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.

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 Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons

2020 ◽  
Vol 21 (17) ◽  
pp. 6101
Author(s):  
Bruno Benedetti ◽  
Dominik Dannehl ◽  
Jan Maximilian Janssen ◽  
Corinna Corcelli ◽  
Sébastien Couillard-Després ◽  
...  
Keyword(s):  
Cell Growth ◽  
Motor Cortex ◽  
Postnatal Development ◽  
Primary Motor Cortex ◽  
Continuous Process ◽  
Network Activity ◽  
Functional Maturation ◽  
Sensory Cortices ◽  
Layer V ◽  
Functional Output

Rodent neocortical neurons undergo prominent postnatal development and maturation. The process is associated with structural and functional maturation of the axon initial segment (AIS), the site of action potential initiation. In this regard, cell size and optimal AIS length are interconnected. In sensory cortices, developmental onset of sensory input and consequent changes in network activity cause phasic AIS plasticity that can also control functional output. In non-sensory cortices, network input driving phasic events should be less prominent. We, therefore, explored the relationship between postnatal functional maturation and AIS maturation in principal neurons of the primary motor cortex layer V (M1LV), a non-sensory area of the rat brain. We hypothesized that a rather continuous process of AIS maturation and elongation would reflect cell growth, accompanied by progressive refinement of functional output properties. We found that, in the first two postnatal weeks, cell growth prompted substantial decline of neuronal input resistance, such that older neurons needed larger input current to reach rheobase and fire action potentials. In the same period, we observed the most prominent AIS elongation and significant maturation of functional output properties. Alternating phases of AIS plasticity did not occur, and changes in functional output properties were largely justified by AIS elongation. From the third postnatal week up to five months of age, cell growth, AIS elongation, and functional output maturation were marginal. Thus, AIS maturation in M1LV is a continuous process that attunes the functional output of pyramidal neurons and associates with early postnatal development to counterbalance increasing electrical leakage due to cell growth.

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 Two Populations of Layer V Pyramidal Cells of the Mouse Neocortex: Development and Sensitivity to Anesthetics

2005 ◽  
Vol 94 (5) ◽  
pp. 3357-3367 ◽  
Author(s):  
Elodie Christophe ◽  
Nathalie Doerflinger ◽  
Daniel J. Lavery ◽  
Zoltán Molnár ◽  
Serge Charpak ◽  
...  
Keyword(s):  
Action Potential ◽  
Calcium Binding ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Membrane Properties ◽  
Subcortical Structures ◽  
Contralateral Cortex ◽  
Layer V ◽  
Intrinsic Membrane Properties ◽  
Two Populations

Previous studies have shown that layer V pyramidal neurons projecting either to subcortical structures or the contralateral cortex undergo different morphological and electrophysiological patterns of development during the first three postnatal weeks. To isolate the determinants of this differential maturation, we analyzed the gene expression and intrinsic membrane properties of layer V pyramidal neurons projecting either to the superior colliculus (SC cells) or the contralateral cortex (CC cells) by combining whole cell recordings and single-cell RT-PCR in acute slices prepared from postnatal day (P) 5–7 or P21–30 old mice. Among the 24 genes tested, the calcium channel subunits α1B and α1C, the protease Nexin 1, and the calcium-binding protein calbindin were differentially expressed in adult SC and CC cells and the potassium channel subunit Kv4.3 was expressed preferentially in CC cells at both stages of development. Intrinsic membrane properties, including input resistance, amplitude of the hyperpolarization-activated current, and action potential threshold, differed quantitatively between the two populations as early as from the first postnatal week and persisted throughout adulthood. However, the two cell types had similar regular action potential firing behaviors at all developmental stages. Surprisingly, when we increased the duration of anesthesia with ketamine–xylazine or pentobarbital before decapitation, a proportion of mature SC cells, but not CC cells, fired bursts of action potentials. Together these results indicate that the two populations of layer V pyramidal neurons already start to differ during the first postnatal week and exhibit different firing capabilities after anesthesia.

Resting and Active Properties of Pyramidal Neurons in Subiculum and CA1 of Rat Hippocampus

2000 ◽  
Vol 84 (5) ◽  
pp. 2398-2408 ◽  
Author(s):  
Nathan P. Staff ◽  
Hae-Yoon Jung ◽  
Tara Thiagarajan ◽  
Michael Yao ◽  
Nelson Spruston
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Pyramidal Neurons ◽  
Current Injection ◽  
Synaptic Integration ◽  
Membrane Properties ◽  
Neuronal Membrane ◽  
Similar Action ◽  
Ca1 Neurons ◽  
Ca1 Pyramidal Neurons

