Movement-specific signaling is differentially distributed across motor cortex layer 5 projection neuron classes

Currie, Stephen; Ammer, Julian; Premchand, Brian; Dacre, Joshua; Wu, Yi; Eleftheriou, Constantinos; Colligan, Matt; Clarke, Thomas; Mitchell, Leah; Faisal, A. Aldo; Hennig, Matthias; Duguid, Ian

doi:10.1016/j.celrep.2022.110801

Cited by 20 publications

(18 citation statements)

References 82 publications

(166 reference statements)

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“…Second, with a phototagging approach, we revealed that the neuronal subpopulation from RFA to CFA contributes equally to planning and execution of movements. To go beyond this experimentally possible dissection, we developed an innovative machine learning-based tool (NeuRL) which allows the generation of predictions about neuronal subpopulations that are otherwise hard to assess due to their invariant responses to movement 40 . This novel machine-learning algorithm enables the functional dissociation of spatiotemporally-concurrent neuronal ensembles.…”

Section: Discussionmentioning

confidence: 99%

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Alyahyay

Kalweit

et al. 2023

Preprint

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Deciphering the neural code underlying goal-directed behavior is a long-term mission in neuroscience. Neurons exhibiting preparation and movement-related activity are intermingled in the premotor and motor cortices, thus concealing the neural code of planned movements. We employed a combination of electrophysiology, pathway-specific optogenetics, phototagging, and inverse reinforcement learning (RL) to elucidate the role of defined neuronal subpopulations in the rat rostral and caudal forelimb areas (RFA and CFA), which correspond to the premotor and motor cortical areas. The inverse RL enabled the functional dissection of spatially intermingled neuronal subpopulations, complementing our pathway-specific optogenetic manipulations and unveiling differential functions of the preparation and movement subpopulations projecting from RFA to CFA. Our results show that the projecting preparation subpopulation suppresses movements, whereas the projecting movement subpopulation promotes actions. We found the influence of RFA on CFA to be adaptable, with the projection either inhibiting or exciting neurons in the superficial and deep CFA layers, depending on context and task phase. These complex interactions between RFA and CFA likely involve the differential recruitment of inhibitory interneurons in the CFA, which is supported by our electron microscopy analysis of the connectivity between these regions. We provide here unprecedented mechanistic insights into how the premotor and primary motor cortices are functionally and structurally interlinked with the potential to advance neuroprosthetics.

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Section: Discussionmentioning

confidence: 99%

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Alyahyay

Kalweit

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…Second, with a phototagging approach, we revealed that the neuronal subpopulation from RFA to CFA contributes equally to planning and execution of movements. To go beyond this experimentally possible dissection, we developed an innovative machine learning-based tool (NeuRL) which allows the generation of predictions about neuronal subpopulations that are otherwise hard to assess due to their invariant responses to movement 40 . This novel machinelearning algorithm enables the functional dissociation of spatiotemporally-concurrent neuronal ensembles.…”

Section: Discussionmentioning

confidence: 99%

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Diester

Alyahyay

Kalweit

et al. 2023

Preprint

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Deciphering the neural code underlying goal-directed behavior is a long-term mission in neuroscience1,2. Neurons exhibiting preparation and movement-related activity are intermingled in the premotor and motor cortices3,4, thus concealing the neural code of planned movements. We employed a combination of electrophysiology, pathway-specific optogenetics, phototagging, and inverse reinforcement learning (RL) to elucidate the role of defined neuronal subpopulations in the rat rostral and caudal forelimb areas (RFA and CFA), which correspond to the premotor and motor cortical areas. The inverse RL enabled the functional dissection of spatially intermingled neuronal subpopulations, complementing our pathway-specific optogenetic manipulations and unveiling differential functions of the preparation and movement subpopulations projecting from RFA to CFA. Our results show that the projecting preparation subpopulation suppresses movements, whereas the projecting movement subpopulation promotes actions. We found the influence of RFA on CFA to be adaptable, with the projection either inhibiting or exciting neurons in the superficial and deep CFA layers, depending on context and task phase. These complex interactions between RFA and CFA likely involve the differential recruitment of inhibitory interneurons in the CFA, which is supported by our electron microscopy analysis of the connectivity between these regions. We provide here unprecedented mechanistic insights into how the premotor and primary motor cortices are functionally and structurally interlinked with the potential to advance neuroprosthetics.

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“…Considering the top-down organization of M1 (40, 41), where layer II/III neurons provide output to neurons located in lower layers, the role of D2+ neurons in motor performance may be of greater significance. Moreover, recent studies show that layer II/III neurons exhibit more prevalent direction-selective activity than layer V neurons (42, 43) and encode previous reach outcomes independent of kinematics and reward (44), which suggests that they play a superior role in motor skill learning and subsequent movement execution.…”

Section: Discussionmentioning

confidence: 99%

Dopamine receptor-expressing neurons are differently distributed throughout layers of the motor cortex to control dexterity

Cieslak,

Drabik,

Gugula

et al. 2023

Preprint

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The motor cortex comprises the primary descending circuits for flexible control of voluntary movements and is critically involved in motor skill learning. Motor skill learning is impaired in patients with Parkinson’s disease, but the precise mechanisms of motor control and skill learning are still not well understood. Here we have used transgenic mice, electrophysiology,in situhybridization and neural tract-tracing methods to target genetically defined cell types expressing D1 and D2 dopamine receptors (D1+ and D2+, respectively) in the motor cortex. We observed that D1+ and D2+ neurons are organized in highly segregated, non-overlapping populations. Moreover, based onex vivopatch-clamp recordings, we showed that D1+ and D2+ cells have distinct morphological and electrophysiological properties. Finally, we observed that chemogenetic inhibition of D2+, but not D1+ neurons, disrupts skilled forelimb reaching in adult mice. Overall, these results demonstrate that dopamine receptor-expressing cells in the motor cortex are highly segregated and play a specialized role in manual dexterity.

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Movement-specific signaling is differentially distributed across motor cortex layer 5 projection neuron classes

Cited by 20 publications

References 82 publications

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Dopamine receptor-expressing neurons are differently distributed throughout layers of the motor cortex to control dexterity

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