Pharmacological dissection of pyloric network of the lobster stomatogastric ganglion using picrotoxin

1980 ◽  
Vol 44 (6) ◽  
pp. 1089-1101 ◽  
Author(s):  
M. Bidaut

1. Picrotoxin (PTX) (10(-7)-10(-6) M) completely blocked most inhibitory synapses in the pyloric pattern generator of the lobster (Panulirus interruptus) stomatogastric ganglion. The sensitivity of synapses from most classes of identified neurons was examined. Blockade was at least partly reversible with prolonged washing. 2. The synapses from pyloric dilator (PD) neurons were the only inhibitory synapses that picrotoxin failed to block completely. 3. A correlation is derived that brief, fast-rise inhibitory postsynaptic potentials (IPSPs) are picrotoxin sensitive, whereas a slow rounded component of IPSPs from PD neurons is not picrotoxin sensitive. 4. Picrotoxin caused specific changes in the pattern of the motor rhythm produced by the 16-cell pyloric network. This sheds some light on the functional role of particular synapses in the pyloric generator. 5. The endogenously bursting neurons (PD and anterior burster (AB)), which drive the pyloric rhythm, kept a similar burst rate. 6. Under picrotoxin, the pyloric "follower" neurons all moved to later phase relative to the "driver" group. Some normally antagonistic cells, related by reciprocal inhibitor connections, became in-phase. These and other pattern changes could be related to blockade of particular synapses. 7. The pyloric rhythm was still quite recognizable under picrotoxin despite the drastically altered circuitry of the synaptic network. This supports the idea that periodic inhibition from the PD driver neurons plays a primary role in creating the pyloric pattern.

2003 ◽  
Vol 90 (2) ◽  
pp. 631-643 ◽  
Author(s):  
Bruce R. Johnson ◽  
Peter Kloppenburg ◽  
Ronald M. Harris-Warrick

We examined the dopamine (DA) modulation of calcium currents (ICa) that could contribute to the plasticity of the pyloric network in the lobster stomatogastric ganglion. Pyloric somata were voltage-clamped under conditions designed to block voltage-gated Na+, K+, and H currents. Depolarizing steps from –60 mV generated voltage-dependent, inward currents that appeared to originate in electrotonically distal, imperfectly clamped regions of the cell. These currents were blocked by Cd2+ and enhanced by Ba2+ but unaffected by Ni2+. Dopamine enhanced the peak ICa in the pyloric constrictor (PY), lateral pyloric (LP), and inferior cardiac (IC) neurons and reduced peak ICa in the ventricular dilator (VD), pyloric dilator (PD), and anterior burster (AB) neurons. All of these effects, except for the AB, are consistent with DA's excitation or inhibition of firing in the pyloric neurons. Enhancement of ICa in PY and LP neurons and reduction of ICa in VD and PD neurons are also consistent with DA-induced synaptic strength changes via modulation of presynaptic ICa. However, the reduction of ICa in AB suggests that DA's enhancement of AB transmitter release is not directly mediated through presynaptic ICa. ICa in PY and PD neurons was more sensitive to nifedipine block than in AB neurons. In addition, nifedipine blocked DA's effects on ICa in the PY and PD neurons but not in the AB neuron. Thus the contribution of specific calcium channel subtypes carrying the total ICa may vary between pyloric neuron classes, and DA may act on different calcium channel subtypes in the different pyloric neurons.


2016 ◽  
Vol 116 (2) ◽  
pp. 619-628 ◽  
Author(s):  
Yanqing Wang ◽  
Brian D. Burrell

Endocannabinoids can elicit persistent depression of excitatory and inhibitory synapses, reducing or enhancing (disinhibiting) neural circuit output, respectively. In this study, we examined whether differences in Cl−gradients can regulate which synapses undergo endocannabinoid-mediated synaptic depression vs. disinhibition using the well-characterized central nervous system (CNS) of the medicinal leech, Hirudo verbana. Exogenous application of endocannabinoids or capsaicin elicits potentiation of pressure (P) cell synapses and depression of both polymodal (Npoly) and mechanical (Nmech) nociceptive synapses. In P synapses, blocking Cl−export prevented endocannabinoid-mediated potentiation, consistent with a disinhibition process that has been indicated by previous experiments. In Nmechneurons, which are depolarized by GABA due to an elevated Cl−equilibrium potentials (ECl), endocannabinoid-mediated depression was prevented by blocking Cl−import, indicating that this decrease in synaptic signaling was due to depression of excitatory GABAergic input (disexcitation). Npolyneurons are also depolarized by GABA, but endocannabinoids elicit depression in these synapses directly and were only weakly affected by disruption of Cl−import. Consequently, the primary role of elevated EClmay be to protect Npolysynapses from disinhibition. All forms of endocannabinoid-mediated plasticity required activation of transient potential receptor vanilloid (TRPV) channels. Endocannabinoid/TRPV-dependent synaptic plasticity could also be elicited by distinct patterns of afferent stimulation with low-frequency stimulation (LFS) eliciting endocannabinoid-mediated depression of Npolysynapses and high-frequency stimulus (HFS) eliciting endocannabinoid-mediated potentiation of P synapses and depression of Nmechsynapses. These findings demonstrate a critical role of differences in Cl−gradients between neurons in determining the sign, potentiation vs. depression, of synaptic modulation under normal physiological conditions.


