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

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. In mammals, a key brain structure in motor control is the primary motor cortex (M1), a large frontal cortical area1−3. The role of M1 neurons in generating movements has been explored by extracellular stimulation with small currents (intracortical microstimulation)4 and by extracellular recordings of single neurons5, 6. Extracellular stimulation experiments in M1 have shown that there are very low current thresholds (as low as 1−2 µA) for movement initiation3 that are thought to stimulate few cortical neurons7, 8. Extracellular recordings from single cells in M1 of awake, behaving monkeys have also shown that there is a close match between AP activity and movement6. The quantitative analysis of such recordings by an AP population vector9, 10 and by real−time analysis of AP activity in M1−motivated by the desire to construct cortically controlled neuroprosthetic devices11−14−has led to the conclusion that the activity of only a few hundred to a few tens of neurons is sufficient to specify accurately complex limb movements. The relationship between neuronal and muscular activity has been also analysed by computing averages of muscle activity (assayed by electromyographic recordings) triggered relative to neuronal APs15. This technique has revealed significant correlations between cortical single−cell activity and muscle activity15−17. Thus, extracellular stimulation and recording studies indicate that there is a close correlation between activity in the motor cortex and muscular activity, consistent with the known synaptic connectivity between cortex and motoneurons16. Intracellular stimulation of cortical cells evokes changes in electromyographic recordings18 and might allow a more direct investigation of the relationship between cortical APs and movement. In rats, whisker movements can escape from sleep or anaesthesia−induced paralysis19, 20. Such movements are rhythmic, are restricted to the plane of the whisker row, and can be quantified as a simple back−and−forth movement21−24. The movements of individual whiskers can be tracked readily, making them a convenient system to quantitatively study the generation of motor output25. Here we have used whole−cell recordings to examine the motor effects of intracellularly evoked APs in identified layer−5 (L5) and layer−6 (L6) pyramidal cells in the vibrissae motor cortex26 of anaesthetized rats