effect of BMI micro-iontophoresis on vFMCx and S1 L-6 neurons.
Figure 2: Effects of vFMCx activation on antidromically identified corticothalamic neurons in S1.
Figure 3: The effect of vFMCx activation on VPm neurons.
Figure 4: Whisker follicle stimulation–evoked VPm LFPs during whisking and nonwhisking conditions.
Figure 5: Medial lemniscal stimulation–evoked VPm LFPs.
Figure 6: Paired-pulse medial lemniscal stimulation.
Figure 7: Contrasting effects of whisker follicle and medial lemniscus stimulation in the same animal.
Figure 8: Whisker follicle stimulation evokes larger VPm responses during whisking when SpVi is inactivated.

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References

  1. Ahissar, E. & Kleinfeld, D. Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. Cereb. Cortex 13, 53–62 (2003).

    Article  PubMed  Google Scholar 

  2. Carvell, G.E., Miller, S.A. & Simons, D.J. The relationship of vibrissal motor cortex unit activity to whisking in the awake rat. Somatosens. Mot. Res. 13, 115–127 (1996).

    Article  CAS  PubMed  Google Scholar 

  3. Fanselow, E.E. & Nicolelis, M.A. Behavioral modulation of tactile responses in the rat somatosensory system. J. Neurosci. 19, 7603–7616 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. 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  CAS  PubMed  Google Scholar 

  5. Hentschke, H., Haiss, F. & Schwarz, C. Central signals rapidly switch tactile processing in rat barrel cortex during whisker movements. Cereb. Cortex 16, 1142–1156 (2006).

    Article  PubMed  Google Scholar 

  6. Ferezou, I. et al. Spatiotemporal dynamics of cortical sensorimotor integration in behaving mice. Neuron 56, 907–923 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Miyashita, E., Keller, A. & Asanuma, H. Input-output organization of the rat vibrissal motor cortex. Exp. Brain Res. 99, 223–232 (1994).

    Article  CAS  PubMed  Google Scholar 

  9. Zhang, Z.W. & Deschenes, M. Projections to layer VI of the posteromedial barrel field in the rat: a reappraisal of the role of corticothalamic pathways. Cereb. Cortex 8, 428–436 (1998).

    Article  CAS  PubMed  Google Scholar 

  10. Sillito, A.M. & Jones, H.E. Corticothalamic interactions in the transfer of visual information. Phil. Trans. R. Soc. Lond. B 357, 1739–1752 (2002).

    Article  Google Scholar 

  11. Alitto, H.J. & Usrey, W.M. Corticothalamic feedback and sensory processing. Curr. Opin. Neurobiol. 13, 440–445 (2003).

    Article  CAS  PubMed  Google Scholar 

  12. Landry, P. & Dykes, R.W. Identification of two populations of corticothalamic neurons in cat primary somatosensory cortex. Exp. Brain Res. 60, 289–298 (1985).

    Article  CAS  PubMed  Google Scholar 

  13. Kelly, M.K., Carvell, G.E., Hartings, J.A. & Simons, D.J. Axonal conduction properties of antidromically identified neurons in rat barrel cortex. Somatosens. Mot. Res. 18, 202–210 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Swadlow, H.A. Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J. Neurophysiol. 62, 288–308 (1989).

    Article  CAS  PubMed  Google Scholar 

  15. Swadlow, H.A. & Hicks, T.P. Somatosensory cortical efferent neurons of the awake rabbit: latencies to activation via supra- and subthreshold receptive fields. J. Neurophysiol. 75, 1753–1759 (1996).

    Article  CAS  PubMed  Google Scholar 

  16. Beloozerova, I.N. et al. Activity of different classes of neurons of the motor cortex during postural corrections. J. Neurosci. 23, 7844–7853 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Sirota, M.G., Swadlow, H.A. & Beloozerova, I.N. Three channels of corticothalamic communication during locomotion. J. Neurosci. 25, 5915–5925 (2005).

