Reward-driven emergence of auditory pattern encoding in the primate motor system

The ability to anticipate rhythmic patterns is fundamental to human experience, enabling music appreciation, speech comprehension, and dancing in sync to music. How the brain learns to use acoustic information to guide motor behavior remains a key question whose neural underpinnings and evolutionary origins are debated, especially in non-human primates. To understand how brain areas involved in motor control naively respond to predictable tone patterns, we recorded large single neuron populations across primary somatosensory (S1), primary motor (M1), dorsal premotor (PMd), supplementary motor (SMA), pre-supplementary motor (preSMA) cortices, globus pallidus interna (GPi), and medial geniculate body (MGB) of a rhesus monkey. During passive listening (Experiment 1) with a reward only at the end of each trial, primarily the MGB, not motor areas, responded to the auditory tone patterns, ruling out the spontaneous entrainment of motor activity to auditory patterns. Almost all areas robustly represented the elapsed time within the trial, suggesting a general tracking of trial progression and reward structure. Next, we tested if motor areas learn to respond to auditory patterns if associated with rewards. When each tone was simultaneously accompanied by a liquid reward (Experiment 2), all areas except S1 showed clear responses to the tone patterns. To test if the tone responses persisted, the reward contingency was subsequently removed (Experiment 3). Strikingly, although the reward was delivered only at the trials end as in Experiment 1, GPi neurons continued to track the occurrence of the tones. These findings suggest that while basic sensory processing of tone patterns occurs in the MGB, higher-order processing in motor areas is profoundly shaped by reward association. This reorganisation of neural responsiveness shows that the capacity for auditory association can be elicited in the motor system through appropriate motivational contexts.