To prepare timely motor actions, we constantly predict future events. Regularly repeating events are often perceived as a rhythm to which we can readily synchronize our movements, just as in dancing to music. However, the neuronal mechanisms underlying the capacity to encode and maintain rhythms are not understood. We trained nonhuman primates to maintain the rhythm of a visual metronome of diverse tempos and recorded neural activity in the supplementary motor area (SMA). SMA exhibited rhythmic bursts of gamma band (30–40 Hz) reflecting an internal tempo that matched the extinguished visual metronome. Moreover, gamma amplitude increased throughout the trial, providing an estimate of total elapsed time. Notably, the timing of gamma bursts and firing rate modulations allowed predicting whether monkeys were ahead or behind the correct tempo. Our results indicate that SMA uses dynamic motor plans to encode a metronome for rhythms and a stopwatch for total elapsed time.

Timing is a fundamental variable for behavior. However, the mechanisms allowing human and non-human primates to synchronize their actions with periodic events are not yet completely understood. Here we characterize the ability of rhesus monkeys and humans to perceive and maintain rhythms of different paces in the absence of sensory cues or motor actions. In our rhythm task subjects had to observe and then internally follow a visual stimulus that periodically changed its location along a circular perimeter. Crucially, they had to maintain this visuospatial tempo in the absence of movements. Our results show that the probability of remaining in synchrony with the rhythm decreased, and the variability in the timing estimates increased, as a function of elapsed time, and these trends were well described by the generalized law of Weber. Additionally, the pattern of errors shows that human subjects tended to lag behind fast rhythms and to get ahead of slow ones, suggesting that a mean tempo might be incorporated as prior information. Overall, our results demonstrate that rhythm perception and maintenance are cognitive abilities that we share with rhesus monkeys, and these abilities do not depend on overt motor commands.

17To prepare timely motor actions we constantly predict future events. Regularly repeating 18 events are often perceived as a rhythm to which we can readily synchronize our movements, 19 just as in dancing to music. However, the neuronal mechanisms underlying the capacity to 20 encode and maintain rhythms are not understood. We trained nonhuman primates to maintain 21 the rhythm of a visual metronome of different tempos and then we recorded neural activity in 22 the supplementary motor area (SMA). SMA exhibited rhythmic bursts of gamma band (30-40 23 Hz) reflecting an internal tempo that matched the extinguished visual metronome. Moreover, 24 gamma amplitude increased throughout the trial and provided an estimate of total elapsed 25 time. Notably, the timing and amplitude of gamma bursts reflected systematic timing biases 26 and errors in the behavioral responses. Our results indicate that premotor areas use dynamic 27 motor plans to encode a metronome for rhythms and a stopwatch for total elapsed time.28 65 appeared on one side, switched to the other, and the back to the initial location. This 66 alternating stimulus defined three entrainment intervals of an isochronous rhythm. On each 67 trial the interval duration was pseudo-randomly chosen to be 500, 750, or 1000 ms. In this 68 manner, animals were presented with a visual metronome whose tempo was changed on a 69 trial-by-trial basis ( Figure 1A). 70 71 5 72 Figure 1. The visual metronome task.73 (A) Rhythms of different tempos were defined by a left-right alternating visual stimulus that appeared on a touch 74 screen. While keeping eye and hand fixation, subjects first observed three isochronous entrainment intervals with 75 duration of either 500, 750, or 1000 ms (pseudo-randomly selected on each trial). After the last entrainment 76 interval, the visual stimulus disappeared initiating the maintenance intervals, during which the subjects had to 77 keep track of the stimulus' virtual location (left of right, broken lines). A go-cue (extinction of the hand fixation) at 78 6 the middle of one of the four maintenance intervals prompted the subjects to reach towards the estimated location 79 of the stimulus. It is important to note that this was not an interception task because the left-right switching 80 stopped at the time of the go-cue. Monkeys received a liquid reward when correctly indicating the stimulus 81 location. 82 (B) The proportion of correct responses is plotted as a function of elapsed time during the maintenance intervals.83 Colors indicate the performance for the three tempos (500, 750, 1000 ms). Performance was significantly above 84 chance (broken line at p=0.5; z-test p<0.001; n=131 sessions; median ± I.Q.R. over sessions). The decrease in 85 performance as a function of elapsed time is expected from variability of the subjects' internal timing in the 86 absence of the external visual rhythm. This drop in performance was captured by a model of timing subject to 87 scalar variability (continuous lines).88 (C) Reaction times to th...

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Imagine practicing a piece of music, or a speech, solely within the mind, without any sensory input or motor output. Our ability to implement dynamic internal representations is key for successful behavior, yet how the brain achieves this is not fully understood. Here we trained primates to perceive, and internally maintain, rhythms of different tempos and performed large-scale recordings of neuronal activity across multiple areas spanning the sensory-motor processing hierarchy. Results show that perceiving and maintaining rhythms engage multiple brain areas, including visual, parietal, premotor, prefrontal, and hippocampal regions. Each area displayed oscillatory activity that reflected the temporal and spatial characteristics of an internal metronome which flexibly encoded fast, medium, and slow tempos on a trial-by-trial basis. The presence of widespread metronome-related activity across the brain, in the absence of stimuli and overt actions, is consistent with the idea that time and rhythm are maintained by a mechanism that internally replays the stimuli and actions that define well-timed behavior.