    Article  CAS  PubMed  Google Scholar 

  18. Temereanca, S. & Simons, D.J. Functional topography of corticothalamic feedback enhances thalamic spatial response tuning in the somatosensory whisker/barrel system. Neuron 41, 639–651 (2004).

    Article  CAS  PubMed  Google Scholar 

  19. Land, P.W., Buffer, S.A. Jr & Yaskosky, J.D. Barreloids in adult rat thalamus: three dimensional architecture and relationship to somatosensory cortical barrels. J. Comp. Neurol. 355, 573–588 (1995).

    Article  CAS  PubMed  Google Scholar 

  20. Temereanca, S. & Simons, D.J. Local field potentials and the encoding of whisker deflections by population firing sychrony in thalamic barreloids. J. Neurophysiol. 89, 2137–2145 (2003).

    Article  PubMed  Google Scholar 

  21. Castro-Alamancos, M.A. Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. J. Physiol. (Lond.) 539, 567–578 (2002).

    Article  CAS  Google Scholar 

  22. Jacquin, M.F., Golden, J. & Rhoades, R.W. Structure-function relationships in rat brainstem subnucleus interpolaris. III. Local circuit neurons. J. Comp. Neurol. 282, 24–44 (1989).

    Article  CAS  PubMed  Google Scholar 

  23. Furuta, T. et al. Inhibitory gating of vibrissal inputs in the brainstem. J. Neurosci. 28, 1789–1797 (2008).

    Article  CAS  PubMed  Google Scholar 

  24. Hattox, A., Li, Y. & Keller, A. Serotonin regulates rhythmic whisking. Neuron 39, 343–352 (2003).

    Article  CAS  PubMed  Google Scholar 

  25. Cramer, N.P. & Keller, A. Cortical control of a whisking central pattern generator. J. Neurophysiol. 96, 209–217 (2006).

    Article  PubMed  Google Scholar 

  26. Jones, E.G. & Powell, T.P. An electron microscopic study of the mode of termination of cortico-thalamic fibres within the sensory relay nuclei of the thalamus. Proc. R. Soc. Lond. B 172, 173–185 (1969).

    Article  CAS  PubMed  Google Scholar 

  27. Liu, X.B., Honda, C.N. & Jones, E.G. Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J. Comp. Neurol. 352, 69–91 (1995).

    Article  CAS  PubMed  Google Scholar 

  28. Erisir, A., Van Horn, S.C. & Sherman, S.M. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc. Natl. Acad. Sci. USA 94, 1517–1520 (1997).

    Article  CAS  PubMed  Google Scholar 

  29. Diamond, M.E., Armstrong-James, M., Budway, M.J. & Ebner, F.F. Somatic sensory responses in the rostral sector of the posteriorgroup (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J. Comp. Neurol. 319, 66–84 (1992).

    Article  CAS  PubMed  Google Scholar 

  30. Ghazanfar, A.A., Krupa, D.J. & Nicolelis, M.A. Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons. Exp. Brain Res. 141, 88–100 (2001).

    Article  CAS  PubMed  Google Scholar 

  31. Yuan, B., Morrow, T.J. & Casey, K.L. Responsiveness of ventrobasal thalamic neurons after suppression of SI cortex in the anesthetized rat. J. Neurosci. 5, 2971–2978 (1985).

    Article  CAS  PubMed  Google Scholar 

  32. Yuan, B., Morrow, T.J. & Casey, K.L. Corticofugal influences of S1 cortex on ventrobasal thalamic neurons in awake rat. J. Neurosci. 6, 3611–3617 (1986).

    Article  CAS  PubMed  Google Scholar 

  33. White, E.L. & Keller, A. Intrinsic circuitry involving the local axon collaterals of corticothalamic projection cells in mouse SmI cortex. J. Comp. Neurol. 262, 13–26 (1987).

