scholarly journals Dopamine D2 receptors modulate intrinsic properties and synaptic transmission of parvalbumin interneurons in the mouse primary motor cortex

2019 ◽  
Author(s):  
Jérémy Cousineau ◽  
Léa Lescouzères ◽  
Anne Taupignon ◽  
Lorena Delgado-Zabalza ◽  
Emmanuel Valjent ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Synaptic Transmission ◽  
Motor Skills ◽  
Primary Motor Cortex ◽  
Pyramidal Neurons ◽  
D2 Receptors ◽  
Receptor Subtypes ◽  
Parvalbumin Interneurons ◽  
Layer V ◽  
Gabaergic Synaptic Transmission

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.

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

PLoS ONE ◽  
2014 ◽  
Vol 9 (1) ◽  
pp. e85109 ◽  
Author(s):  
Michael G. Lacey ◽  
Gerard Gooding-Williams ◽  
Emma J. Prokic ◽  
Naoki Yamawaki ◽  
Stephen D. Hall ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Primary Motor Cortex ◽  
Pyramidal Neurons ◽  
Beta Oscillations ◽  
Layer V ◽  
Spike Firing

scholarly journals Enhancing motor learning by increasing stability of newly formed dendritic spines in motor cortex

2021 ◽  
Author(s):  
Eddy Albarran ◽  
Aram Raissi ◽  
Omar Jáidar ◽  
Carla J. Shatz ◽  
Jun B. Ding
Keyword(s):  
Motor Cortex ◽  
Motor Learning ◽  
Motor Skills ◽  
Motor Performance ◽  
Primary Motor Cortex ◽  
Pyramidal Neurons ◽  
Spine Density ◽  
Immunoglobulin Receptor ◽  
Reaching Task ◽  
Spine Dynamics

SUMMARYDendritic spine dynamics of Layer 5 Pyramidal neurons (L5PNs) are thought to be physical substrates for motor learning and memory of motor skills and altered spine dynamics are frequently correlated with poor motor performance. Here we describe an exception to this rule by studying mice lacking Paired immunoglobulin receptor B (PirB−/−). Using chronic two-photon imaging of primary motor cortex (M1) of PirB−/−;Thy1-YFP-H mice, we found a significant increase in the survival of spines on apical dendritic tufts of L5PNs, as well as increased spine formation rates and spine density. Surprisingly and contrary to expectations, adult PirB−/− mice learn a skilled reaching task more rapidly compared to wild type (WT) littermate controls. Conditional excision of PirB from forebrain pyramidal neurons in adult mice replicated these results. Furthermore, chronic imaging of L5PN dendrites throughout the learning period revealed that the stabilization of learning-induced newly formed spines is significantly elevated in PirB−/− mice. The degree of survival of newly formed spines in M1 yielded the strongest correlation with task performance, suggesting that this increased spine stability is advantageous and can translate into enhanced acquisition and maintenance of motor skills. Notably, inhibiting PirB function acutely in M1 of adult WT mice throughout training increases the survival of spines formed during early training and enhances motor learning. These results suggest that increasing the stability of newly formed spines is sufficient to improve long-lasting learning and motor performance and demonstrate that there are limits on motor learning that can be lifted by manipulating PirB, even in adulthood.

scholarly journals Dopamine D2-Like Receptors Modulate Intrinsic Properties and Synaptic Transmission of Parvalbumin Interneurons in the Mouse Primary Motor Cortex

eNeuro ◽  
2020 ◽  
Vol 7 (3) ◽  
pp. ENEURO.0081-20.2020 ◽  
Author(s):  
Jérémy Cousineau ◽  
Léa Lescouzères ◽  
Anne Taupignon ◽  
Lorena Delgado-Zabalza ◽  
Emmanuel Valjent ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Synaptic Transmission ◽  
Primary Motor Cortex ◽  
Intrinsic Properties ◽  
Dopamine D2 ◽  
Parvalbumin Interneurons

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

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.

