Premotor population dynamics as neural substrate for auditory and visual rhythmic entrainment

Abstract

Precise timing is a fundamental requisite for a select group of complex actions, such as music appreciation and performance, where subjects extract the regular beat of a rhythmic sequence to generate an internal pulse representation that allows for predictive responses to the beat. The neural substrate for beat extraction and response entrainment to auditory and visual rhythms is still largely unknown. Here we recorded and analyzed the population activity of hundreds of MPC neurons of two rhesus monkeys performing an isochronous tapping task guided by brief flashing stimuli or auditory tones. The animals showed a strong bias towards visual metronomes, with rhythmic tapping that was more precise and accurate than for auditory metronomes. The population dynamics in state space as well as the corresponding neural sequences shared the following properties across modalities: the circular dynamics of the neural trajectories and the neural sequences formed a regenerating loop for every produced interval, producing a relative time representation; the trajectories converged in similar state space at tapping times while the moving bumps restart at this point, resetting the beat-based clock; the tempo of the synchronized tapping was encoded by a combination of amplitude modulation and temporal scaling in the neural trajectories. The latter correlated with a mixture of response duration and recruitment properties in the neural sequences. In addition, the modality induced a displacement in the neural trajectories in auditory and visual subspaces without greatly altering time keeping mechanism. These results suggest that the interaction between the amodal internal representation of pulse within MPC and a modality specific external input generates a neural rhythmic clock whose dynamics define the temporal execution of tapping using auditory and visual metronomes.