The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping

Abstract

Our motor commands can be exquisitely timed according to the demands of the environment, and the ability to generate rhythms of different tempos is a hallmark of musical cognition. Yet, the neuronal underpinnings behind rhythmic tapping remain elusive. Here, we found that the activity of hundreds of primate medial premotor cortices (MPCs; pre-supplementary motor area [preSMA] and supplementary motor area [SMA]) neurons show a strong periodic pattern that becomes evident when their responses are projected into a state space using dimensionality reduction analysis. We show that different tapping tempos are encoded by circular trajectories that travelled at a constant speed but with different radii, and that this neuronal code is highly resilient to the number of participating neurons. Crucially, the changes in the amplitude of the oscillatory dynamics in neuronal state space are a signature of duration encoding during rhythmic timing, regardless of whether it is guided by an external metronome or is internally controlled and is not the result of repetitive motor commands. This dynamic state signal predicted the duration of the rhythmically produced intervals on a trial-by-trial basis. Furthermore, the increase in variability of the neural trajectories accounted for the scalar property, a hallmark feature of temporal processing across tasks and species. Finally, we found that the interval-dependent increments in the radius of periodic neural trajectories are the result of a larger number of neurons engaged in the production of longer intervals. Our results support the notion that rhythmic timing during tapping behaviors is encoded in the radial curvature of periodic MPC neural population trajectories.

Trial-by-trial predictions of subjective time from human brain activity

“…Neither approach is able to intrinsically account for biases in subjective duration by content because both are rooted in the idea that the brain attempts to track clock time. While tracking clock time is likely to be useful for short, repetitive motor commands such as drumming (11)(12)(13)(14) this is not necessarily the case for longer intervals, and indeed as established, subjective experience of longer intervals is characterized more by deviation from rather than adherence to clock time.…”

“…Many animal and human electrophysiology and neuroimaging studies have searched for potential neural regions or putative mechanisms underlying time perception (15,16). This literature finds potential mechanisms in a diverse set of regions including pre-/supplementary motor areas (11,14,17), parietal areas (18,19), insula (20), midbrain dopaminergic neurons (21), and hippocampus and entorhinal cortex (22)(23)(24)(25). The diversity of neural regions apparently associated with human time perception supports the intuition underlying the population clock approach -that the dynamics of a neural system can be interpreted as reflecting time to an external observer because it is dynamic, i.e.…”

Neural trajectories in the supplementary motor area and primary motor cortex exhibit distinct geometries, compatible with different classes of computation

“…Our motivating hypothesis, derived from prior studies 7,11,[14][15][16][19][20][21][39][40][41] , is that SMA tracks internal and/or 74 contextual factors for the purpose of guiding action. If so, the SMA population response should be 75 shaped by the need to consistently distinguish situations that involve different future actions, even if the 76 current motor output is identical.…”

A Temporal Signal-Processing Circuit Based on Spiking Neuron and Synaptic Learning

“…It has also been found that there is tuning for interval and/or serial order as an orderly change in the power of transient modulations in β- and γ- bands across putaminal LFPs during the execution of the SCT (Bartolo et al, 2014). Recent research shows that the neural population trajectories during SCT in SMA/preSMA can act as a neural clock (Gámez et al, 2019). However, the neural code linked to the temporal production of this neural clock during SCT remains unknown.…”