scholarly journals Synergistic plasticity of intrinsic conductance and electrical coupling restores synchrony in an intact motor network

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Brian J Lane ◽  
Pranit Samarth ◽  
Joseph L Ransdell ◽  
Satish S Nair ◽  
David J Schulz
Keyword(s):  
Motor Neurons ◽  
Electrical Coupling ◽  
High Threshold ◽  
Cardiac Ganglion ◽  
Physiological Regulation ◽  
Blocking High ◽  
Motor Network ◽  
Ionic Conductances ◽  
Network Output ◽  
Coupling Conductance

Motor neurons of the crustacean cardiac ganglion generate virtually identical, synchronized output despite the fact that each neuron uses distinct conductance magnitudes. As a result of this variability, manipulations that target ionic conductances have distinct effects on neurons within the same ganglion, disrupting synchronized motor neuron output that is necessary for proper cardiac function. We hypothesized that robustness in network output is accomplished via plasticity that counters such destabilizing influences. By blocking high-threshold K+ conductances in motor neurons within the ongoing cardiac network, we discovered that compensation both resynchronized the network and helped restore excitability. Using model findings to guide experimentation, we determined that compensatory increases of both GA and electrical coupling restored function in the network. This is one of the first direct demonstrations of the physiological regulation of coupling conductance in a compensatory context, and of synergistic plasticity across cell- and network-level mechanisms in the restoration of output.

scholarly journals Dopamine maintains network synchrony via direct modulation of gap junctions in the crustacean cardiac ganglion

2018 ◽  
Author(s):  
Brian J Lane ◽  
Daniel R Kick ◽  
David K Wilson ◽  
Satish S Nair ◽  
David J Schulz
Keyword(s):  
Motor Neurons ◽  
Channel Blocker ◽  
Electrical Coupling ◽  
Membrane Conductance ◽  
Large Cell ◽  
Protective Role ◽  
Cardiac Ganglion ◽  
Junctional Conductance ◽  
Network Synchrony ◽  
Gap Junctional

AbstractAbstract The Large Cell (LC) motor neurons of the crab (C. borealis) cardiac ganglion have variable membrane conductance magnitudes even within the same individual, yet produce identical synchronized activity in the intact network. In our previous study (Lane et al., 2016) we blocked a subset of K+ conductances across LCs, resulting in loss of synchronous activity. In this study, we hypothesized that this same variability of conductances could make LCs vulnerable to desynchronization during neuromodulation. We exposed the LCs to serotonin (5HT) and dopamine (DA) while recording simultaneously from multiple LCs. Both amines had distinct excitatory effects on LC output, but only 5HT caused desynchronized output. We further determined that DA rapidly increased gap junctional conductance. Co-application of both amines induced 5HT-like output, but waveforms remained synchronized. Furthermore, DA prevented desynchronization induced by the K+ channel blocker tetraethylammonium (TEA), suggesting that dopaminergic modulation of electrical coupling plays a protective role in maintaining network synchrony.

scholarly journals Dopamine maintains network synchrony via direct modulation of gap junctions in the crustacean cardiac ganglion

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Brian J Lane ◽  
Daniel R Kick ◽  
David K Wilson ◽  
Satish S Nair ◽  
David J Schulz
Keyword(s):  
Motor Neurons ◽  
Electrical Coupling ◽  
Membrane Conductance ◽  
Large Cell ◽  
Protective Role ◽  
K Channel ◽  
Cardiac Ganglion ◽  
Junctional Conductance ◽  
Network Synchrony ◽  
Gap Junctional

The Large Cell (LC) motor neurons of the crab cardiac ganglion have variable membrane conductance magnitudes even within the same individual, yet produce identical synchronized activity in the intact network. In a previous study we blocked a subset of K+ conductances across LCs, resulting in loss of synchronous activity (Lane et al., 2016). In this study, we hypothesized that this same variability of conductances makes LCs vulnerable to desynchronization during neuromodulation. We exposed the LCs to serotonin (5HT) and dopamine (DA) while recording simultaneously from multiple LCs. Both amines had distinct excitatory effects on LC output, but only 5HT caused desynchronized output. We further determined that DA rapidly increased gap junctional conductance. Co-application of both amines induced 5HT-like output, but waveforms remained synchronized. Furthermore, DA prevented desynchronization induced by the K+ channel blocker tetraethylammonium (TEA), suggesting that dopaminergic modulation of electrical coupling plays a protective role in maintaining network synchrony.