2003 ◽  
Vol 90 (4) ◽  
pp. 2720-2730 ◽  
Author(s):  
Jason A. Luther ◽  
Alice A. Robie ◽  
John Yarotsky ◽  
Christopher Reina ◽  
Eve Marder ◽  
...  

The pyloric rhythm of the stomatogastric ganglion of the crab, Cancer borealis, slows or stops when descending modulatory inputs are acutely removed. However, the rhythm spontaneously resumes after one or more days in the absence of neuromodulatory input. We recorded continuously for days to characterize quantitatively this recovery process. Activity bouts lasting 40–900 s began several hours after removal of neuromodulatory input and were followed by stable rhythm recovery after 1–4 days. Bout duration was not related to the intervals (0.3–800 min) between bouts. During an individual bout, the frequency rapidly increased and then decreased more slowly. Photoablation of back-filled neuromodulatory terminals in the stomatogastric ganglion (STG) neuropil had no effect on activity bouts or recovery, suggesting that these processes are intrinsic to the STG neuronal network. After removal of neuromodulatory input, the phase relationships of the components of the triphasic pyloric rhythm were altered, and then over time the phase relationships moved toward their control values. Although at low pyloric rhythm frequency the phase relationships among pyloric network neurons depended on frequency, the changes in frequency during recovery did not completely account for the change in phase seen after rhythm recovery. We suggest that activity bouts represent underlying mechanisms controlling the restructuring of the pyloric network to allow resumption of an appropriate output after removal of neuromodulatory input.


1998 ◽  
Vol 79 (4) ◽  
pp. 2063-2069 ◽  
Author(s):  
Amir Ayali ◽  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

Ayali, Amir, Bruce R. Johnson, and Ronald M. Harris-Warrick. Dopamine modulates graded and spike-evoked synaptic inhibition independently at single synapses in pyloric network of lobster. J. Neurophysiol. 79: 2063–2069, 1998. Bath application of dopamine (DA) modifies the rhythmic motor pattern generated by the pyloric network in the stomatogastric ganglion of the spiny lobster, Panulirus interruptus. Synaptic transmission between network members is an important target of DA action. All pyloric neurons employ both graded transmitter release and action-potential–mediated synaptic inhibition. DA was previously shown to alter the graded synaptic strength of every pyloric synapse. In this study, we compared DA's effects on action-potential–mediated and graded synaptic inhibition at output synapses of the lateral pyloric (LP) neuron. At each synapse the postsynaptic cell tested was isolated from other descending and pyloric synaptic inputs. DA caused a reduction in the size of the LP spike-evoked inhibitory postsynaptic potentials (IPSPs) in the pyloric dilator (PD) neuron. The change in IPSP size was significantly and linearly correlated with DA-induced reduction in the input resistance of the postsynaptic PD neuron. In contrast, graded inhibition, tested in the same preparations after superfusing the stomatogastric ganglion (STG) with tetrodotoxin (TTX), was consistently enhanced by DA. DA shifted the amplitude of spike-evoked IPSPs in the same direction as the alteration of the postsynaptic cell input resistance at two additional synapses tested: DA weakened the LP spike-mediated inhibition of the ventricular dilator (VD) and reduced the VD input resistance, while strengthening the LP → pyloric constrictor (PY) synapse and increasing PY input resistance. As previously reported, graded inhibition was enhanced at these two LP output synapses. We conclude that DA can differentially modulate the spike-evoked and graded components of synapses between members of a central pattern generator network. At the synapses we studied, actions on the presynaptic cell predominate in the modulation of graded transmission, whereas effects on postsynaptic cells predominate in the regulation of spike-evoked IPSPs.


