Corticospinal neurons encode complex motor signals that are broadcast to dichotomous striatal circuits

Abstract

SummarySensorimotor cortex controls movement in part through direct projections to the spinal cord. Here we show that these corticospinal neurons (CSNs) possess axon collaterals that innervate many supraspinal brain regions critical for motor control, most prominently the main input to the basal ganglia, the striatum. Corticospinal neurons that innervate the striatum form more synapses on D1-than D2-striatal projection neurons (SPNs). This biased innervation strategy corresponds to functionally distinct patterns of termination in spinal cord. CSNs are strongly driven during a striatum-dependent sequential forelimb behavior, and often represent high level movement features that are not linearly related to kinematic output. Copies of these activity patterns are relayed in a balanced fashion to both D1 and D2 projection pathways. These results reveal a circuit logic by which motor cortex corticospinal neurons relay both kinematic-related and unrelated signals to distinct striatal and spinal cord pathways, where postsynaptic connectivity ultimately dictates motor specificity.HighlightsCorticospinal neurons send axon collaterals most abundantly to the striatumBiases in striatal innervation correspond to biases in spinal innervationCSNs represent complex movement sequence informationCorollary motor sequence signals are relayed to both striatal projection pathwayseTOC BlurbNelson, A. et al. detail the organization of corticospinal neurons and their coordinated cell type-specific targets in the dorsolateral striatum and spinal cord. Corticospinal neurons encode both kinematic-related and unrelated signals during motor sequences, and relay this information in a balanced fashion to dichotomous striatal pathways.

The Contribution of Premotor Cortico-Striatal Projections to the Execution of Serial Order Sequences

“…3B). These results show that both M2 and M1 contain units encoding the sequences' execution (Berlot et al, 2020;Nelson et al, 2020).…”

“…3 B ). These results show that both M2 and M1 contain units encoding the sequences’ execution ( Nelson et al, 2020 ; Berlot et al, 2021 ). However, it must be acknowledged that the lack of differences in some of the comparisons between M2 and M1 may be influenced by the small set of recorded cells (34 cells from M2 and 26 from M1).…”

“…suggested (Nelson et al, 2020;Wall et al, 2013) to direct the structuring of sequences in serial order tasks (Rothwell et al, 2015), though only after learning.…”

pyControl: Open source, Python based, hardware and software for controlling behavioural neuroscience experiments

“…Task and hardware definition files for these experiments are provided in the manuscripts data repository. For additional use cases see the following studies (Korn et al, 2019;Akam et al, 2020;Koralek and Costa, 2020;Nelson et al, 2020).…”

Pyramidal tract neurons drive feed-forward excitation of striatum through cholinergic interneurons

“…The somata of IT neurons span cortical L5 and their axons extend within ipsi- and contralateral cortical areas, and also to the ipsi-and contralateral striatum. On the other hand, PT somata are located in deep L5 and their corticofugal projections send collaterals to several ipsilateral subcortical structures, predominating those to the ipsilateral striatum ( Nelson et al , 2020). Moreover, while IT axons synapse onto PTs, direct PT contacts onto ITs are rare, suggesting a hierarchical IT→PT anatomo-functional organization ( Morishima , 2006; Brown and Hestrin , 2009; Anderson et al , 2010; Kiritani et al , 2012).…”