Large-scale all-optical dissection of motor cortex connectivity shows a segregated organization of mouse forelimb representations

Resta, Francesco; Montagni, Elena; Vito, Giuseppe de; Scaglione, Alessandro; Mascaro, Anna Letizia Allegra; Pavone, Francesco S.

doi:10.1016/j.celrep.2022.111627

Cited by 14 publications

(13 citation statements)

References 59 publications

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“…First, we confirmed that both RFA and CFA are involved in movement planning and execution and that the hierarchy flows from RFA to CFA as previously suggested [5][6][7][8][9][13][14][15]21,22,26,30,[34][35][36][37] . In detail, we demonstrate here that the RFA contained a much higher number of preparation neurons than the CFA and that the activity of movement neurons in the RFA preceded their counterparts in the CFA.…”

Section: Discussionsupporting

confidence: 86%

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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Section: Discussionsupporting

confidence: 86%

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Diester

Alyahyay

Kalweit

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…First, we confirmed that both RFA and CFA are involved in movement planning and execution and that the hierarchy flows from RFA to CFA as previously suggested 5-9, [13][14][15]21,22,26,30,[34][35][36][37] . In detail, we demonstrate here that the RFA contained a much higher number of preparation neurons than the CFA and that the activity of movement neurons in the RFA preceded their counterparts in the CFA.…”

Section: Discussionsupporting

confidence: 86%

Mechanisms of Premotor-Motor Cortex Interactions during Goal Directed Behavior

Alyahyay

Kalweit

et al. 2023

Preprint

View full text Add to dashboard Cite

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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“…Their rostro-caudal separation has led to the suggestion that RFA may be involved in motor planning, and CFA more involved in execution. However, microstimulation, recording, and manipulation studies found mixed results, suggesting preparation and execution are encoded in both regions, while others concluded CFA and RFA are distinct somatotopic representations of the forelimb 8,14,19,41 . One obstacle for synthesizing these results is the difference in methods used and specific circuits studied.…”

Section: Discussionmentioning

confidence: 99%

Topographical and cell type-specific connectivity of rostral and caudal forelimb corticospinal neuron populations

Carmona,

Thomas,

Smith

et al. 2023

Preprint

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SUMMARYCorticospinal neurons (CSNs) synapse directly on spinal neurons, a diverse group of neurons with unique structural and functional properties necessary for body movements. CSNs modulating forelimb behavior fractionate into caudal forelimb area (CFA) and rostral forelimb area (RFA) motor cortical populations. Despite their prominence, no studies have mapped the diversity of spinal cell types targeted by CSNs, let alone compare CFA and RFA populations. Here we use anatomical and RNA-sequencing methods to show that CSNs synapse onto a remarkably selective group of spinal cell types, favoring inhibitory populations that regulate motoneuron activity and gate sensory feedback. CFA and RFA CSNs target similar spinal cell types, with notable exceptions that suggest these populations differ in how they influence behavior. Finally, axon collaterals of CFA and RFA CSNs target similar brain regions yet receive surprisingly divergent inputs. These results detail the rules of CSN connectivity throughout the brain and spinal cord for two regions critical for forelimb behavior.

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Large-scale all-optical dissection of motor cortex connectivity shows a segregated organization of mouse forelimb representations

Cited by 14 publications

References 59 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

Topographical and cell type-specific connectivity of rostral and caudal forelimb corticospinal neuron populations

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