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Peptide Neuromodulation of Synaptic Dynamics in an Oscillatory Network

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Peptide Neuromodulation of Synaptic Dynamics in an Oscillatory Network The Journal of Neuroscience, September 28, 2011 • 31(39):13991–14004 • 13991 Behavioral/Systems/Cognitive Peptide Neuromodulation of Synaptic Dynamics in an Oscillatory Network Shunbing Zhao,1 Amir Farzad Sheibanie,2 Myongkeun Oh,3 Pascale Rabbah,1 and Farzan Nadim1,3 1Department of Biological Sciences, Rutgers University, Newark, New Jersey 07102, 2Department of Neuroscience, University of Medicine and Dentistry of New Jersey, Newark, New Jersey 07102, and 3Department of Mathematical Sciences, New Jersey Institute of Technology, Newark, New Jersey 07102 Although neuromodulation of synapses is extensively documented, its consequences in the context of network oscillations are not well known. We examine the modulation of synaptic strength and short-term dynamics in the crab pyloric network by the neuropeptide proctolin. Pyloric oscillations are driven by a pacemaker group which receives feedback through the inhibitory synapse from the lateral pyloric (LP) to pyloric dilator (PD) neurons. We show that proctolin modulates the spike-mediated and graded components of the LP to PDsynapse.Proctolinenhancesthegradedcomponentandunmasksasurprisingheterogeneityinitsdynamicswherethereisdepression or facilitation depending on the amplitude of the voltage waveform of the presynaptic LP neuron. The spike-mediated component is influenced by the baseline membrane potential and is also enhanced by proctolin at all baseline potentials. In addition to direct modu- lation of this synapse, proctolin also changes the shape and amplitude of the presynaptic voltage waveform which additionally enhances synaptic output during ongoing activity. During ongoing oscillations, proctolin reduces the variability of cycle period but only when the LP to PD synapse is functionally intact. Using the dynamic clamp technique we find that the reduction in variability is a direct conse- quence of modulation of the LP to PD synapse. These results demonstrate that neuromodulation of synapses involves complex and interacting influences that target different synaptic components and dynamics as well as the presynaptic voltage waveform. At the network level, modulation of feedback inhibition can result in reduction of variability and enhancement of stable oscillatory output. Introduction and examine how these modulatory actions shape the combined Short-term synaptic dynamics such as facilitation and depression synapse in the context of network activity. have been shown to play an important role in shaping the output The crustacean pyloric oscillations are generated in the stoma- of neuronal networks (Abbott et al., 1997; Tsodyks et al., 2000; togastric nervous system (STNS) by a pacemaker group consist- Manor and Nadim, 2001; Zucker and Regehr, 2002; Deeg, 2009). ing of the gap-junction-coupled anterior burster (AB), pyloric Synaptic plasticity also ensues from modification of synaptic dilator (PD), and (in crabs) lateral posterior gastric (LPG) neu- strength by neuromodulators (Ayali et al., 1998; Sakurai and rons that burst in synchrony. The sole chemical feedback from Katz, 2003). Neuromodulation of the short-term dynamics, re- the pyloric follower neurons to the pacemakers is the synapse ported in many systems (Bristol et al., 2001; Baimoukhametova et from the lateral pyloric (LP) to the PD neurons, according a key al., 2004; Cartling, 2004; Sakurai and Katz, 2009), is considered a role for this synapse in the regulation of pyloric oscillations form of metaplasticity and can have complex network conse- (Manor et al., 1997; Mamiya et al., 2003; Weaver and Hooper, quences (Fischer et al., 1997b); yet, little is known about neuro- 2003). A variety of neuromodulators in the STNS modify the modulation of synaptic dynamics in the context of network intrinsic properties of individual pyloric neurons (Harris- oscillations. Synapses often involve distinct components that act Warrick et al., 1998; Swensen and Marder, 2000) and the strength at different time scales or involve spike-mediated, graded or asyn- and dynamics of synapses among these neurons (Johnson et al., chronous release (Warzecha et al., 2003; Otsu et al., 2004; Ivanov 2005, 2011). We demonstrate the ability of the modulatory neu- and Calabrese, 2006b). We explore how neuromodulation mod- ropeptide proctolin to alter the strength and unmask novel ifies distinct components of a synapse in an oscillatory network dynamics in the LP to PD synapse. Proctolin is released by pro- jection neurons in the STNS (Nusbaum et al., 2001) and activates a voltage-gated ionic current in several pyloric neurons (Swensen and Marder, 2001). However, the effect of proctolin on the pylo- Received July 15, 2011; revised Aug. 8, 