    Article  CAS  PubMed  Google Scholar 

  34. Urbain, N. & Deschênes, M. A new thalamic pathway of vibrissal information modulated by the motor cortex. J. Neurosci. 27, 12407–12412 (2007).

    Article  CAS  PubMed  Google Scholar 

  35. Ghez, C. & Pisa, M. Inhibition of afferent transmission in cuneate nucleus during voluntary movement in the cat. Brain Res. 40, 145–155 (1972).

    Article  CAS  PubMed  Google Scholar 

  36. Coulter, J.D. Sensory transmission through lemniscal pathway during voluntary movement in the cat. J. Neurophysiol. 37, 831–845 (1974).

    Article  CAS  PubMed  Google Scholar 

  37. Seki, K., Perlmutter, S.I. & Fetz, E.E. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nat. Neurosci. 6, 1309–1316 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Furuta, T., Nakamura, K. & Deschenes, M. Angular tuning bias of vibrissa-responsive cells in the paralemniscal pathway. J. Neurosci. 26, 10548–10557 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Leiser, S.C. & Moxon, K.A. Responses of trigeminal ganglion neurons during natural whisking behaviors in the awake rat. Neuron 53, 117–133 (2007).

    Article  CAS  PubMed  Google Scholar 

  40. Urbain, N. & Deschenes, M. Motor cortex gates vibrissal responses in a thalamocortical projection pathway. Neuron 56, 714–725 (2007).

    Article  CAS  PubMed  Google Scholar 

  41. Hall, R.D. & Lindholm, E.P. Organization of motor and somatosensory neocortex in the albino rat. Brain Res. 66, 23–38 (1974).

    Article  Google Scholar 

  42. Hoffer, Z.S., Hoover, J.E. & Alloway, K.D. Sensorimotor corticocortical projections from rat barrel cortex have an anisotropic organization that facilitates integration of inputs from whiskers in the same row. J. Comp. Neurol. 466, 525–544 (2003).

    Article  PubMed  Google Scholar 

  43. Donoghue, J.P. & Wise, S.P. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. Comp. Neurol. 212, 76–88 (1982).

    Article  CAS  PubMed  Google Scholar 

  44. Haiss, F. & Schwarz, C. Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex. J. Neurosci. 25, 1579–1587 (2005).

    Article  CAS  PubMed  Google Scholar 

  45. Kakei, S., Hoffman, D.S. & Strick, P.L. Muscle and movement representations in the primary motor cortex. Science 285, 2136–2139 (1999).

    Article  CAS  PubMed  Google Scholar 

  46. Graziano, M. The organization of behavioral repertoire in motor cortex. Annu. Rev. Neurosci. 29, 105–134 (2006).

    Article  CAS  PubMed  Google Scholar 

  47. Welker, W.I. Analysis of sniffing of the albino rat. Behaviour 22, 223–244 (1964).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  49. Towal, R.B. & Hartmann, M.J. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J. Neurosci. 26, 8838–8846 (2006).

    Article  CAS  PubMed  Google Scholar 

  50. Simons, D.J. & Carvell, G.E. Thalamocortical response transformation in the rat vibrissa/barrel system. J. Neurophysiol. 61, 311–330 (1989).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank H. Kyriazi and T. Prigg for excellent technical assistance, and E. Merriam for helpful comments on the manuscript. This work was supported by US National Institutes of Health grants NS19950 and NS58758.

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S.L., G.E.C. and D.J.S. designed the experiments. S.L. conducted the experiments. S.L., G.E.C. and D.J.S. analyzed data. G.E.C. and D.J.S. supervised the project. S.L., G.E.C. and D.J.S. wrote the manuscript.

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Correspondence to Daniel J Simons.

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Lee, S., Carvell, G. & Simons, D. Motor modulation of afferent somatosensory circuits. Nat Neurosci 11, 1430–1438 (2008). https://doi.org/10.1038/nn.2227

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