Whole body withdrawal circuit and its involvement in the behavioral hierarchy of the mollusk Clione limacina

1996 ◽  
Vol 75 (2) ◽  
pp. 529-537 ◽  
Author(s):  
T. P. Norekian ◽  
R. A. Satterlie
Keyword(s):  
Feeding Behavior ◽  
Motor Neurons ◽  
Prey Capture ◽  
The Body ◽  
Whole Body ◽  
High Threshold ◽  
Behavioral Repertoire ◽  
Withdrawal Behavior ◽  
Cerebral Neurons ◽  
Clione Limacina

1. The behavioral repertoire of the holoplanktonic pteropod mollusk Clione limacina includes a few well-defined behaviors organized in a priority sequence. Whole body withdrawal takes precedence over slow swimming behavior, whereas feeding behavior is dominant over withdrawal. In this study a group of neurons is described in the pleural ganglia, which controls whole body withdrawal behavior in Clione. Each pleural withdrawal (Pl-W) neuron has a high threshold for spike generation and is capable of inducing whole body withdrawal in a semi-intact preparation: retraction of the body-tail, wings, and head. Each Pl-W neuron projects axons into the main central nerves and innervates all major regions of the body. 2. Stimulation of Pl-W neurons produces inhibitory inputs to swim motor neurons that terminate swimming activity in the preparation. In turn, Pl-W neurons receive inhibitory inputs from the cerebral neurons involved in the control of feeding behavior in Clione, neurons underlying extrusion of specialized prey capture appendages. Thus it appears that specific inhibitory connections between motor centers can explain the dominance of withdrawal behavior over slow swimming and feeding over withdrawal in Clione.

Electrically coupled pacemaker neurons respond differently to same physiological inputs and neurotransmitters

1984 ◽  
Vol 51 (6) ◽  
pp. 1362-1374 ◽  
Author(s):  
E. Marder ◽  
J. S. Eisen
Keyword(s):  
Motor Neurons ◽  
Slow Wave ◽  
Lucifer Yellow ◽  
Electrical Coupling ◽  
Excitatory Postsynaptic Potential ◽  
Panulirus Interruptus ◽  
Bursting Neuron ◽  
Postsynaptic Potential ◽  
Pyloric Dilator ◽  
Muscarinic Cholinergic

The two pyloric dilator (PD) motor neurons and the single anterior burster (AB) interneuron are electrically coupled and together comprise the pacemaker for the pyloric central pattern generator of the stomatogastric ganglion of the lobster, Panulirus interruptus. Previous work (31) has shown that the AB neuron is an endogenously bursting neuron, while the PD neuron is a conditional burster. In this paper the effects of physiological inputs and neurotransmitters on isolated PD neurons and AB neurons were studied using the lucifer yellow photoinactivation technique (33). Stimulation of the inferior ventricular nerve (IVN) fibers at high frequencies elicits a triphasic response in AB and PD neurons: a rapid excitatory postsynaptic potential (EPSP) followed by a slow inhibitory postsynaptic potential (IPSP), followed by an enhancement of the pacemaker slow-wave depolarizations. Photoinactivation experiments indicate that the enhancement of the slow wave is due primarily to actions of the IVN fibers on the PD neurons but not on the AB neuron. Bath-applied dopamine dramatically alters the motor output of the pyloric system. Photoinactivation experiments show that 10(-4) M dopamine increases the amplitude and frequency of the slow-wave depolarizations recorded in the AB neurons but hyperpolarizes and inhibits the PD neurons. Bath-applied serotonin increases the frequency and amplitude of the slow-wave depolarizations in the AB neuron but has no effect on PD neurons. Pilocarpine, a muscarinic cholinergic agonist, stimulates slow-wave depolarization production in both PD neurons and the AB neuron, but the waveform and frequency of the slow waves elicited are quite different. These results show that although the electrically coupled PD and AB neurons always depolarize synchronously and act together as the pacemaker for the pyloric system, they respond differently to a neuronal input and to several putative neuromodulators. Thus, despite electrical coupling sufficient to ensure synchronous activity, the PD and AB neurons can be modulated independently.

