P-17 Cortical-subcortical information flow reverses from naive to skilled movements

TY - JOUR

T1 - P-17 Cortical-subcortical information flow reverses from naive to skilled movements

AU - Lemke, Stefan

AU - Celotto, Marco

AU - Maffulli, R.

AU - Ganguly, K.

AU - Panzeri, Stefano

PY - 2023

Y1 - 2023

N2 - Background: Despite the dense interconnectivity of the brain’smotor network, cortical and subcortical motor regions are associatedwith distinct types of movements. Stable or habitual actions are classicallylinked to subcortical regions, while more flexible or exploratorycontrol is commonly attributed to cortex. Nonetheless, no studyhas investigated how motor-specific information is transmittedbetween cortical and subcortical regions at different stages oflearning.Objective: Studying how cortical and subcortical regions communicateduring the learning of a reach-to-grasp task by monitoring neuralsignals in motor cortex (M1) and dorsolateral striatum (DLS) asrats produce naive exploratory and stable skilled movements.Methods: We used information theory to measure the timing ofinformation encoded about task-relevant movement features in M1and DLS at different stages of learning. Then, we applied the recentlydeveloped measure of Feature-specific Information Transfer (FIT) tomeasure the motor-specific information flow between M1 and DLS.FIT merges the Wiener-Granger causality principle of informationtransmission with feature-specificity. In doing so, FIT extends previousmethodologies such as Directed Information (DI) which measuresthe total, non-feature-specific, information transmissionbetween neural signals. By measuring both FIT and DI, we could dissociatethe transmission that was specifically about movement fromthe overall information flow between M1 and DLS. Lastly, we developeda simple network model to understand which type of modificationin the structure of the M1-DLS network could reproduce theresults we obtained from experimental data.Results: We found that the timing of motor information in M1 andDLS changed from naïve to skilled stages of learning. In particular,the motor-information peaks in DLS were anticipated in time, whilethey occurred later in M1, in the skilled compared to the naïve condition.Crucially, using FIT, we measured that the directionality ofmotor-specific information transmission between M1 and DLSreversed with learning, with motor information flowing mainly fromM1 to DLS in the naïve and from DLS to M1 in the skilled condition.This reversal was hidden when measuring overall neural informationtransmission with DI, which bi-directionally increased between M1and DLS with learning. We could reproduce the above results in anetwork model by reversing the area that originated the motorspecificinformation, going from a cortical-origin during naive movementsto a striatal-origin during skilled movements.Conclusion: Our results provide evidence of a reversal in the areaoriginating, and then transmitting motor-specific information withinthe M1-DLS network as rats learned a reach-to-grasp task. Such findingprovide essential support to the idea that cortical and subcorticalregions have a leading role in controlling, respectively, naïve andautomatized movements.

AB - Background: Despite the dense interconnectivity of the brain’smotor network, cortical and subcortical motor regions are associatedwith distinct types of movements. Stable or habitual actions are classicallylinked to subcortical regions, while more flexible or exploratorycontrol is commonly attributed to cortex. Nonetheless, no studyhas investigated how motor-specific information is transmittedbetween cortical and subcortical regions at different stages oflearning.Objective: Studying how cortical and subcortical regions communicateduring the learning of a reach-to-grasp task by monitoring neuralsignals in motor cortex (M1) and dorsolateral striatum (DLS) asrats produce naive exploratory and stable skilled movements.Methods: We used information theory to measure the timing ofinformation encoded about task-relevant movement features in M1and DLS at different stages of learning. Then, we applied the recentlydeveloped measure of Feature-specific Information Transfer (FIT) tomeasure the motor-specific information flow between M1 and DLS.FIT merges the Wiener-Granger causality principle of informationtransmission with feature-specificity. In doing so, FIT extends previousmethodologies such as Directed Information (DI) which measuresthe total, non-feature-specific, information transmissionbetween neural signals. By measuring both FIT and DI, we could dissociatethe transmission that was specifically about movement fromthe overall information flow between M1 and DLS. Lastly, we developeda simple network model to understand which type of modificationin the structure of the M1-DLS network could reproduce theresults we obtained from experimental data.Results: We found that the timing of motor information in M1 andDLS changed from naïve to skilled stages of learning. In particular,the motor-information peaks in DLS were anticipated in time, whilethey occurred later in M1, in the skilled compared to the naïve condition.Crucially, using FIT, we measured that the directionality ofmotor-specific information transmission between M1 and DLSreversed with learning, with motor information flowing mainly fromM1 to DLS in the naïve and from DLS to M1 in the skilled condition.This reversal was hidden when measuring overall neural informationtransmission with DI, which bi-directionally increased between M1and DLS with learning. We could reproduce the above results in anetwork model by reversing the area that originated the motorspecificinformation, going from a cortical-origin during naive movementsto a striatal-origin during skilled movements.Conclusion: Our results provide evidence of a reversal in the areaoriginating, and then transmitting motor-specific information withinthe M1-DLS network as rats learned a reach-to-grasp task. Such findingprovide essential support to the idea that cortical and subcorticalregions have a leading role in controlling, respectively, naïve andautomatized movements.

U2 - 10.1016/j.clinph.2023.02.034

DO - 10.1016/j.clinph.2023.02.034

M3 - Conference abstract in journal

VL - 148

SP - e17

JO - CLIN NEUROPHYSIOL

JF - CLIN NEUROPHYSIOL

SN - 1388-2457

ER -