2001 ◽  
Vol 86 (6) ◽  
pp. 2957-2965 ◽  
Author(s):  
Jack H. Peck ◽  
Stan T. Nakanishi ◽  
Ross Yaple ◽  
Ronald M. Harris-Warrick

The pyloric network of the stomatogastric ganglion of the lobster Panulirus interruptus is a model system used to understand how motor networks change their output to produce a variety of behaviors. The transient potassium current ( I A) shapes the activity of individual pyloric neurons by affecting their rate of postinhibitory rebound and spike frequency. We used two electrode voltage clamp to study the modulatory effects of dopamine (DA), octopamine (OCT), and serotonin (5-HT) on I A in the anterior burster (AB), inferior cardiac (IC), and ventricular dilator (VD) neurons of the pyloric circuit. DA significantly reduced I A in the AB and IC neurons and shifted their voltages of activation ( V act) and inactivation ( V inact) in a depolarized direction. These ionic changes contribute to the depolarization and increased firing rate of the AB and IC neurons produced by DA. Likewise, 5-HT significantly reduced I A and shifted V inact in the depolarized direction in the IC neuron, consistent with 5-HT's enhancement of IC firing. None of the amines evoked significant changes in I A in the VD neuron, suggesting that other currents mediate the amine effects on this neuron.


1997 ◽  
Vol 78 (6) ◽  
pp. 3210-3221 ◽  
Author(s):  
Bruce R. Johnson ◽  
Ronald M. Harris-Warrick

Johnson, Bruce R. and Ronald M. Harris-Warrick. Amine modulation of glutamate responses from pyloric motor neurons in lobster stomatogastric ganglion. J. Neurophysiol. 78: 3210–3221, 1997. The amines dopamine (DA), serotonin (5-HT), and octopamine (Oct) each elicit a distinctive motor pattern from a quiescent pyloric network in the lobster stomatogastric ganglion (STG). We previously have demonstrated that these amines alter the synaptic strength at multiple, distributed sites within the pyloric network that could contribute to the amine-induced motor patterns. Here, we examined the postsynaptic contribution to these changes in synaptic strength by determining how the amines modify responses of pyloric motor neurons to glutamate (Glu), one of the network transmitters, applied iontophoretically into the STG neuropil. Dopamine reduced the Glu responses of the pyloric dilator (PD), ventricular dilator (VD), and inferior cardiac (IC) neurons and enhanced the Glu responses of the lateral pyloric (LP) and pyloric constrictor (PY) neurons. The only effect of 5-HT was to reduce the Glu response of the VD neuron. Oct enhanced the Glu responses of the LP and PY neurons but did not affect the PD, VD, and IC responses. We also examined amine effects on the depolarizing responses to iontophoresed acetylcholine (ACh) in the PD and VD and found that they paralleled the amine effects on Glu responses in these neurons. This suggests that amine modulation of PD and VD responses to Glu and ACh may be explained by general changes in the ionic conductance of these neurons. We compare our results with our earlier work describing amine effects on synaptic strength and input resistance to show that amines act at both pre- and postsynaptic sites to modify graded synaptic transmission in the pyloric network.


1984 ◽  
Vol 112 (1) ◽  
pp. 147-167 ◽  
Author(s):  
E. Marder

Understanding fully the operation of a neural circuit requires both a description of the individual neurones within the circuit as well as the characterization of their synaptic interactions. These aims are often particularly difficult to achieve in neural circuits containing electrically-coupled neurones. In recent years two new methods (photoinactivation after Lucifer Yellow injection and intracellular injection of pronase) have been employed to delete selectively single neurones or small groups of neurones from neural circuits. These techniques have been successfully used in the analysis of circuits containing electrically-coupled neurones. In several systems new roles for electrical synapses in the integrative function of neural circuits have been proposed. In the nervous systems of both the leech and lobster it is now thought that synaptic interactions previously thought to be direct are mediated through an interposed, electrically-coupled neurone. In the pyloric system of the stomatogastric ganglion of the lobster, Panulirus interruptus, the Lucifer Yellow photoinactivation technique has permitted a separate analysis of the properties of several electrically-coupled neurones previously thought quite similar. We now know that the Anterior Burster (AB) interneurone and the Pyloric Dilator (PD) motor neurones, which together act as the pacemaker ensemble for the pyloric network, differ in many regards including their intrinsic ability to generate bursting pacemaker potentials, their neurotransmitters, their sensitivity to some neurotransmitters and hormones, the neural inputs they receive and their pattern of synaptic connectivity. These results will be discussed in the context of the role of electrical coupling in neuronal integration.