2011; accepted Aug. 9, 2011. ric synapses has not been previously examined. The LP to PD Author contributions: S.Z. and F.N. designed research; S.Z., A.F.S., P.R., and F.N. performed research; S.Z., M.O., P.R., and F.N. analyzed data; S.Z. and F.N. wrote the paper. synapse has both spike-mediated and graded components, as This work was supported by National Institutes of Health Grant MH-60605. A.F.S. was supported by NINDS Grant found in other systems (Angstadt and Calabrese, 1991; Pan et al., 1T32NS051157. We thank Jorge Golowasch, Isabel Soffer, and the anonymous reviewers for their comments on the 2001; Warzecha et al., 2003; Ivanov and Calabrese, 2006b). We manuscript. characterize the effect of proctolin on the strength and short- Correspondence should be addressed to Farzan Nadim, Department of Biological Sciences, Rutgers University, 195 University Avenue, Newark, NJ 07102. E-mail: [email protected]. term dynamics of the two components of the LP to PD synapse DOI:10.1523/JNEUROSCI.3624-11.2011 separately. The graded component of this synapse, which de- Copyright © 2011 the authors 0270-6474/11/3113991-14$15.00/0 presses in control conditions (Manor et al., 1997), is enhanced 13992 • J. Neurosci., September 28, 2011 • 31(39):13991–14004 Zhao et al. • Neuromodulation of Synaptic Dynamics and can show facilitation in proctolin, while the spike-mediated component is also strengthened by proctolin. To mea- sure the combined effect of proctolin, we record voltage waveforms of the LP neu- ron during ongoing activity and use these realistic waveforms in the voltage- clamped LP neuron to unmask the contri- bution of these changes to total synaptic output in biologically realistic conditions. Finally, using the dynamic clamp tech- nique to modify the synaptic current, we show that proctolin reduces variability in pyloric oscillations through its modula- tion of the LP to PD synapse. Figure 1. Proctolin enhances the pyloric rhythm. A, Top, Schematic diagram of the stomatogastric nervous system. The paired Materials and Methods commissural ganglia (CoGs) and oesophageal ganglion (OG) contain modulatory projection neurons that send axons to the STG Preparation and identification of the neurons. throughthestomatogastricnerve(stn).Bottom,Simplifieddiagramofthepyloricnetworkshowsthepacemakergroupconsisting Experiments were conducted on the STNS of of the AB, PD, and LPG neurons coupled strongly with electrical synapses (gap junctions) and synaptically inhibiting the follower male crabs Cancer borealis. Animals were ob- neuronLP.TheLPneuroninturninhibitsthetwoPDneurons,producingareciprocallyinhibitorysubnetwork.B,Intracellulartraces tained from local markets and maintained recorded in the normal ongoing pyloric rhythm with intact descending neuromodulatory inputs show the rhythmic alternation of in filtered, recirculating seawater tanks at thePDandLPneurons(Control).BlockingorcuttingthestnremovesalldescendingneuromodulatoryinputtotheSTGanddisrupts Ϫ Ϫ6 10 12°C. The STNS was dissected out using the pyloric rhythm (Decentralized). Bath application of 10 M proctolin recovers the pyloric rhythm, increases the amplitude standard procedures (Blitz et al., 2004; Tohidi of the slow-wave oscillations in the PD and LP neurons and increases the spike frequency and number of spikes per burst (Procto- and Nadim, 2009). Briefly, the complete iso- lin). Line segments indicate the baselines for the membrane oscillations of PD (Ϫ56 mV) and LP (Ϫ59 mV) recorded in Control. lated STNS [including the stomatogastric gan- stn, Stomatogastric nerve, lvn, lateral ventricular nerve, lpn, lateral pyloric nerve; pdn, pyloric dilator nerve. glion (STG), the oesophageal ganglion (OG), and the paired commissural ganglia (CoG); noted in Results), as well as realistic waveforms of different amplitudes Fig. 1A] was pinned down on a Sylgard-coated Petri dish. The STG was and frequencies. Application of realistic waveforms for synaptic mea- desheathed to facilitate penetration of the pyloric neuron cell bodies. All surements was done according to methods we have previously described Ϫ preparations were continuously superfused with chilled (10 13°C) (Mamiya et al., 2003; Tseng and Nadim, 2010). Graded synaptic re- physiological Cancer saline containing (in mM): 11 KCl, 440 NaCl, 13 sponses were used to measure synaptic input–output relationships ϭ CaCl2, 26 MgCl2, 11.2 Trizma base, 5.1 maleic acid, pH 7.4–7.5. Proc- ϩ Ϫ which were fit with Boltzmann-type equations 1/(1 exp ((VLP tolin (Sigma-Aldrich) was dissolved as stock solution in distilled water to V )/k )). Ϫ3 half half a final concentration of 10 M, divided into aliquots and frozen at In almost all recordings, the amplitude of the graded IPSP (gIPSP) did Ϫ 20°C. The final concentration was made by dissolving the stock solu- not change subsequent to the fourth pulse and therefore we refer to the tion
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