Spike Firing and IPSPs in Layer V Pyramidal Neurons during Beta Oscillations in Rat Primary Motor Cortex (M1) In Vitro

AbstractDopamine (DA) plays a crucial role in the control of motor and higher cognitive functions such as learning, working memory and decision making. The primary motor cortex (M1), which is essential for motor control and the acquisition of motor skills, receives dopaminergic inputs in its superficial and deep layers from the midbrain. However, the precise action of DA and DA receptor subtypes on the cortical microcircuits of M1 remains poorly understood. The aim of this work was to investigate how DA, through the activation of D2 receptors (D2R), modulates the cellular and synaptic activity of M1 parvalbumin-expressing interneurons (PVINs) which are crucial to regulate the spike output of pyramidal neurons (PNs). By combining immunofluorescence, ex vivo electrophysiology, pharmacology and optogenetics approaches, we show that D2R activation increases neuronal excitability of PVINs and GABAergic synaptic transmission between PVINs and PNs in layer V of M1. Our data reveal a mechanism through which cortical DA modulates M1 microcircuitry and might participate in the acquisition of motor skills.Significance StatementPrimary motor cortex (M1), which is a region essential for motor control and the acquisition of motor skills, receives dopaminergic inputs from the midbrain. However, precise action of dopamine and its receptor subtypes on specific cell types in M1 remained poorly understood. Here, we demonstrate in M1 that dopamine D2 receptors (D2R) are present in parvalbumin interneurons (PVINs) and their activation increases the excitability of the PVINs, which are crucial to regulate the spike output of pyramidal neurons (PNs). Moreover the activation of the D2R facilitates the GABAergic synaptic transmission of those PVINs on layer V PNs. These results highlight how cortical dopamine modulates the functioning of M1 microcircuit which activity is disturbed in hypo- and hyperdopaminergic states.

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In vitro characterization of intrinsic properties and local synaptic inputs to pyramidal neurons in macaque primary motor cortex

European Journal of Neuroscience ◽

10.1111/ejn.14076 ◽

2018 ◽

Vol 48 (4) ◽

pp. 2071-2083 ◽

Cited By ~ 1

Author(s):

Wei Xu ◽

Stuart N. Baker

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Pyramidal Neurons ◽

Intrinsic Properties ◽

Synaptic Inputs ◽

In Vitro Characterization

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Refinement of Active and Passive Membrane Properties of Layer V Pyramidal Neurons in Rat Primary Motor Cortex During Postnatal Development

Frontiers in Molecular Neuroscience ◽

10.3389/fnmol.2021.754393 ◽

2021 ◽

Vol 14 ◽

Author(s):

Patricia Perez-García ◽

Ricardo Pardillo-Díaz ◽

Noelia Geribaldi-Doldán ◽

Ricardo Gómez-Oliva ◽

Samuel Domínguez-García ◽

...

Keyword(s):

Motor Cortex ◽

Postnatal Development ◽

Primary Motor Cortex ◽

Neuronal Excitability ◽

Pyramidal Neurons ◽

Membrane Properties ◽

Neuronal Membrane ◽

Maturation Process ◽

Postnatal Maturation ◽

Layer V

Achieving the distinctive complex behaviors of adult mammals requires the development of a great variety of specialized neural circuits. Although the development of these circuits begins during the embryonic stage, they remain immature at birth, requiring a postnatal maturation process to achieve these complex tasks. Understanding how the neuronal membrane properties and circuits change during development is the first step to understand their transition into efficient ones. Thus, using whole cell patch clamp recordings, we have studied the changes in the electrophysiological properties of layer V pyramidal neurons of the rat primary motor cortex during postnatal development. Among all the parameters studied, only the voltage threshold was established at birth and, although some of the changes occurred mainly during the second postnatal week, other properties such as membrane potential, capacitance, duration of the post-hyperpolarization phase or the maximum firing rate were not defined until the beginning of adulthood. Those modifications lead to a decrease in neuronal excitability and to an increase in the working range in young adult neurons, allowing more sensitive and accurate responses. This maturation process, that involves an increase in neuronal size and changes in ionic conductances, seems to be influenced by the neuronal type and by the task that neurons perform as inferred from the comparison with other pyramidal and motor neuron populations.

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Dendritic changes of the pyramidal neurons in layer V of sensory-motor cortex of the rat brain during the postresuscitation period

Resuscitation ◽

10.1016/s0300-9572(97)00048-8 ◽

1997 ◽

Vol 35 (2) ◽

pp. 157-164 ◽

Cited By ~ 17

Author(s):

Victor A Akulinin ◽

Sergey S Stepanov ◽

Valeriy V Semchenko ◽

Pavel V Belichenko

Keyword(s):

Motor Cortex ◽

Rat Brain ◽

Pyramidal Neurons ◽

Postresuscitation Period ◽

Sensory Motor ◽

Layer V

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Do neurons from the primary motor cortex grow in response to signals from the developing spinal cord in vitro?