Action potentials are the end product of synaptic integration, a process influenced by resting and active neuronal membrane properties. Diversity in these properties contributes to specialized mechanisms of synaptic integration and action potential firing, which are likely to be of functional significance within neural circuits. In the hippocampus, the majority of subicular pyramidal neurons fire high-frequency bursts of action potentials, whereas CA1 pyramidal neurons exhibit regular spiking behavior when subjected to direct somatic current injection. Using patch-clamp recordings from morphologically identified neurons in hippocampal slices, we analyzed and compared the resting and active membrane properties of pyramidal neurons in the subiculum and CA1 regions of the hippocampus. In response to direct somatic current injection, three subicular firing types were identified (regular spiking, weak bursting, and strong bursting), while all CA1 neurons were regular spiking. Within subiculum strong bursting neurons were found preferentially further away from the CA1 subregion. Input resistance ( R N), membrane time constant (τm), and depolarizing “sag” in response to hyperpolarizing current pulses were similar in all subicular neurons, while R N and τm were significantly larger in CA1 neurons. The first spike of all subicular neurons exhibited similar action potential properties; CA1 action potentials exhibited faster rising rates, greater amplitudes, and wider half-widths than subicular action potentials. Therefore both the resting and active properties of CA1 pyramidal neurons are distinct from those of subicular neurons, which form a related class of neurons, differing in their propensity to burst. We also found that both regular spiking subicular and CA1 neurons could be transformed into a burst firing mode by application of a low concentration of 4-aminopyridine, suggesting that in both hippocampal subfields, firing properties are regulated by a slowly inactivating, D-type potassium current. The ability of all subicular pyramidal neurons to burst strengthens the notion that they form a single neuronal class, sharing a burst generating mechanism that is stronger in some cells than others.

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.

Postnatal maturation of the hyperpolarization-activated cation current, Ih, in trigeminal sensory neurons

2011 ◽  
Vol 106 (4) ◽  
pp. 2045-2056 ◽  
Author(s):  
Hyun-jung Cho ◽  
John B. Furness ◽  
Ernest A. Jennings
Keyword(s):  
Action Potential ◽  
Postnatal Development ◽  
Sensory Neurons ◽  
Neuronal Excitability ◽  
Firing Frequency ◽  
Moderate Intensity ◽  
Hcn Channels ◽  
Action Potential Firing ◽  
Membrane Hyperpolarization ◽  
Postnatal Maturation

Hyperpolarization-activated inward currents ( Ih) contribute to neuronal excitability in sensory neurons. Four subtypes of hyperpolarization-activated cyclic nucleotide-gated (HCN) channels generate Ih, with different activation kinetics and cAMP sensitivities. The aim of the present study was to examine the postnatal development of Ih and HCN channel subunits in trigeminal ganglion (TG) neurons. Ih was investigated in acutely dissociated TG neurons from rats aged between postnatal day (P)1 and P35 with whole cell patch-clamp electrophysiology. In voltage-clamp studies, Ih was activated by a series of hyperpolarizing voltage steps from −40 mV to −120 mV in −10-mV increments. Tail currents from a common voltage step (−100 mV) were used to determine Ih voltage dependence. Ih activation was faster in older rats and occurred at more depolarized potentials; the half-maximal activation voltage ( V1/2) changed from −89.4 mV (P1) to −81.6 mV (P35). In current-clamp studies, blocking Ih with ZD7288 caused membrane hyperpolarization and increases in action potential half-duration at all postnatal ages examined. ZD7288 also reduced the action potential firing frequency in multiple-firing neurons. Western blot analysis of the TG detected immunoreactive bands corresponding to all HCN subtypes. HCN1 and HCN2 band density increased with postnatal age, whereas the low-intensity HCN3 and moderate-intensity HCN4 bands were not changed. This study suggests that functional Ih are activated in rat trigeminal sensory neurons from P1 during postnatal development, have an increasing role with age, and modify neuronal excitability.

COUP-TFI/Nr2f1 Orchestrates Intrinsic Neuronal Activity during Development of the Somatosensory Cortex

2020 ◽  
Vol 30 (11) ◽  
pp. 5667-5685 ◽  
Author(s):  
Isabel Del Pino ◽  
Chiara Tocco ◽  
Elia Magrinelli ◽  
Andrea Marcantoni ◽  
Celeste Ferraguto ◽  
...  
Keyword(s):  
Neuronal Excitability ◽  
Pyramidal Neurons ◽  
Time Windows ◽  
Critical Time ◽  
Network Activity ◽  
Intrinsic Excitability ◽  
Developmental Sequence ◽  
Genetic Mechanisms ◽  
Layer V ◽  
Voltage Gated Ion Channels

Abstract The formation of functional cortical maps in the cerebral cortex results from a timely regulated interaction between intrinsic genetic mechanisms and electrical activity. To understand how transcriptional regulation influences network activity and neuronal excitability within the neocortex, we used mice deficient for Nr2f1 (also known as COUP-TFI), a key determinant of primary somatosensory (S1) area specification during development. We found that the cortical loss of Nr2f1 impacts on spontaneous network activity and synchronization of S1 cortex at perinatal stages. In addition, we observed alterations in the intrinsic excitability and morphological features of layer V pyramidal neurons. Accordingly, we identified distinct voltage-gated ion channels regulated by Nr2f1 that might directly influence intrinsic bioelectrical properties during critical time windows of S1 cortex specification. Altogether, our data suggest a tight link between Nr2f1 and neuronal excitability in the developmental sequence that ultimately sculpts the emergence of cortical network activity within the immature neocortex.

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