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Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex

Abstract

Neuronal activity in the motor cortex is understood to be correlated with movements, but the impact of action potentials (APs) in single cortical neurons on the generation of movement has not been fully determined. Here we show that trains of APs in single pyramidal cells of rat motor cortex can evoke long sequences of small whisker movements. For layer-5 pyramids, we find that evoked rhythmic movements have a constant phase relative to the AP train, indicating that single layer-5 pyramids can reset the rhythm of whisker movements. Action potentials evoked in layer-6 pyramids can generate bursts of rhythmic whisking, with a variable phase of movements relative to the AP train. An increasing number of APs decreases the latency to onset of movement, whereas AP frequency determines movement direction and amplitude. We find that the efficacy of cortical APs in evoking whisker movements is not dependent on background cortical activity and is greatly enhanced in waking rats. We conclude that in vibrissae motor cortex sparse AP activity can evoke movements.

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Figure 1: Whisker movements evoked by intracellular stimulation of an L6 pyramidal neuron.
Figure 2: Action potential initiation specifically evokes whisker movements.
Figure 3: Whisker movements evoked by intracellular stimulation of single L5 and L6 cells.
Figure 4: Effect of AP number and frequency on evoked movements.
Figure 5: Efficacy of APs initiated in cortical up states and down states with and without prestimulation movement.
Figure 6: Cortical APs are more effective in awake rats.

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Acknowledgements

We thank I. Manns, R. Friedrich, C. Schwarz, W. Denk and S. Petrou for comments and R. Erickson for inspiration; E. Heil, M. Kaiser, R. Rödel, P. Mayer and K. Schmidt for technical assistance; and A. Krauss, S. Muhammad, S. Bellanca and L. Sinai-Esfahani for help with cell staining and reconstruction. This work was supported by the Max Planck Society, the NHMRC of Australia and the Wellcome Trust.

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Correspondence to Michael Brecht.

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Supplementary information

Supplementary Figure 1

Comparison of L5- and L6-cell stimulation effects. (PDF 27 kb)

Supplementary Figure 2

Effect of action potential frequency and number on evoked movements: averaged traces. (PDF 36 kb)

Supplementary Figure 3

Interaction of initiated action potentials with cortical up states and down states. (PDF 567 kb)

Supplementary Movie 1

Whisker movements evoked by intracellular stimulation of an L6 cell. (MP4 2457 kb)

Supplementary Movie 2

Whisker movements evoked by intracellular stimulation of an L5 cell. (MP4 2493 kb)

Supplementary Figure, Movies Legends and References (DOC 153 kb)

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Brecht, M., Schneider, M., Sakmann, B. et al. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704–710 (2004). https://doi.org/10.1038/nature02266

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