scholarly journals Reactive oxygen species regulate activity-dependent neuronal plasticity in Drosophila

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Matthew CW Oswald ◽  
Paul S Brooks ◽  
Maarten F Zwart ◽  
Amrita Mukherjee ◽  
Ryan JH West ◽  
...  
Keyword(s):  
Reactive Oxygen Species ◽  
Neuronal Plasticity ◽  
Second Messengers ◽  
Reactive Oxygen ◽  
Structural Plasticity ◽  
Oxygen Species ◽  
Redox Sensor ◽  
Motor Network ◽  
Network Output ◽  
Activity Dependent

Reactive oxygen species (ROS) have been extensively studied as damaging agents associated with ageing and neurodegenerative conditions. Their role in the nervous system under non-pathological conditions has remained poorly understood. Working with the Drosophila larval locomotor network, we show that in neurons ROS act as obligate signals required for neuronal activity-dependent structural plasticity, of both pre- and postsynaptic terminals. ROS signaling is also necessary for maintaining evoked synaptic transmission at the neuromuscular junction, and for activity-regulated homeostatic adjustment of motor network output, as measured by larval crawling behavior. We identified the highly conserved Parkinson’s disease-linked protein DJ-1β as a redox sensor in neurons where it regulates structural plasticity, in part via modulation of the PTEN-PI3Kinase pathway. This study provides a new conceptual framework of neuronal ROS as second messengers required for neuronal plasticity and for network tuning, whose dysregulation in the ageing brain and under neurodegenerative conditions may contribute to synaptic dysfunction.

scholarly journals Differential Modulation of Synaptic Strength and Timing Regulate Synaptic Efficacy in a Motor Network

2011 ◽  
Vol 105 (1) ◽  
pp. 293-304 ◽  
Author(s):  
Bruce R. Johnson ◽  
Jessica M. Brown ◽  
Mark D. Kvarta ◽  
Jay Y. J. Lu ◽  
Lauren R. Schneider ◽  
...  
Keyword(s):  
Synaptic Input ◽  
Synaptic Strength ◽  
Neuronal Firing ◽  
Cycle Period ◽  
Cycle Frequency ◽  
Pyloric Network ◽  
Motor Network ◽  
Pyloric Dilator ◽  
Network Output ◽  
Firing Properties

Neuromodulators modify network output by altering neuronal firing properties and synaptic strength at multiple sites; however, the functional importance of each site is often unclear. We determined the importance of monoamine modulation of a single synapse for regulation of network cycle frequency in the oscillatory pyloric network of the lobster. The pacemaker kernel of the pyloric network receives only one chemical synaptic feedback, an inhibitory synapse from the lateral pyloric (LP) neuron to the pyloric dilator (PD) neurons, which can limit cycle frequency. We measured the effects of dopamine (DA), octopamine (Oct), and serotonin (5HT) on the strength of the LP→PD synapse and the ability of the modified synapse to regulate pyloric cycle frequency. DA and Oct strengthened, whereas 5HT weakened, LP→PD inhibition. Surprisingly, the DA-strengthened LP→PD synapse lost its ability to slow the pyloric oscillations, whereas the 5HT-weakened LP→PD synapse gained a greater influence on the oscillations. These results are explained by monoamine modulation of factors that determine the firing phase of the LP neuron in each cycle. DA acts via multiple mechanisms to phase-advance the LP neuron into the pacemaker's refractory period, where the strengthened synapse has little effect. In contrast, 5HT phase-delays LP activity into a region of greater pacemaker sensitivity to LP synaptic input. Only Oct enhanced LP regulation of cycle period simply by enhancing LP→PD synaptic strength. These results show that modulation of the strength and timing of a synaptic input can differentially affect the synapse's efficacy in the network.

