Tuned thalamic excitation is amplified by visual cortical circuits

Abstract

Cortical neurons in thalamic recipient layers receive excitation from the thalamus and the cortex. The relative contribution of these two sources of excitation to sensory tuning is poorly understood. We optogenetically silenced the visual cortex of mice to isolate thalamic excitation onto layer 4 neurons during visual stimulation. Thalamic excitation contributed to a third of the total excitation and was organized in spatially offset, yet overlapping, ON and OFF receptive fields. This receptive field structure predicted the orientation tuning of thalamic excitation. Finally, both thalamic and total excitation were similarly tuned to orientation and direction and had the same temporal phase relationship to the visual stimulus. Our results indicate that tuning of thalamic excitation is unlikely to be imparted by direction- or orientation-selective thalamic neurons and that a principal role of cortical circuits is to amplify tuned thalamic excitation.

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Figure 1: Isolating thalamic excitation.
Figure 2: Receptive field structure of thalamic excitation.
Figure 3: Orientation tuning of thalamic excitation.
Figure 4: Separation of ON and OFF thalamic subfields predicts preferred orientation of thalamic excitation.
Figure 5: Tuning of non-thalamic excitatory charge.
Figure 6: Tuning of non-thalamic excitatory F1 modulation.
Figure 7: Co-tuning and phase relationship between thalamic and non-thalamic excitation.

Change history

  • 16 July 2018

    In the published version of this article, a data point is missing from Fig. 4f, and the y-axis label reads "RFpre"; it should read "RFpref". The original article has not been corrected. The original and corrected figures are shown in the accompanying Publisher Correction.

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Acknowledgements

We thank J. Evora for help with genotyping and mouse husbandry, J. Isaacson, E. Chichilnisky and the members of the Scanziani and Isaacson laboratories for helpful discussions of this project, and S. Olsen and K. Reinhold for help with dLGN recordings. This project was supported by the Gatsby charitable foundation, the Brain and Behavior Research Foundation and the Howard Hughes Medical Institute.

Author information

A.D.L. and M.S. designed the study. A.D.L. conducted all experiments and analysis. A.D.L. and M.S. wrote the paper.

Correspondence to Anthony D Lien or Massimo Scanziani.

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Lien, A., Scanziani, M. Tuned thalamic excitation is amplified by visual cortical circuits. Nat Neurosci 16, 1315–1323 (2013) doi:10.1038/nn.3488

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