Complementary cortical and thalamic contributions to cell-type-specific striatal activity dynamics during movement

Coordinated motor behavior emerges from information flow across brain
regions. How long-range inputs influence cell-type-specific activity
within motor circuits remains unclear. The dorsolateral striatum (DLS)
contains direct- and indirect-pathway medium spiny neurons (dMSNs and
iMSNs) that exhibit distinct roles in movement control, and receives
converging cortical and thalamic inputs. We performed 2-photon imaging
from dMSNs, iMSNs, and their cortical and thalamic inputs identified by
monosynaptic rabies tracing, as mice executed a skilled locomotion task.
We used recurrent neural network (RNN) classifiers and hierarchical
clustering analyses to reveal functionally heterogeneous subpopulations in
each population. We found that dMSNs were preferentially active at
movement onset and offset, and iMSNs during execution. Cortical and
thalamic inputs were preferentially active during onset/offset and
execution, respectively. dMSN- and iMSN-projecting neurons in each region
showed similar trial-averaged activity patterns, although single-trial
features might contribute to cell-type-specific differences. Furthermore,
a subset of thalamic neurons projecting to dMSNs encoded rhythmic limb
movements in a locomotion phase-specific manner, a pattern also found in a
small subset of dMSNs. Inactivation of either cortex or thalamus
substantially reduced MSN activity. These results suggest that
corticostriatal and thalamostriatal inputs contribute complementary
motor-related information via shared and cell-type-specific pathways.