Brain dynamics in the primate audiomotor circuit during isochronous beat perception and entrainment
Hugo Merchant
Institute of Neurobiology, National University of Mexico
The ability to extract the regular pulse in music and to respond in synchrony to this pulse is called beat synchronization and is a natural human behavior exhibited during dancing and musical ensemble playing. Previously, we showed that macaques can predictively entrain to isochronous metronomes, although they have a bias towards visual rather than auditory rhythmic stimuli (Gamez et al., 2018). In this study we recorded the simultaneous activity of hundreds of cells in the core (A1) and belt (A2) areas of the auditory cortex as well as in the medial premotor areas (SMA) when monkeys performed both a task that included beat perception (BP) and tapping synchronization (TS) epochs and during passive listening of the metronome. Notably, we found that both A1 and A2 not only showed responses associated with auditory sensation in all tasks, but also neural signals related with active sensing. The latter showed activity that increased during BP and TS with a switch in response phase from sensory driven, tens of ms after the stimulus in the passive condition, to a predictive sensory response during BP and TS. In addition, some A2 neurons showed neural responses aligned to the tapping movements, suggesting that the auditory cortex has access to an internal beat prediction signal, probably coming from the cortical premotor system. Indeed, in SMA we found time-varying single-cell responses which, when projected into a low dimensional space, formed rotatory population neural trajectories that showed two main properties. First, a complete circular loop was formed for each produced interval, converging to a similar state-space location close to the tapping time. The convergence to this neural attractor state could be the internal representation of the pulse that is transmitted as a phasic top-down signal to the auditory areas before each tap. Second, these oscillatory trajectories did not overlap across durations, a signature of temporal scaling; instead, they showed a linear increase in their radius as a function of the target interval (Gamez et al., 2019). These preliminary results give experimental support to the notion of a dynamic interplay between the active sensing signals of the auditory areas and the internal beat representation of medial premotor system during rhythmic perception and entrainment.
Gamez J., Yc, K., Ayala, Y., Prado, L. and Merchant, H. Predictive rhythmic tapping to isochronous and tempo changing metronomes in the nonhuman primate. ANYAS. (2018) 1423: 396–414.
Gamez J, Mendoza, G., Prado, L. Betancourt, A., and Merchant, H*. The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping. PLoS Biol (2019) 17(4): e3000054.