Modulation of Jellyfish Potassium Channels by External Potassium Ions

1999 ◽  
Vol 82 (4) ◽  
pp. 1728-1739 ◽  
Author(s):  
Nikita G. Grigoriev ◽  
J. David Spafford ◽  
Andrew N. Spencer
Keyword(s):  
Potassium Channels ◽  
Motor Neurons ◽  
Fruit Fly ◽  
Site Directed Mutagenesis ◽  
High Threshold ◽  
Extracellular Potassium ◽  
Potassium Ions ◽  
Polyorchis Penicillatus ◽  
State Dependent ◽  
Inactivation Mechanism

The amplitude of an A-like potassium current ( I Kfast) in identified cultured motor neurons isolated from the jellyfish Polyorchis penicillatus was found to be strongly modulated by extracellular potassium ([K+]out). When expressed in Xenopus oocytes, two jellyfish Shaker-like genes, jShak1 and jShak2, coding for potassium channels, exhibited similar modulation by [K+]out over a range of concentrations from 0 to 100 mM. jShak2-encoded channels also showed a decreased rate of inactivation and an increased rate of recovery from inactivation at high [K+]out. Using site-directed mutagenesis we show that inactivation of jShak2 can be ascribed to an unusual combination of a weak “implicit” N-type inactivation mechanism and a strong, fast, potassium-sensitive C-type mechanism. Interaction between the two forms of inactivation is responsible for the potassium dependence of cumulative inactivation. Inactivation of jShak1 was determined primarily by a strong “ball and chain” mechanism similar to fruit fly Shaker channels. Experiments using fast perfusion of outside-out patches with jShak2 channels were used to establish that the effects of [K+]out on the peak current amplitude and inactivation were due to processes occurring at either different sites located at the external channel mouth with different retention times for potassium ions, or at the same site(s) where retention time is determined by state-dependent conformations of the channel protein. The possible physiological implications of potassium sensitivity of high-threshold potassium A-like currents is discussed.

scholarly journals Electrophysiological Properties of Inferior Olive Neurons: A Compartmental Model

1999 ◽  
Vol 82 (2) ◽  
pp. 804-817 ◽  
Author(s):  
Nicolas Schweighofer ◽  
Kenji Doya ◽  
Mitsuo Kawato
Keyword(s):  
Calcium Current ◽  
Potassium Current ◽  
Inferior Olive ◽  
Sodium Current ◽  
Electrical Coupling ◽  
Biophysical Model ◽  
Delayed Rectifier ◽  
High Threshold ◽  
Electrophysiological Properties

As a step in exploring the functions of the inferior olive, we constructed a biophysical model of the olivary neurons to examine their unique electrophysiological properties. The model consists of two compartments to represent the known distribution of ionic currents across the cell membrane, as well as the dendritic location of the gap junctions and synaptic inputs. The somatic compartment includes a low-threshold calcium current ( I Ca_l), an anomalous inward rectifier current ( I h), a sodium current ( I Na), and a delayed rectifier potassium current ( I K_dr). The dendritic compartment contains a high-threshold calcium current ( I Ca_h), a calcium-dependent potassium current ( I K_Ca), and a current flowing into other cells through electrical coupling ( I c). First, kinetic parameters for these currents were set according to previously reported experimental data. Next, the remaining free parameters were determined to account for both static and spiking properties of single olivary neurons in vitro. We then performed a series of simulated pharmacological experiments using bifurcation analysis and extensive two-parameter searches. Consistent with previous studies, we quantitatively demonstrated the major role of I Ca_l in spiking excitability. In addition, I h had an important modulatory role in the spike generation and period of oscillations, as previously suggested by Bal and McCormick. Finally, we investigated the role of electrical coupling in two coupled spiking cells. Depending on the coupling strength, the hyperpolarization level, and the I Ca_l and I hmodulation, the coupled cells had four different synchronization modes: the cells could be in-phase, phase-shifted, or anti-phase or could exhibit a complex desynchronized spiking mode. Hence these simulation results support the counterintuitive hypothesis that electrical coupling can desynchronize coupled inferior olive cells.

