Representation of rhythmic chunking in striatum of mice executing complex continuous movement sequences.

We used a step-wheel system to examine the activity of striatal projection neurons as mice practiced stepping on complexly arranged foothold pegs in this Ferris-wheel-like device to receive reward. Sets of dorsolateral striatal projection neurons were sensitive to specific parameters of repetitive motor coordination during the runs. They responded to combinations of the parameters of continuous movements (interval, phase, and repetition), forming "chunking responses"-some for combinations of these parameters across multiple body parts. Recordings in sensorimotor cortical areas exhibited notably fewer such responses but were documented for smaller neuron sets whose heterogeneity was significant. Striatal movement encoding via chunking responsivity could provide insight into neural strategies governing effective motor control by the striatum. It is possible that the striking need for external rhythmic cuing to allow movement sequences by Parkinson's patients could, at least in part, reflect dysfunction in such striatal coding.

Rhythm Receptive Fields in Striatum of Mice Executing Complex Continuous Movement Sequences.

By the use of a novel experimental system, the step-wheel, we investigated the neural underpinnings of complex and continuous movements. We recorded neural activities from the dorsolateral striatum and found neurons sensitive to movement rhythm parameters. These neurons responded to specific combinations of interval, phase, and repetition of movement, effectively forming what we term "rhythm receptive fields." Some neurons even responsive to the combination of movement phases of multiple body parts. In parallel, cortical recordings in sensorimotor areas highlighted a paucity of neurons responsive to multiple parameter combinations, relative to those in the striatum. These findings have implications for comprehending motor coordination deficits seen in brain disorders including Parkinson's disease. Movement encoding by rhythm receptive fields should streamline the brain's capacity to encode temporal patterns, help to resolve the degrees of freedom problem. Such rhythm fields hint at the neural mechanisms governing effective motor control and processing of rhythmic information.

Emergence of rhythmic chunking in complex stepping of mice.

Motor chunking is important for motor execution, allowing atomization and efficiency of movement sequences. However, it remains unclear why and how chunks contribute to motor execution. To analyze the structure of naturally occurring chunks, we trained mice to run in a complex series of steps and identified the formation of chunks. We found that intervals (cycle) and the positional relationship between the left and right limbs (phase) of steps inside the chunks, unlike those outside the chunks, were consistent across occurrences. Further, licking by the mice was also more periodic and linked to the specific phases of limb movements within the chunk. Based on these findings, we propose the rhythm chunking hypothesis, whereby within chunks, the repetitive movements of many body parts are linked by the rhythm parameters: cycle and phase. The computational complexity of movement may thereby be reduced by adjusting movements as the combination of rhythms.

[Generation of Gait Rhythm in Mice].

The arrangement of a series of repetitive motions on the time axis should be planned while constructing continuous movement. To understand the mechanism for planning continuous movement and its neural basis, mice were trained to perform complicated continuous step running. The repeated foot movements and neural activities of the animals were recorded. The scaffolding peg arrangement was complex; however, the steps turned out to be more rhythmic, indicating that the mice adjusted to repeat their movements periodically rather than fitting their foot timing with the peg arrangement. In addition, neural activity recorded from the striatum was also found to be rhythmic, suggesting that the striatum may be involved in converting complex inputs into more rhythmic outputs.