How Beat Perception Co-opts Motor Neurophysiology

Abstract

Beat perception offers cognitive scientists an exciting opportunity to explore how cognition and action are intertwined in the brain even in the absence of movement. Many believe the motor system predicts the timing of beats, yet current models of beat perception do not specify how this is neurally implemented. Drawing on recent insights into the neurocomputational properties of the motor system, we propose that beat anticipation relies on action-like processes consisting of precisely patterned neural time-keeping activity in the supplementary motor area (SMA), orchestrated and sequenced by activity in the dorsal striatum. In addition to synthesizing recent advances in cognitive science and motor neuroscience, our framework provides testable predictions to guide future work.

Keywords: basal ganglia; beat perception; motor system; music cognition; supplementary motor area.

Figure 1:. Beat perception and the motor system.

A) A simple, repeating non-isochronous rhythm is shown in music notation and illustrated as an acoustic waveform. The rhythm induces an isochronous beat percept (beat locations shown by triangle tips). Note that some beats are not marked by sounds (hollow triangles), and some sounds occur at non-beat times. The reader is encouraged to listen to the corresponding sound example (in which the above rhythm is looped several times) to verify the beat percept. B) A simplified schematic of the direct pathway loop connecting the two key areas discussed in this paper in reference to beat perception. The supplementary motor area (SMA) projects to the dorsal striatum (consisting of the putamen and caudate nucleus). Dorsal striatum inhibits the internal segment of globus pallidus (shown here hidden behind the striatum), which inhibits thalamus. Closing the loop, thalamus excites SMA. During physical movement, this pathway is thought to selectively disinhibit populations in SMA necessary for the next sub-movement in a sequence. Here, we propose that the same process is used to disinhibit populations that generate the temporal dynamics necessary to covertly anticipate the next beat in a rhythm. Figure adapted from [117]. CC BY 3.0 https://creativecommons.org/licenses/by/3.0/

Figure 2:. Illustration of time-keeping by a neural firing rate trajectory.

In monkey SMA, reliably patterned fluctuations in the collective firing rates of neural populations keep time during deliberately timed behaviors like rhythmic tapping. These fluctuations can be visualized as tracing out paths (“trajectories”) in a high-dimensional space of firing rates, with the shape and time course of the path dependent on the time course of the behavior. A) Fluctuations in the firing rates of three neurons graphed over time during a timed behavior. B) The same fluctuations visualized as a trajectory in a three-dimensional space, where each axis represents the firing rate of one neuron and each point on the trajectory represents the three firing rates at one point in time. Three example time points are marked. C) Trajectories traced by firing rates in large neural populations (i.e., hundreds, rather than just three) are easier to visually understand in “principal component” space [118], where each axis is a “component” corresponding to the correlated activation of many neurons, and where components accounting for the most combined variance in population firing rates are displayed. Empirical research on periodic tapping in monkeys shows that the firing-rate fluctuations in SMA between consecutive taps trace out circular trajectories in principal component space. For shorter inter-tap intervals, firing rates fluctuate faster but with lower amplitudes, creating smaller loops that repeat with a shorter period [46]. (Image adapted from the results of [46] and simplified for illustration.)

Figure 3:. Basal ganglia sequences the beat-tracking trajectories in SMA.

A) Once a beat has been inferred in an auditory rhythm, neural firing rates in SMA follow a trajectory which tracks progress through a beat cycle, informing the anticipation of the beat and possibly other sounds locked to the cycle (such as a subdivision of the beat, indicated by the “&” symbol on the trajectory). The activity of neurons generating this trajectory is initiated and reinforced by selective disinhibition by the basal ganglia: a population specific to the first beat cycle is active in dorsal striatum (blue). Acting through the internal segment of the Globus Pallidus (Gpi), this population disinhibits a thalamic population, which provides SMA with excitation specific to that trajectory. B) As the first beat cycle ends and the second beat arrives, some combination of SMA’s evolving input to dorsal striatum and inhibitory interactions within dorsal striatum activates a new striatal subpopulation (red). This population disinhibits a new subpopulation in SMA that allows SMA activity to continue to evolve along a new trajectory similar to the previous one. It spans the same time interval, but plays a different role in the metrical structure and may inform different auditory expectations specific to that beat cycle.