Shaping somatosensory responses in awake rats: cortical modulation of thalamic neurons

Abstract

Massive corticothalamic afferents originating from layer 6a of primary sensory cortical areas modulate sensory responsiveness of thalamocortical neurons and are pivotal for shifting neuronal firing between burst and tonic modes. The influence of the corticothalamic pathways on the firing mode and sensory gain of thalamic neurons has only been extensively examined in anesthetized animals, but has yet to be established in the awake state. We made lesions of the rat barrel cortex and on the following day recorded responses of single thalamocortical and thalamic reticular neurons to a single vibrissal deflection in the somatosensory system during wakefulness. Our results showed that the cortical lesions shifted the response of thalamic neurons towards bursting, elevated the response probability and the gain of thalamocortical neurons, predominantly of recurring responses. In addition, after the lesions, the spontaneous activities of the vibrissa-responsive thalamic neurons, but not those of vibrissa-unresponsive cells, were typified by waxing-and-waning spindle-like rhythmic spiking with frequent bursting. In awake rats with intact cortex, identified layer 6a corticothalamic neurons responded to a single vibrissal deflection with short latencies that matched those of layer 4 neurons, strongly suggesting the existence of an immediate corticothalamic feedback. The present results show the importance of corticothalamic neurons in shaping thalamic activities during wakefulness.

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Acknowledgements

We thank Profs R. Guillery and J. P. Bolam, Drs. A. S. Mitchell, M. Murayama, N. Nakashima, Y. Hirai, and Y. R. Tanaka for helpful comments and discussion, Mr. S. Momma for technical support, Profs K. Nakamura and Y. Isomura for technical advice. This work was supported by Grants-in-Aid for Scientific Research from Ministry of Education, Culture, Sports, Science, and Technology (23135519, 24500409, 15H04266 to T. F.; 15K19274 to D. H.; 26430015, 15H01663 to K. C. N.; 15K14333, 15H01430, 16H01426, 16H04663 to H. H.).

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Hirai, D., Nakamura, K.C., Shibata, Ki. et al. Shaping somatosensory responses in awake rats: cortical modulation of thalamic neurons. Brain Struct Funct 223, 851–872 (2018). https://doi.org/10.1007/s00429-017-1522-z

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Keywords

  • Barrel cortex
  • Corticothalamic
  • Thalamus
  • Burst and tonic modes
  • Lesion