Converging sensory and motor cortical inputs onto the same striatal neurons: An in vivo intracellular investigation. 2020

Stéphane Charpier, and Morgane Pidoux, and Séverine Mahon
Institut du Cerveau et de la Moelle épinière, ICM, INSERM UMRS 1127, CNRS UMR 7225, Hôpital Pitié-Salpêtrière, Paris, France.

The striatum is involved in the completion and optimization of sensorimotor tasks. In rodents, its dorsolateral part receives converging glutamatergic corticostriatal (CS) inputs from whisker-related primary somatosensory (S1) and motor (M1) cortical areas, which are interconnected at the cortical level. Although it has been demonstrated that the medium-spiny neurons (MSNs) from the dorsolateral striatum process sensory information from the whiskers via the S1 CS pathway, the functional impact of the corresponding M1 CS inputs onto the same striatal neurons remained unknown. Here, by combining in vivo S1 electrocorticogram with intracellular recordings from somatosensory MSNs in the rat, we first confirmed the heterogeneity of striatal responsiveness to whisker stimuli, encompassing MSNs responding exclusively by subthreshold synaptic depolarizations, MSNs exhibiting sub- and suprathreshold responses over successive stimulations, and non-responding cells. All recorded MSNs also exhibited clear-cut monosynaptic depolarizing potentials in response to electrical stimulations of the corresponding ipsilateral M1 cortex, which were efficient to fire striatal cells. Since M1-evoked responses in MSNs could result from the intra-cortical recruitment of S1 CS neurons, we performed intracellular recordings of S1 pyramidal neurons and compared their firing latency following M1 stimuli to the latency of striatal synaptic responses. We found that the onset of M1-evoked synaptic responses in MSNs significantly preceded the firing of S1 neurons, demonstrating a direct synaptic excitation of MSNs by M1. However, the firing of MSNs seemed to require the combined excitatory effects of S1 and M1 CS inputs. This study directly demonstrates that the same somatosensory MSNs can process excitatory synaptic inputs from two functionally-related sensory and motor cortical regions converging into the same striatal sector. The effectiveness of these convergent cortical inputs in eliciting action potentials in MSNs may represent a key mechanism of striatum-related sensorimotor behaviors.

UI MeSH Term Description Entries
D008297 Male Males
D004558 Electric Stimulation Use of electric potential or currents to elicit biological responses. Stimulation, Electric,Electrical Stimulation,Electric Stimulations,Electrical Stimulations,Stimulation, Electrical,Stimulations, Electric,Stimulations, Electrical
D004567 Electrodes, Implanted Surgically placed electric conductors through which ELECTRIC STIMULATION is delivered to or electrical activity is recorded from a specific point inside the body. Implantable Electrodes,Implantable Stimulation Electrodes,Implanted Electrodes,Implanted Stimulation Electrodes,Electrode, Implantable,Electrode, Implantable Stimulation,Electrode, Implanted,Electrode, Implanted Stimulation,Electrodes, Implantable,Electrodes, Implantable Stimulation,Electrodes, Implanted Stimulation,Implantable Electrode,Implantable Stimulation Electrode,Implanted Electrode,Implanted Stimulation Electrode,Stimulation Electrode, Implantable,Stimulation Electrode, Implanted,Stimulation Electrodes, Implantable,Stimulation Electrodes, Implanted
D000818 Animals Unicellular or multicellular, heterotrophic organisms, that have sensation and the power of voluntary movement. Under the older five kingdom paradigm, Animalia was one of the kingdoms. Under the modern three domain model, Animalia represents one of the many groups in the domain EUKARYOTA. Animal,Metazoa,Animalia
D013003 Somatosensory Cortex Area of the parietal lobe concerned with receiving sensations such as movement, pain, pressure, position, temperature, touch, and vibration. It lies posterior to the central sulcus. Brodmann Area 1,Brodmann Area 2,Brodmann Area 3,Brodmann Areas 1, 2, 3,Brodmann Areas 1, 2, and 3,Brodmann Areas 3, 1, 2,Brodmann Areas 3, 1, and 2,Brodmann's Area 1,Brodmann's Area 2,Brodmann's Area 3,Brodmann's Areas 1, 2, and 3,Brodmann's Areas 3, 1, and 2,Parietal-Opercular Cortex,Primary Somesthetic Area,S1 Cortex,S2 Cortex,SII Cortex,Anterior Parietal Cortex,Gyrus Postcentralis,Post Central Gyrus,Postcentral Gyrus,Primary Somatic Sensory Area,Primary Somatosensory Area,Primary Somatosensory Areas,Primary Somatosensory Cortex,SI Cortex,Second Somatic Sensory Area,Secondary Sensory Cortex,Secondary Somatosensory Area,Secondary Somatosensory Cortex,Area 1, Brodmann,Area 1, Brodmann's,Area 2, Brodmann,Area 2, Brodmann's,Area 3, Brodmann,Area 3, Brodmann's,Area, Primary Somatosensory,Area, Primary Somesthetic,Area, Secondary Somatosensory,Areas, Primary Somatosensory,Brodmanns Area 1,Brodmanns Area 2,Brodmanns Area 3,Cortex, Anterior Parietal,Cortex, Parietal-Opercular,Cortex, Primary Somatosensory,Cortex, S1,Cortex, S2,Cortex, SI,Cortex, SII,Cortex, Secondary Sensory,Cortex, Secondary Somatosensory,Cortex, Somatosensory,Gyrus, Post Central,Gyrus, Postcentral,Parietal Cortex, Anterior,Parietal Opercular Cortex,Parietal-Opercular Cortices,Primary Somatosensory Cortices,Primary Somesthetic Areas,S1 Cortices,S2 Cortices,SII Cortices,Secondary Somatosensory Areas,Sensory Cortex, Secondary,Somatosensory Area, Primary,Somatosensory Area, Secondary,Somatosensory Areas, Primary,Somatosensory Cortex, Primary,Somatosensory Cortex, Secondary,Somesthetic Area, Primary,Somesthetic Areas, Primary
D017207 Rats, Sprague-Dawley A strain of albino rat used widely for experimental purposes because of its calmness and ease of handling. It was developed by the Sprague-Dawley Animal Company. Holtzman Rat,Rats, Holtzman,Sprague-Dawley Rat,Rats, Sprague Dawley,Holtzman Rats,Rat, Holtzman,Rat, Sprague-Dawley,Sprague Dawley Rat,Sprague Dawley Rats,Sprague-Dawley Rats
D051381 Rats The common name for the genus Rattus. Rattus,Rats, Laboratory,Rats, Norway,Rattus norvegicus,Laboratory Rat,Laboratory Rats,Norway Rat,Norway Rats,Rat,Rat, Laboratory,Rat, Norway,norvegicus, Rattus
D055366 Synaptic Potentials The voltages across pre- or post-SYNAPTIC MEMBRANES. Postsynaptic Current,Postsynaptic Potentials,Synaptic Potential,Current, Postsynaptic,Currents, Postsynaptic,Postsynaptic Currents,Postsynaptic Potential,Potential, Postsynaptic,Potential, Synaptic,Potentials, Postsynaptic
D017966 Pyramidal Cells Projection neurons in the CEREBRAL CORTEX and the HIPPOCAMPUS. Pyramidal cells have a pyramid-shaped soma with the apex and an apical dendrite pointed toward the pial surface and other dendrites and an axon emerging from the base. The axons may have local collaterals but also project outside their cortical region. Pyramidal Neurons,Cell, Pyramidal,Cells, Pyramidal,Neuron, Pyramidal,Neurons, Pyramidal,Pyramidal Cell,Pyramidal Neuron

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