1992 ◽  
Vol 163 (1) ◽  
pp. 209-230
Author(s):  
E. Rezer ◽  
M. Moulins

In the lobster Jasus lalandii, 14 neurones of the stomatogastric ganglion (STG) are organized in a network that produces rhythmic pyloric outputs. In vitro experiments have shown that the STG neurones receive, via the stomatogastric nerve (stn), neuromodulatory inputs that influence the expression of the bursting properties of the neurones and the ability of the network to produce its rhythmic output. In contrast to these in vitro observations, in vivo transection of the stn does not abolish the pyloric rhythm. Rhythmic output can be recorded by electromyography immediately after stn transection and for up to 2 years afterwards. We have shown that, under these experimental conditions, the STG appears to be isolated from any neuronal input that might account for the maintenance of the rhythmic output. Experiments carried out in the 2 days after stn transection showed that an in vitro preparation of the isolated STG was unable to produce any rhythmic output, but blood serum added to the system could restore the pyloric output. These results suggest strongly that the pyloric network receives neural and humoral modulatory influences in parallel and that each type of influence alone is able to maintain the bursting capability of the pyloric neurones.


2003 ◽  
Vol 89 (4) ◽  
pp. 1902-1909 ◽  
Author(s):  
Y. Zhang ◽  
J. N. MacLean ◽  
W. F. An ◽  
C. C. Lanning ◽  
R. M. Harris-Warrick

The transient potassium current ( I A) plays an important role in shaping the firing properties of pyloric neurons in the stomatogastric ganglion (STG) of the spiny lobster, Panulirus interruptus. The shal gene encodes I A in pyloric neurons. However, when we over-expressed the lobster Shal protein by shal RNA injection into the pyloric dilator (PD) neuron, the increased I A had somewhat different properties from the endogenous I A. The recently cloned K-channel interacting proteins (KChIPs) can modify vertebrate Kv4 channels in cloned cell lines. When we co-expressed hKChIP1 with lobster shal in Xenopusoocytes or lobster PD neurons, they produced A-currents resembling the endogenous I A in PD neurons; compared with currents evoked by shal alone, their voltage for half inactivation was depolarized, their kinetics of inactivation were slowed, and their recovery from inactivation was accelerated. We also co-expressed shal in PD neurons with lobster frequenin, which encodes a protein belonging to the same EF-hand family of Ca2+ sensing proteins as hKChIP. Frequenin also restored most of properties of the shal-evoked currents to those of the endogenous A-currents, but the time course of recovery from inactivation was not corrected. These results suggest that lobster shal proteins normally interact with proteins in the KChIP/frequenin family to produce the transient potassium current in pyloric neurons.


2006 ◽  
Vol 95 (3) ◽  
pp. 1762-1770 ◽  
Author(s):  
Vatsala Thirumalai ◽  
Astrid A. Prinz ◽  
Christian D. Johnson ◽  
Eve Marder

The neuropeptide, red pigment concentrating hormone (RPCH), strengthened the inhibitory synapse from the lateral pyloric (LP) neuron to the pyloric dilator (PD) neurons in the pyloric network of the stomatogastric ganglion (STG) of the lobster, Homarus americanus. RPCH produced several-fold increases in the amplitude of both action potential–mediated and non–impulse-mediated transmission that persisted for as long as the peptide remained present. Because the LP to PD synapse is the only feedback to the pacemaker kernel of the pyloric network, which consists of the electrically coupled two PD neurons and the anterior burster (AB) neuron, it might have been expected that strengthening the LP to PD synapse would increase the period of the pyloric rhythm. However, the period of the pyloric rhythm increased only transiently in RPCH, and a transient increase in cycle period was observed even when the LP neuron was hyperpolarized. Phase response curves were measured using the dynamic clamp to create artificial inhibitory inputs of variable strength and duration to the PD neurons. Synaptic conductance values seen in normal saline were ineffective at changing the pyloric period throughout the pyloric cycle. Conductances similar to those seen in 10−6 M RPCH also did not evoke phase resets at phases when the LP neuron is typically active. Thus the dramatic effects of RPCH on synaptic strength have little role in modulation of the period of the pyloric rhythm under normal operating conditions but may help to stabilize the rhythm when the cycle period is too slow or too fast.


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