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

Resuscitation ◽  
1997 ◽  
Vol 35 (2) ◽  
pp. 157-164 ◽  
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

scholarly journals Mu-opioids suppress GABAergic synaptic transmission onto orbitofrontal cortex pyramidal neurons with subregional selectivity

2020 ◽  
Author(s):  
Benjamin K. Lau ◽  
Brittany P. Ambrose ◽  
Catherine S. Thomas ◽  
Min Qiao ◽  
Stephanie L. Borgland
Keyword(s):  
Synaptic Transmission ◽  
Opioid Receptor ◽  
Orbitofrontal Cortex ◽  
Pyramidal Neurons ◽  
Mu Opioid Receptor ◽  
Mu Opioid ◽  
Inhibitory Synaptic Transmission ◽  
Receptor Coupling ◽  
Mu Opioids ◽  
Gabaergic Synaptic Transmission

AbstractThe orbitofrontal cortex (OFC) plays a critical role in evaluating outcomes in a changing environment. Administering opioids to the OFC can alter the hedonic reaction to food rewards and increase their consumption in a subregion specific manner. However, it is unknown how mu-opioid signalling influences synaptic transmission in the OFC. Thus, we investigated the cellular actions of mu-opioids within distinct subregions of the OFC. Using in-vitro patch clamp electrophysiology in brain slices containing the OFC, we found that the mu-opioid agonist, DAMGO produced a concentration-dependant inhibition of GABAergic synaptic transmission onto medial OFC (mOFC), but not lateral OFC (lOFC) neurons. This effect was mediated by presynaptic mu-opioid receptor activation of local parvalbumin (PV+)-expressing interneurons. The DAMGO-induced suppression of inhibition was long-lasting and not reversed upon washout of DAMGO, or by application of the mu-opioid receptor antagonist, CTAP, suggesting an inhibitory long-term depression (iLTD) induced by an exogenous mu-opioid. We show that LTD at inhibitory synapses is dependent on downstream cAMP/PKA signaling, which differs between the mOFC and lOFC. Finally, we demonstrate that endogenous opioid release triggered via moderate physiological stimulation can induce LTD. Taken together, these results suggest that presynaptic mu-opioid stimulation of local PV+ interneurons induces a long-lasting suppression of GABAergic synaptic transmission, which depends on subregional differences in mu-opioid receptor coupling to the downstream cAMP/PKA intracellular cascade. These findings provide mechanistic insight into the opposing functional effects produced by mu-opioids within the OFC.Significance StatementConsidering that both the OFC and the opioid system regulate reward, motivation, and food intake; understanding the role of opioid signaling within the OFC is fundamental for a mechanistic understanding of the sequelae for several psychiatric disorders. This study makes several novel observations. First, mu-opioids induce a long-lasting suppression of inhibitory synaptic transmission onto OFC pyramidal neurons in a regionally selective manner. Secondly, mu-opioids recruit PV+ inputs to suppress inhibitory synaptic transmission in the mOFC. Thirdly, the regional selectivity of mu-opioid action of endogenous opioids is due to the efficacy of mu-opioid receptor coupling to the downstream cAMP/PKA intracellular cascades. These experiments are the first to reveal a cellular mechanism of opioid action within the OFC.

scholarly journals Plasticity of the Cortical Motor System

2008 ◽  
Vol 20 (1) ◽  
pp. 5-22 ◽  
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.

scholarly journals Neural Substrates of Practice Structure That Support Future Off-Line Learning

2009 ◽  
Vol 102 (4) ◽  
pp. 2462-2476 ◽  
Author(s):  
Nicholas F. Wymbs ◽  
Scott T. Grafton
Keyword(s):  
Motor Cortex ◽  
Motor Skills ◽  
Primary Motor Cortex ◽  
Neural Substrates ◽  
Skill Learning ◽  
Opposite Pattern ◽  
Practice Schedule ◽  
Random Schedule ◽  
Subcortical Regions ◽  
Equivalent Motor

Off-line learning is facilitated when motor skills are acquired under a random practice schedule and retention suffers when a similar set of motor skills are practiced under a blocked schedule. The current study identified the neural correlates of a random training schedule while participants learned a set of four-element finger sequences using their nondominant hand during functional magnetic resonance imaging. A go/no go task was used to separately probe brain areas supporting sequence preparation and production. By the end of training, the random practice schedule, relative to the block schedule, recruited a broad premotor–parietal network as well as sensorimotor and subcortical regions during both preparation and production trials, despite equivalent motor performance. Longitudinal analysis demonstrated that preparation-related activity under a random schedule remained stable or increased over time. The blocked schedule showed the opposite pattern. Across individual subjects, successful skill retention was correlated with greater activity at the end of training in the ipsilateral left motor cortex, for both preparation and production. This is consistent with recent evidence that attributes off-line learning to training-related processing within primary motor cortex. These results reflect the importance of an overlooked aspect of motor skill learning. Specifically, how trials are organized during training—with a random schedule—provides an effective basis for the formation of enduring motor memories, through enhanced engagement of core regions involved in the active preparation and implementation of motor programs.

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