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Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements

Abstract

Motor cortex neurons are activated at different times during self-initiated voluntary movement. However, the manner in which excitatory and inhibitory neurons in distinct cortical layers help to organize voluntary movement is poorly understood. We carried out juxtacellular and multiunit recordings from actively behaving rats and found temporally and functionally distinct activations of excitatory pyramidal cells and inhibitory fast-spiking interneurons. Across cortical layers, pyramidal cells were activated diversely for sequential motor phases (for example, preparation, initiation and execution). In contrast, fast-spiking interneurons, including parvalbumin-positive basket cells, were recruited predominantly for motor execution, with pyramidal cells producing a command-like activity. Thus, fast-spiking interneurons may underlie command shaping by balanced inhibition or recurrent inhibition, rather than command gating by temporally alternating excitation and inhibition. Furthermore, initiation-associated pyramidal cells excited similar and different functional classes of neurons through putative monosynaptic connections. This suggests that these cells may temporally integrate information to initiate and coordinate voluntary movement.

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Figure 1: Efficient operant learning of the voluntary forelimb-movement task.
Figure 2: Diverse functional activation of identified pyramidal cells.
Figure 3: Movement-associated activation in identified fast-spiking interneurons.
Figure 4: Contrasting functional diversity between pyramidal cells and fast-spiking interneurons.
Figure 5: Time course and specificity in pyramidal cells and fast-spiking interneurons with movement activity.
Figure 6: Excitatory synaptic interactions between functionally different neurons.

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Acknowledgements

We thank G. Buzsáki and J. Tanji for helpful comments and discussion, M. Fujii, K. Ishii, M. Kobayashi, R. Nakatomi and S. Tanaka for technical assistance, and K. O'hara for developing the multi-rat task-training system. This work was supported by the institutional research grants from RIKEN (T.F.) and by Grants-in-Aid for Scientific Research from Ministry of Education, Culture, Sports, Science and Technology (18019041 and 18700386 to Y.I. and 40218871 to T.F.).

Author information

Authors and Affiliations

Authors

Contributions

Y.I. designed the experiments. Y.I., R.H. and H.A. performed the experiments. Y.I. and T.T. analyzed the data. Y.I. and T.F. wrote the paper.

Corresponding author

Correspondence to Yoshikazu Isomura.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8 (PDF 877 kb)

Supplementary Video 1

Initial behavior of an untrained rat in the training box. This beginner rat entered the body-supporting cylinder by himself, because he had become accustomed to a dummy cylinder (see Supplementary Figure 1c). After his head-attachment was fastened to the stereotaxic frame, the rat grasped the lever naturally and tried to move it with his right forelimb without struggling. (MPG 2886 kb)

Supplementary Video 2

Efficient task-training of six rats in separate training boxes. Up to six rats were simultaneously and separately trained in our multi-rat task-training system to perform the voluntary forelimb movement task in the head-restraint condition. The rat in the lower right box (no. 6) was a beginner in the forelimb movement task. (MPG 2388 kb)

Supplementary Video 3

Pre-movement spiking activity during task performance (with sound). Pre-movement activity was recorded juxtacellularly from the layer 6 pyramidal cell shown in Supplementary Figure 6a while the rat was moving the lever. The sound represents the spiking of this neuron. (MPG 1886 kb)

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Isomura, Y., Harukuni, R., Takekawa, T. et al. Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12, 1586–1593 (2009). https://doi.org/10.1038/nn.2431

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