scholarly journals Differential neuropeptide modulation of premotor and motor neurons in the lobster cardiac ganglion

2020 ◽  
Vol 124 (4) ◽  
pp. 1241-1256
Author(s):  
Emily R. Oleisky ◽  
Meredith E. Stanhope ◽  
J. Joe Hull ◽  
Andrew E. Christie ◽  
Patsy S. Dickinson
Keyword(s):  
Motor Neurons ◽  
Homarus Americanus ◽  
Cardiac Ganglion ◽  
Differential Distribution

Premotor and motor neurons of the Homarus americanus cardiac ganglion (CG) are normally electrically and chemically coupled, and generate rhythmic bursting that drives cardiac contractions; we show that they can establish independent bursting patterns when physically decoupled by a ligature. The neuropeptide myosuppressin modulates different aspects of the bursting pattern in these neuron types to determine the overall modulation of the intact CG. Differential distribution of myosuppressin receptors may underlie the observed responses to myosuppressin.

scholarly journals Action-potential broadening and endogenously sustained bursting are substrates of command ability in a feeding neuron of Pleurobranchaea

1980 ◽  
Vol 43 (3) ◽  
pp. 669-685 ◽  
Author(s):  
R. Gillette ◽  
M. U. Gillette ◽  
W. J. Davis
Keyword(s):  
Action Potential ◽  
Action Potentials ◽  
Motor Output ◽  
Buccal Ganglion ◽  
Short Pulses ◽  
Motor Network ◽  
Single Axon ◽  
Network Output ◽  
Bilateral Pair ◽  
Potential Activity

1. The ventral white cells (VWC's) of the buccal ganglion of Pleurobranchaea, so named for their position and color, are a bilateral pair of neuron somata. Each sends a single axon out its contralateral stomatogastric nerve and has a dendritic field originating close to the soma. 2. The vwcs exhibit spontaneous episodes of prolonged depolarization (duration 1--4 min) accompanied by repetitive action-potential activity and separated by regular intervals of 3--30 min. Such prolonged burst episodes can be triggered by short pulses of depolarizing current. During the repetitive activity of the spontaneous bursts or that driven by imposed depolarization, the action potentials progressively broaden to 5--16 times their initial duration. 3. During spontaneous bursting or activity driven by imposed depolarization, the cyclic motor output of the feeding network is initiated or accelerated with a latency corresponding with the development of appreciable VWC spike broadening. When broadening of antidromic VWC spikes is suppressed by imposed hyperpolarization of the soma, the frequency of feeding cycles is significantly lower than when broadened spikes are allowed to develop. When trains of spikes are driven by depolarizing current, the motor output of the feeding network is not initiated until the VWC spikes have broadened to a repeatable "threshold" duration, regardless of the intensity of the depolarizing current. 4. The endogenous production of prolonged burst episodes, triggered by depolarizing current pulses, and progressive spike broadening can be demonstrated in the surgically isolated VWC soma. 5. The paired VWCs are strongly electrically coupled and display highly synchronous activity. They receive synaptic inputs from many previously identified interneurons of the feeding network and are thus reciprocally coupled within the network. 6. These results demonstrate that the capacity of this neuron to generate broadened action potentials during repetitive activity confers the ability to command coordinated motor-network output. The appropriate repetitive activity can be produced endogenously in the form of prolonged bursts of spikes.

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