How neuronal activity of motor cortex is related to movement is a central topic in motor neuroscience. Motor-cortical single neurons are more closely related to hand movement velocity than speed, that is, the magnitude of the (directional) velocity vector. Recently, there is also increasing interest in the representation of movement parameters in neuronal population activity, such as reflected in the intracranial EEG (iEEG). We show that in iEEG, contrasting to what has been previously found on the single neuron level, speed predominates over velocity. The predominant speed representation was present in nearly all iEEG signal features, up to the 600–1000 Hz range. Using a model of motor-cortical signals arising from neuronal populations with realistic single neuron tuning properties, we show how this reversal can be understood as a consequence of increasing population size. Our findings demonstrate that the information profile in large population signals may systematically differ from the single neuron level, a principle that may be helpful in the interpretation of neuronal population signals in general, including, for example, EEG and functional magnetic resonance imaging. Taking advantage of the robust speed population signal may help in developing brain–machine interfaces exploiting population signals.

In neuronal population signals, including the electroencephalogram (EEG) and electrocorticogram (ECoG), the low-frequency component (LFC) is particularly informative about motor behavior and can be used for decoding movement parameters for brain-machine interface (BMI) applications. An idea previously expressed, but as of yet not quantitatively tested, is that it is the LFC phase that is the main source of decodable information. To test this issue, we analyzed human ECoG recorded during a game-like, one-dimensional, continuous motor task with a novel decoding method suitable for unfolding magnitude and phase explicitly into a complex-valued, time-frequency signal representation, enabling quantification of the decodable information within the temporal, spatial and frequency domains and allowing disambiguation of the phase contribution from that of the spectral magnitude. The decoding accuracy based only on phase information was substantially (at least 2 fold) and significantly higher than that based only on magnitudes for position, velocity and acceleration. The frequency profile of movement-related information in the ECoG data matched well with the frequency profile expected when assuming a close time-domain correlate of movement velocity in the ECoG, e.g., a (noisy) “copy” of hand velocity. No such match was observed with the frequency profiles expected when assuming a copy of either hand position or acceleration. There was also no indication of additional magnitude-based mechanisms encoding movement information in the LFC range. Thus, our study contributes to elucidating the nature of the informative LFC of motor cortical population activity and may hence contribute to improve decoding strategies and BMI performance.