Thalamocortical credit routing from the basal ganglia and cerebellum: anatomical constraints and circuit principles
- 1Institute of Science Tokyo
Abstract
Animals learn to select actions that maximize reward in complex environments. A central challenge in this process is credit routing: behavioral outcomes must be routed back to the neural populations that contributed to generating the relevant actions. One possible route is through thalamocortical pathways conveying learning signals from the basal ganglia and cerebellum, where plasticity is shaped by reward-prediction errors. However, how these pathways route such signals back to specific cortical circuits remains unclear. To address this question, we combined anatomical circuit mapping in mice with closed-loop circuit modeling. Anterograde transsynaptic tracing revealed that thalamic neurons receiving input from the substantia nigra pars reticulata or the lateral cerebellar nucleus were largely segregated, with partial overlap in the ventromedial thalamus. Nevertheless, their cortical axons shared a pronounced enrichment in layer 1a, most prominently in secondary motor cortex. In a brain- wide synergistic loop-circuit model, learning was enhanced when both pathways delivered additive and gain-modulating feedback aligned with the cortical action readout. Local activity- based calibration established this alignment, whereas dendritic-spike- and reward-prediction- error-dependent thalamocortical plasticity further refined behavioral output. Module-specific feedback was essential for a brain-machine interface task requiring the simultaneous conditioning of multiple target neurons. Together, these findings define a credit-routing architecture in which laminar convergence, plastic alignment, and modular feedback link parallel subcortical learning systems to cortical action representations.
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BibTeX
@misc{tanno2026thalamocortical,
title = {{Thalamocortical credit routing from the basal ganglia and cerebellum: anatomical constraints and circuit principles}},
author = {S. Tanno and M. Morishima and K. Fujita and S. Kato and K. Kobayashi and Y. Kawaguchi and Y. Isomura and R. Hira},
howpublished = {bioRxiv},
year = {2026},
month = oct,
doi = {10.64898/2026.10.02.755501},
url = {https://www.biorxiv.org/content/10.64898/2026.10.02.755501v1},
note = {CC BY},
}
RIS
TY - UNPB
TI - Thalamocortical credit routing from the basal ganglia and cerebellum: anatomical constraints and circuit principles
AU - S. Tanno
AU - M. Morishima
AU - K. Fujita
AU - S. Kato
AU - K. Kobayashi
AU - Y. Kawaguchi
AU - Y. Isomura
AU - R. Hira
PY - 2026
DA - 2026/10/02
PB - bioRxiv
DO - 10.64898/2026.10.02.755501
UR - https://www.biorxiv.org/content/10.64898/2026.10.02.755501v1
AB - Animals learn to select actions that maximize reward in complex environments. A central challenge in this process is credit routing: behavioral outcomes must be routed back to the neural populations that contributed to generating the relevant actions. One possible route is through thalamocortical pathways conveying learning signals from the basal ganglia and cerebellum, where plasticity is shaped by reward-prediction errors. However, how these pathways route such signals back to specific cortical circuits remains unclear. To address this question, we combined anatomical circuit mapping in mice with closed-loop circuit modeling. Anterograde transsynaptic tracing revealed that thalamic neurons receiving input from the substantia nigra pars reticulata or the lateral cerebellar nucleus were largely segregated, with partial overlap in the ventromedial thalamus. Nevertheless, their cortical axons shared a pronounced enrichment in layer 1a, most prominently in secondary motor cortex. In a brain- wide synergistic loop-circuit model, learning was enhanced when both pathways delivered additive and gain-modulating feedback aligned with the cortical action readout. Local activity- based calibration established this alignment, whereas dendritic-spike- and reward-prediction- error-dependent thalamocortical plasticity further refined behavioral output. Module-specific feedback was essential for a brain-machine interface task requiring the simultaneous conditioning of multiple target neurons. Together, these findings define a credit-routing architecture in which laminar convergence, plastic alignment, and modular feedback link parallel subcortical learning systems to cortical action representations.
ER -