Hamdan Medical Journal ◽

10.7707/hmj.537 ◽

2015 ◽

Author(s):

F Alhumaid ◽

S Almutairi ◽

P Roach ◽

HR Fuller ◽

MA Gates

Keyword(s):

Spinal Cord ◽

Motor Cortex ◽

Primary Motor Cortex ◽

Developing Spinal Cord

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Plasticity of the Cortical Motor System

Journal of Human Kinetics ◽

10.2478/v10078-008-0014-x ◽

2008 ◽

Vol 20 (1) ◽

pp. 5-22 ◽

Cited By ~ 3

Author(s):

Bogdan Sadowski

Keyword(s):

Motor Cortex ◽

Motor System ◽

Primary Motor Cortex ◽

Pyramidal Neurons ◽

Pyramidal Cells ◽

Long Term Potentiation ◽

Skill Learning ◽

Dynamic Features ◽

Cortical Motor

Plasticity of the Cortical Motor SystemThe involvement of brain plastic mechanisms in the control of motor functions under normal and pathological conditions is described. These mechanisms are based on a similar principle as the neuronal models of neuronal plasticity - long-term potentiation (LTP), and long-term depression (LTD). In the motor cortex, LTP-like phenomena play a role in strengthening synaptic connections between pyramidal neurons. LTD is important for the elimination of unnecessary inputs to the cortex. The dynamic features of the primary motor cortex activity depend on particular neuronal interconnectivity within this area. The pyramidal cells send horizontal collaterals to adjacent subregions of the primary motor cortex, and so can either excite or inhibit remote pyramidal cells. These connections can expand or shrink depending on actual physiological demands, and play a role in skill learning.

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Otx1 promotes basal dendritic growth and regulates intrinsic electrophysiological and synaptic properties of layer V pyramidal neurons in mouse motor cortex

Neuroscience ◽

10.1016/j.neuroscience.2014.11.019 ◽

2015 ◽

Vol 285 ◽

pp. 139-154 ◽

Cited By ~ 11

Author(s):

Y.-F. Zhang ◽

L.-X. Liu ◽

H.-T. Cao ◽

L. Ou ◽

J. Qu ◽

...

Keyword(s):

Motor Cortex ◽

Dendritic Growth ◽

Pyramidal Neurons ◽

Layer V

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NMDA Receptor-Mediated Motor Cortex Plasticity After 20 Hz Transcranial Alternating Current Stimulation

Cerebral Cortex ◽

10.1093/cercor/bhy160 ◽

2018 ◽

Vol 29 (7) ◽

pp. 2924-2931 ◽

Cited By ~ 26

Author(s):

M Wischnewski ◽

M Engelhardt ◽

M A Salehinejad ◽

D J L G Schutter ◽

M -F Kuo ◽

...

Keyword(s):

Motor Cortex ◽

Primary Motor Cortex ◽

Cortical Excitability ◽

Alternating Current ◽

Beta Oscillations ◽

Human Motor Cortex ◽

After Effects ◽

Transcranial Alternating Current Stimulation ◽

Human Motor ◽

Motor Cortex Plasticity

Abstract Transcranial alternating current stimulation (tACS) has been shown to modulate neural oscillations and excitability levels in the primary motor cortex (M1). These effects can last for more than an hour and an involvement of N-methyl-d-aspartate receptor (NMDAR) mediated synaptic plasticity has been suggested. However, to date the cortical mechanisms underlying tACS after-effects have not been explored. Here, we applied 20 Hz beta tACS to M1 while participants received either the NMDAR antagonist dextromethorphan or a placebo and the effects on cortical beta oscillations and excitability were explored. When a placebo medication was administered, beta tACS was found to increase cortical excitability and beta oscillations for at least 60 min, whereas when dextromethorphan was administered, these effects were completely abolished. These results provide the first direct evidence that tACS can induce NMDAR-mediated plasticity in the motor cortex, which contributes to our understanding of tACS-induced influences on human motor cortex physiology.

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Pre-movement changes in sensorimotor beta oscillations predict motor adaptation drive

10.1101/2020.01.13.903807 ◽

2020 ◽

Cited By ~ 2

Author(s):

Henry T Darch ◽

Nadia L Cerminara ◽

Iain D Gilchrist ◽

Richard Apps

Keyword(s):

Reaction Time ◽

Motor Cortex ◽

Primary Motor Cortex ◽

Visuomotor Adaptation ◽

Beta Oscillations ◽

Scalp Eeg ◽

Eeg Recordings ◽

Beta Frequency ◽

Late Adaptation ◽

Adaptation Task

AbstractBeta frequency oscillations in scalp electroencephalography (EEG) recordings over the primary motor cortex have been associated with the preparation and execution of voluntary movements. Here, we test whether changes in beta frequency are related to the preparation of adapted movements in human, and whether such effects generalise to other species (cat). Eleven healthy adult humans performed a joystick visuomotor adaptation task. Beta (15-25Hz) scalp EEG signals recorded over the motor cortex during a pre-movement preparatory phase were, on average, significantly reduced in amplitude during early adaptation trials compared to baseline or late adaptation trials (p=0.01). The changes in beta were not related to measurements of reaction time or duration of the reach. We also recorded LFP activity within the primary motor cortex of three cats during a prism visuomotor adaptation task. Analysis of these signals revealed similar reductions in motor cortical LFP beta frequencies during early adaptation. This effect was also present when controlling for any influence of the reaction time and reaching duration. Overall, the results are consistent with a reduction in pre-movement beta oscillations predicting an increase in adaptive drive in upcoming task performance when motor errors are largest in magnitude and the rate of adaptation is greatest.

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